Amandine Germon

Docteur De

Montpellier De

Supagro

Soutenue Par Amandine

Germon Le

Jean-Paul Laclau

Christophe Jourdan

Professeur Jean-Christophe Domec

Professeur Daniel Epron

Professeur, ESALQ José Leonardo Gonçalves

Catherine Roumet

Alain Pierret

Invitée Invité

Thèse Pour

Obtenir Le

Montpellier Supagro

Germon Le 21 Juin

Sous La

Rapporteur Examinateur

Antonio Ciro

José Leonardo Rosolem

Gonçalves

Alexia Stokes

Agnès Robin

Lydie Chapuis-Lardy

Ciro

Amaral Guerrini

Magali Ribeiro

Dona Ines

! Agradecimentos

A Eder Gilmar

Éder Araújo

Dorrival Pires De Arruda

Tiara Moraes Guimarães

Bernard « Bb »

Didou Alain Komi

Anne-Laure Carlos

Claude

Gabrielle Louis

Tiphaine Isabelle Raphael

Pierro, Babychou, Guybou, Ti poulet, Katou ! Elodie

Mes

Germon

water table in Eucalyptus grandis stands conducted in coppice in a throughfall-exclusion experiment

Consequences of clear-cutting on the production of fine roots, CO2, CH4 and N2O down to the water table in

Eucalyptus grandis stands conducted in coppice in a throughfall-exclusion experiment.

A plusieurs reprises durant ces années de thèse je me suis rappelé à quel point j'avais de la chance d'avoir mes encadrants, une association tellement efficace et complémentaire, que je n'aurai changé pour rien au monde ! Mes premiers mots vont à Jean-Paul Laclau, à qui je dois tant ! Jean-Paul je pourrai écrire une thèse entière rien que pour te dire à quel point je t'en suis reconnaissante ! Merci pour toute la patience et la disponibilité que tu as eu à mon égard et surtout tous ses judicieux conseils qui ont contribué à alimenter ma réflexion et mon travail. Merci pour les connaissances que tu m'as transmises, ta gentillesse, ta modestie et ta disponibilité à toute épreuve (même les dimanches et jours fériés !). Tu es pour moi un modèle d'inspiration permanent ! C'est un réel privilège d'avoir travaillé aux côtés d'une personne comme toi qui maitrise autant l'aspect humain que professionnel.

Je remercie de tout coeur Christophe Jourdan. Si tu ne m'avais pas « adopté » en master puis sorti de la chikungunya je n'aurais jamais fait de thèse ! Merci infiniment de m'avoir fait découvrir le monde des racines ! Merci de m'avoir expliqué des concepts que je ne maitrisais pas et fait en sorte que ce monde devienne le mien ! Merci pour ta patience, pour ta bonne humeur perpétuelle, pour avoir été à l'écoute quand j'en avais besoin et pour m'avoir encouragé quand mon moral commençait à faiblir. Je n'oublierai jamais tout ce que tu m'as appris et tacherai d'en faire bon usage. Du fond du coeur merci ! Je tiens ensuite à remercier Agnès Robin, il y a tellement de choses à dire que je ne sais même pas par quoi commencer ! Agnès ton arrivée au Brésil a changé le cours de ma thèse ! Merci d'avoir fédéré ce groupe du brésil et d'avoir simplifié à ton dépend beaucoup de choses pour nous. Merci de m'avoir considérée à la fois comme ton étudiante, ta collègue et ton ami ! Merci pour ton soutien éternel. Si j'ai évolué au cours de ces dernières années c'est en grande partie grâce à toi ! Je n'oublierai jamais tout ce que nous avons vécu ensemble et tout ce que tu m'as apporté ! #coeurcoeurcoeur à l'infini ! Merci également à Lydie Chapuis-Lardy de m'avoir guidée avec bienveillance, sans faille, pour les conseils et encouragements tout au long de ma thèse. Merci pour le temps que tu as pu dégager que ce soit pour la mise en place des manips, les mails de dernière minute ou les skypes Et puis of course les amis de Montpel : Maxou tellement de supers moments ensemble que tu serais presque indispensable, Esther comment dire : Love to Love for ever : Un cadeau du ciel ! Damichou ton surnom te va tellement bien : la bonté incarnée !, Anne, Patoche, Nancy, Simon,

RESUME

Les racines fines jouent un rôle majeur dans le cycle global du carbone, en assurant l'absorption d'eau et de nutriments nécessaire à la croissance des plantes ainsi qu'au travers de flux de carbone souterrains. Améliorer notre compréhension de la dynamique spatio-temporelle des racines fines et des gaz à effet de serre dans les couches profondes du sol est un élément clé pour identifier des pratiques sylvicoles plus durables pour les forêts plantées dans un contexte de changement climatique et pour améliorer les modèles biogéochimiques actuels. Cette étude visait à évaluer l'effet de la coupe des arbres et de la sécheresse sur la production de racines fines et la production de CO2, N2O et CH4 dans des profils de sol très profonds en plantation d'Eucalyptus conduite en taillis au Brésil. Les racines fines, d'un diamètre inférieur à 2 millimètres, ont été échantillonnées jusqu'à une profondeur de 17 m sur un dispositif d'exclusion de pluie comparant des peuplements soumis à une exclusion de 37% des pluies (-W) et des peuplements sans exclusion (+ W). La dynamique des racines a été étudiée à l'aide de minirhizotrons installés dans deux fosses permanentes d'une profondeur de 17 m dans les traitement -W et + W, pendant un an avant la coupe des arbres, puis pendant deux ans en taillis, et jusqu'à 4 m de profondeur dans un peuplement non récolté (NH) servant de témoin. Les efflux de CO2, CH4 et N2O à la surface du sol ont été mesurés durant trois ans dans les traitements -W, + W et NH. Les concentrations en CO2, CH4 et N2O dans le sol ont été mesurées à partir de fosses permanentes jusqu'à une profondeur de 15.5 m dans les traitements -W, + W et NH durant 3 mois avant la coupe des arbres et 1.5 ans après la coupe, en taillis. La croissance des racines fines était considérable à grande profondeur (> 13 m) chez les arbres menés en taillis et, étonnamment, la mortalité des racines fines était extrêmement faible quelle que soit la profondeur et le traitement. La biomasse totale de racines fines jusqu'à 17 m de profondeur était de 1266 et 1017 g m -2 dans les traitements -W et +W, respectivement, 1.5 an après la coupe des arbres et de 1078 g m -2 dans le traitement NH, 7.5 ans après la plantation. La longueur spécifique et la surface spécifique des racines fines étaient environ 15% plus élevées dans les peuplements -W que dans les peuplements +W. Les émissions de CO2, CH4 et N2O à la surface du sol ne différaient pas significativement entre -W et + W et ne changeaient pas après la coupe des arbres dans les peuplements menés en taillis par rapport aux peuplements non exploités. Alors que les concentrations en CO2 et CH4 augmentaient fortement avec la profondeur, les concentrations en N2O étaient pratiquement constantes de la surface du sol jusqu'à une profondeur de 15.5 m. Les concentrations moyennes en CO2 et en N2O dans les sols -W étaient respectivement inférieures de 20.7% et 7.6% à celles dans les sols +W et les concentrations en CH4 dans les sols -W étaient de 44.4% supérieures à celles dans les sols +W. Un modèle de diffusivité a montré que les productions de CO2, N2O et CH4 étaient similaires dans les traitements + W, -W et NH. Les fortes différences de concentrations en CO2, CH4 et N2O dans les sols entre les traitements s'expliquaient principalement par des différences de proportion de la porosité du sol occupée par l'eau. La coupe des arbres n'a pas augmenté les émissions de CO2, de CH4 et de N2O, quel que soit le régime hydrique. La mise en place de systèmes racinaires profonds dans les forêts tropicales plantées pourrait permettre aux arbres de résister aux périodes de sécheresse attendues dans un contexte de changement climatique. Notre étude réalisée dans des peuplements d'eucalyptus gérés en taillis, représentatifs de vastes zones tropicales, suggère que les émissions de gaz à effet de serre pourraient être peu influencées par les modifications de régimes de précipitations dus au changement climatique.

Mots clés : Brésil, Eucalyptus grandis, croissance racinaire en profondeur, gaz à effet de serre, exclusion de pluie, sol tropical très profond, taillis

RESUMO

Melhorar nossa compreensão sobre a dinâmica espaço-temporal de raízes finas e dos gases de efeito estufa em camadas profundas do solo é um componente chave para identificar práticas silviculturais mais sustentáveis para florestas plantadas num contexto de mudança climática e para melhorar os atuais modelos biogeoquímicos. Nosso estudo teve como objetivo avaliar o efeito do corte raso e da seca na produção de raízes finas, nos efluxos de CO2, CH4 e N2O do solo e da produção ao longo dos perfis profundos do solo até o lençol freático nas plantações de eucalipto manejadas em talhadia. A raízes finas (diâmetro <2 mm) foram amostradas até 17 m de profundidade num experimento de exclusão de chuva comparando parcelas com 37% de precipitação excluída (-W) e sem exclusão de chuva (+ W). A dinâmica das raízes foi estudada usando minirhizotron em duas trincheiras permanentes até 17 m de profundidade nos tratamentos -W e + W, durante 1 ano antes do corte raso e 2 anos depois do corte em talhadia, e tambem até 4 m de profundidade numa parcela sem corte (NH), servindo como controle. Os efluxos de CO2, CH4 e N2O na superfície do solo foram medidos ao longo de três anos utilizando o método de câmara manual nos tratamentos -W, + W e NH. As concentrações de CO2, CH4 e N2O no solo foram medidas a partir das trincheiras até uma profundidade de 15.5 m nos tratamentos -W, + W e NH durante 3 meses antes do corte raso e 1.5 ano depois em talhadia.

Após o corte, ocorreu um grande crescimento radicular das árvores conduzidas em talhadia nas camadas muito profundas do solo (> 13 m) e, surpreendentemente, a mortalidade das raízes permaneceu extremamente baixa, independentemente da profundidade e do tratamento. A biomassa total de raízes finas em talhadia até 17 m de profundidade foi de 1266 e 1017 g m -2 em + W e -W, respectivamente, 1.5 ano após o corte raso, e 1078 g m -2 em NH 7.5 anos após o plantio. O comprimento específico e a área específica das raízes foram cerca de 15% maiores em -W do que em + W. Os efluxos de CO2, CH4 e N2O não foram significativamente diferentes entre -W e + W e não alteraram após o corte raso nas parcelas manejadas por talhadia em comparação com o povoamento não colhido. As concentrações de CO2 e CH4 aumentaram muito com a profundidade e as concentrações de N2O permaneceram aproximadamente constantes na superfície do solo até uma profundidade de 15.5 m. As concentrações médias de CO2 e N2O em -W foram 20.7% e 7.6% menores que em + W, respectivamente, e as concentrações de CH4 em -W foram 44.4% maiores que em + W em todo o perfil de solo. Um modelo de difusividade mostrou que a produção e o consumo de CO2, N2O e CH4 ocorreram em grandes profundidades e foram similares nos tratamentos + W, -W e NH. O corte raso não aumentou os efluxos e as produções de CO2, CH4 e N2O, independentemente do regime de abastecimento de água.

O estabelecimento de sistemas radiculares profundos em florestas tropicais plantadas pode ajudar as árvores a resistir aos longos períodos de seca esperados pelas mudanças climáticas em muitas regiões tropicais. Nosso estudo sugeriu que o manejo em talhadia pode ser uma opção interessante nas plantações tropicais de eucalipto para melhorar a tolerância das árvores à seca e armazenar carbono em grande profundidade no solo. As conseqüências das mudanças climáticas nas emissões de gases de efeito estufa podem ser menores quando as plantações tropicais de eucaliptos são manejadas em talhadia.

Palavras-chave: Brazil, Eucalyptus grandis, crescimento de raízes profundas, gases de efeito estufa, exclusão de chuvas, solo tropical muito profundo, talhadia

RESUMO ESTENDIDO EM PORTUGUES

Introdução

O crescimento das árvores é altamente dependente da função de absorção das raízes finas para a água e os nutrientes. Raízes finas também desempenham um papel importante no ciclo global de carbono (C), principalmente nos processos de produção, respiração, exsudação e decomposição. Melhorar a compreensão da dinâmica espaço-temporal de raízes finas ao longo de todo o perfil do solo até o lençol freático é importante para identificar práticas silviculturais mais sustentáveis para as florestas plantadas. Após uma forte expansão nos últimos 20 anos, as plantações florestais representam 7% da área florestal total do mundo (Keenan et al., 2015).

Em regiões tropicais e subtropicais, as plantações industriais de eucalipto de rápido crescimento, participam no armazenamento de carbono atmosférico e ajudam a reduzir a exploração das florestas naturais fornecendo um proporção crescente da demanda mundial em madeira (Keenan et al., 2015). As plantações de eucalipto de rápido crescimento cobrem cerca de 20 milhões de hectares em todo o mundo (Booth, 2013), incluindo cerca de 5.67 milhões de hectares no Brasil (IBA, 2016). As florestas tropicais têm uma forte influência nas concentrações de dióxido de carbono (CO2), óxido nitroso (N2O) e metano (CH4) na atmosfera.

As práticas silviculturais nas florestas plantadas afetam os fluxos de gases de efeito estufa na superfície do solo e os principais determinantes da produção de gases de efeito estufa nos solos florestais (substrato, temperatura, teor de água) variam em função da profundidade do solo. No Brasil, a maioria das plantações de eucalipto são estabelecidas em solos com baixa fertilidade e submetidas a períodos de seca de até 6 meses (Gonçalves et al., 2013). Apesar das projeções sobre o futuro das precipitações ainda sejam difíceis de prever em nível local, estudos mostraram que o aquecimento global será associado a uma intensificação das estações secas em muitas partes do globo (Solomon et al., 2009). especialmente em regiões subtropicais já sujeitas a secas severas [START_REF] Meehl | Global climate projections[END_REF]. Neste contexto, o manejo do Eucalyptus através da talhadia tem sido praticado por empresas do setor florestal no Brasil e pode ser uma vantagem contra o estresse hídrico, uma vez que as brotações do Eucalyptus já possuem um sistema radicular formado em camadas profundas, onde as quantidades de água disponíveis podem ser maiores.

As conseqüências do corte raso das árvores na dinâmica radicular no primeiro ano de rotação de plantações em talhadia implicam questões específicas nunca estudadas nas camadas profundas do solo. Além disso, o corte da parte aérea das árvores tem um impacto significativo na saída de carbono do ecossistema e nas emissões de gases de efeito estufa. Após o corte, a mortalidade das raízes leva à um suprimento de matéria orgânica fresca em diferentes profundidades (Berhongaray et al., 2015). A decomposição da matéria orgânica fresca pode promover a degradação da matéria orgânica existente (Fontaine et al., 2007;Derrien et al., 2014) com um "efeito priming" (Kuzyakov et al., 2000). O "efeito priming" pode afetar o armazenamento de carbono pelo ecossistema e afetar indiretamente o ciclo do nitrogênio. Existe pouca pesquisa sobre os ciclos biogeoquímicos em plantações florestais manejadas em talhadia, e nenhuma comparando experimentalmente estresse hídrico (exclusão de chuva) e precipitação normal. A avaliação da contribuição das raízes finas profundas e da dinâmica espaço-temporal das concentrações de gases de efeito estufa nas camadas profundas do solo é um verdadeiro desafio metrológico e uma grande barreira científica, a qual é importante levantar para estudar a sustentabilidade das plantações florestais e sua resiliência no contexto das mudanças climáticas globais. O objetivo principal da tese é avaliar o efeito do corte e da redução de chuva na produção das raízes finas, CO2, CH4 e N2O ao longo do perfil do solo até o lençol freático.

Estes efeitos foram acompanhados antes e após o corte raso das árvores em uma plantação de Eucalyptus grandis conduzida em talhadia e submetida à dois regimes hídricos contrastantes.

Os objetivos específicos da tese são:

-Melhorar a compreensão da influência das chuvas sobre a mortalidade e a produção de raízes finas em função da profundidade do solo em plantações conduzidas por talhadia; -Avaliar o efeito do corte raso e do manejo em talhadia sobre a dinâmica das raízes finas até 17 m de profundidade; -Avaliar a dinâmica de raízes finas, CO2, CH4 e N2O próxima ao lençol freático (17 m de profundidade) em tratamentos com dois níveis de pluviosidade contrastantes; -Determinar o perfil vertical das taxas de produção de CO2, CH4 e N2O a partir da superfície até uma profundidade de 17 m, através de amostragens dos gases, seguida de análises por cromatografia gasosa e modelagem da produção e do transporte no solo.

Estratégia de pesquisa

Os experimentos deste doutorado ocorreram no Brasil, na Estação Experimental de Itatinga (Estado de São Paulo), destinada à descrição, quantificação e modelagem do funcionamento dos ecossistemas florestais tropicais. A precipitação média anual nesta área é de 1390 mm; a vegetação dominante é o eucalipto; o solo é muito profundo (> 15m) do tipo arenoso ferralítico (Laclau et al., 2010). Uma plantação de Eucalyptus grandis de mais de dois hectares foi instalada em 2010 em um delineamento em parcelas subdivididas (split-plot) com 3 blocos. O principal fator estudado é a redução da chuva e o fator secundário é a fertilização potássica. O trabalho de tese concentra-se em modalidades com adubação potássica não limitante como em plantações comerciais no Brasil, comparando chuvas não perturbadas e exclusão parcial por um sistema de calhas para coletar e excluir 37% das chuvas.

Duas trincheiras profundas (17 m de profundidade x 1.5 m de diâmetro) foram escavadas no início de 2014 em tratamentos com e sem exclusão de chuva e estão equipadas com plataformas que facilitam a manipulação e medições em profundidades diferentes.

As árvores foram cortadas no experimento em junho de 2016, com a idade de 6 anos, e a plantação foi conduzida em talhadia após o corte raso. No entanto, uma parcela de referência (NH) foi mantida com as árvores existentes (fertilização e chuvas não perturbadas). Nesta parcela, uma terceira trincheira de 3 m de profundidade foi escavada e preparada.

Desde sua criação em 2014, as duas trincheiras profundas foram equipadas com minirhizotrons para monitorar a dinâmica das raízes (Maeght et al., 2013). Vinte e quatro tubos transparentes de 180 cm de comprimento foram instalados a 45° dentro das trincheiras permanentes (12 por trincheira) e permitiram a observação das raízes 130 cm abaixo de cada ponto de instalação (na superfície, 1.0, 3.5, 5.5, 7.5, 9.5, 11.5, 13.5 e 15.5 m). Sete tubos foram instalados na parcela de referência (superfície, 1 e 3.5 m).

A observação das raízes foi realizada por aquisição de imagem por meio de um scanner circular (CI-600 Root Growth Monitoring System, CID, EUA). Oito imagens (21.59 cm x 19.56 centímetros) no tubo foram tomadas a cada duas semanas desde Maio de 2015: um ano antes do corte das árvores e durante 2 anos após o corte das árvores, em Junho de 2016. As imagens foram analisadas usando o software WinRHIZOtron (Regent, Canadá) para traçar as raízes, marcando o comprimento e diâmetro para estimar o crescimento ao longo do tempo.

Raízes finas (diâmetro <2 mm) foram amostradas até a profundidade de 17 m para estimar a biomassa (raízes vivas) e necromassa em todo o perfil do solo, 1.5 anos após o corte nos tratamentos + W, -W e 7.5 anos após o plantio no tratamento NH.

As emissões de gases do solo foram medidas colocando um sino (diâmetro de 40 cm, altura de 10 cm) sobre uma base de amostragem instalada no local experimental. Quatro câmaras foram colocadas aleatoriamente à quatro distâncias das árvores em cada tratamento. As câmaras foram fechadas cada vez por 30 minutos. Uma alíquota de ar ambiente foié coletada com uma seringa quatro vezes consecutivas (0, 10 min, 20 min e 30 min) após o fechamento. As medições foram feitas a cada duas semanas: três meses antes do corte e 1.5 anos após o corte. Câmaras de respiração no solo (9 por tratamento e bloco) também foram conectadas à um analisador Li-Cor 8100 (Li-cor, Lincoln, Ne, EUA) para monitorar as emissões de CO2 na superfície do solo medido a cada duas semanas. Para coletar regularmente os gases do solo (duas vezes por mês: três meses antes do corte e 1.5 anos após o corte), as trincheiras foram equipadas com seringas instaladas em profundidades (Metay et al., 2007) também cobertas por imagens de minirhizotrons (0.1, 0.5, 1.0, 3.5, 7.5, 11.5 e 15.5 m). As concentrações dos gases foram determinadas por cromatografia gasosa (GC-ECD). Os dados foram aplicados à um modelo de difusividade para estimar os fluxos de CO2, N2O e CH4, bem como a produção de cada camada de solo a partir das concentrações medidas nas trincheiras.

Principais resultados

O sistema de redução de chuva implantado resultou em uma diminuição significativa do conteúdo de água do solo, em média uma redução de 12.9% em -W em comparação ao + W, da superfície a uma profundidade de 16 m. Este dispositivo mostrou-se eficaz para estudar dois regimes de precipitação contrastante. Após o corte das árvores houve uma interrupção da transpiração da parte aérea, e consequentemente o solo foi recarregado com água. O teor de água no solo foi menor no tratamento -W em relação ao tratamento + W antes do corte, essa diferença entre os dois tratamentos persistiu um ano e meio após o corte.

Em primeiro lugar investigamos o impacto da redução de chuvas e do corte raso das árvores na dinâmica radicular em uma plantação de eucalipto conduzida em talhadia. Nossos resultados mostraram que as taxas diárias de crescimento radicular foram fortemente dependentes da profundidade e da estação nos tratamentos + W e -W. Após o corte das árvores, o crescimento de raízes finas começou nas camadas superiores do solo e foi crescendo ao longo do tempo em profundidade em ambos os tratamentos + W e -W. Assim, quando a plantação é conduzida em talhadia, após o corte das árvores, o início do crecimento radicular foi observado pela primeira vez 6 meses após o corte na superfície. Na profundidade 3.5-4.8 m do solo 12 meses após o corte e na profundidade 13.5-14.8 m do solo 16 meses após o corte, nos tratamentos + W e -W.

As taxas diárias de crecimento alongamento das raízes atingiram o pico no final da estação seca para todas as camadas do solo nas profundidades > 6 m, quando o teor de água no solo diminuiu nas camadas superficiais. Assim, os valores diários de alongamento das raízes não foram necessariamente correlacionados com os níveis de umidade do solo para uma dada camada de solo. Observamos uma sincronização entre a diminuição da quantidade de água extraível na camada superficial e os picos de alongamento das raízes após o corte no tratamento -W. Além disso, vimos que a densidade das raízes finas reduz abaixo de 20 cm de profundidade, depois diminui gradualmente até o lençol freático nos três tratamentos NH, + W e -W. A biomassa total de raízes finas em talhadia até 17 m de profundidade foi de 1266 e 1017 g m -2 em + W e -W, respectivamente, 1.5 ano após o corte raso, e 1078 g m -2 em NH 7.5 anos após o plantio. A densidade de raízes finas foi cerca de 25% maior em -W do que em + W e NH na maioria das camadas do solo. Em profundidades > 7 m, as densidades de raízes finas foram pelo menos duas vezes maiores em -W que em + W e NH, respectivamente.

Além disso, estávamos também interessados no efeito da redução de chuva sobre a adaptação morfológica das raízes finas em todo o perfil do solo. Nos tratamentos NH, + W e -W, mostramos que a profundidade teve pouco efeito no comprimento específico das raízes (SRL), na área específico das raízes (SRA) e no diâmetro das raízes finas. SRL e SRA foram significativamente maiores em -W que em + W, e valores semelhantes foram observados em + W e NH. Até 17 m de profundidade, os valores médios de SRL foram 28.8, 30.6 e 34.4 m g -1 , os valores médios de SRA de 258.8, 267.5 e 305.3 cm 2 g -1 e os diâmetros médios das raízes finas de 0.31, 0.32 e 0.36 mm nos tratamentos NH, + W e -W, respectivamente. Durante todo o período de estudo (3 anos) o comprimento acumulado de raízes mortas representou 6-7% do comprimento total de raízes produzido em todo o perfil do solo até 17 m de profundidade em ambos os tratamentos W e -W. Surpreendentemente, o comprimento das raízes finas mortas não aumentou após o corte raso das árvores e não diferiu entre as profundidades do solo e entre os tratamentos + W e -W.

Em seguida, analisamos o impacto do corte raso das árvores e da redução da precipitação nas emissões de gases de efeito estufa, bem como sua produção / consumo em todo o perfil do solo.

Os fluxos cumulativos de CO2 medidos nos tratamentos + W e -W foram 136.5 ± 21.8 mol m - 2 e 130.3 ± 24.8 mol m -2 ano -1 no último ano antes do corte raso das árvores e 108.0 ± 15.8 e 119.3 ± 22.5 mol m -2 ano -1 no primeiro ano após o corte raso quando a plantação foi conduzida em talhadia. Não encontramos diferenças significativas entre as emissão de CO2, CH4 e N2O entre os dois tratamentos + W e -W. Os fluxos de CH4 foram negativos ao longo do período de estudo, de março de 2016 a dezembro de 2017, indicando um consumo líquido de CH4 atmosférico pelo solo. Não foram observadas diferenças significativas entre os tratamentos NH e + W nas emissões de CO2, CH4 e N2O mostrando nenhum efeito do corte das árvores.

Os efluxos de CO2, CH4, e N2O não foram significativamente diferentes entre -W e + W e não mudaram após o corte das árvores nas parcelas manejadas em talhadia comparado às parcelas sem corte raso. As concentrações de CO2 e CH4 aumentaram significativamente com a profundidade e as concentrações de N2O permaneceram constantes da superfície a uma profundidade de 15.5 m. As concentrações médias de CO2 e N2O em -W foram, respectivamente, inferior de 20.7% e 7.6% a os de +W e as concentrações de CH4 foram 44.4% superior em -W do que em + W sobre a totalidade do perfil do solo. O modelo de difusividade mostrou que a produção e o consumo de CO2, N2O e CH4 ocorreu em grandes profundidades e foram semelhantes nos tratamentos + W, W, e NH. O corte raso das árvores não aumentou os efluxos e as produções de CO2, CH4 e N2O independentemente do regime de água.

As produções de CO2, CH4, e N2O entre 0.1 e 15.5 m de profundidade, não foram significativamente diferentes entre + W e -W. As produções mais elevadas de CO2 e N2O e a menor produção de CH4 foram estimadas na superficie do solo devido ao forte gradiente de concentrações e a maior difusividade efetiva calculada na camada superficial do solo. A produção de CO2 e N2O e o consumo de CH4 ocorreu principalmente na superfície e uma parte da produção de CO2 e CH4 atingiu uma profundidade de até 15.5 m.

Discussão geral

A principal novidade dos nossos resultados está na primeira observação direta da fenologia das raízes finas, bem como nas primeiras medições in situ das concentrações de CO2, N2O e CH4 em profundidades à mais de 10 m em uma plantação de eucalipto conduzida em talhadia. As conseqüências do corte raso das árvores e da redução das chuvas na dinâmica da produção de raízes finas e dos gases de efeito estufa em plantações florestais levantam questões específicas que nunca foram estudadas em um perfil de solo profundo em clima tropical.

Efeito da redução de chuva

Diante de uma seca induzida, o eucalipto aumentou a densidade de raízes finas em grande profundidade. O crescimento das raízes em camadas profundas do solo pode aumentar a quantidade de água disponível necessária para o crecimento das árvores, o que poderia ser um benefício crítico para as árvores em condições severas de seca (Christina et al., 2017). Após o corte, observou-se um grande crescimento das raízes à mais de 4 m de profundidade no final da temporada seca, independentemente do tratamento. O crescimento das raízes finas nas camadas profundas do solo começou quando o teor de água na camada de 0-2 m caiu abaixo de um limiar de cerca de 80 mm, sugerindo que o teor de umidade no solo, em uma determinada camada do solo, não foi o principal fator responsável pelo crescimento das raízes finas. Sucessivos afrouxamentos no crescimento radicular da superfície do solo para suas camadas mais profundas, no final da temporada seca e nos primeiros meses após o início da temporada chuvosa nos tratamentos + W e -W, seria devido ao rápido esgotamento dos recursos hídricos superficiais, o que induziria as raízes das árvores a buscarem as camadas mais profundas do solo (Schenk and Jackson, 2002;Billings, 2015).

Além disso, mostramos que os eucaliptos em condições de seca adaptaram sua morfologia radicular para maximizar a superfície das raízes em contato com o solo para absorver os recursos limitados. Os valores de SRL e SRA foram maiores em -W que em + W, o que combinado com maiores densidades de raízes finas levaria à um índice de superfície de raiz muito maior. Nosso estudo mostrou que o eucalipto pode modificar as características das raízes finas para melhorar a captura de recursos e a exploração de camadas muitas profundas do solo, a fim de sua sobrevivência em um contexto de mudanças climáticas ajudando assim, a manter a absorção de água durante períodos secos (Brunner et al., 2015;Christina et al., 2017).

A exclusão da chuva não teve efeito nos fluxos de CO2, N2O e CH4 medidos na superfície ou calculados em profundidade com um modelo de difusividade. As diferenças na concentração de gás no solo, medidas entre + W e -W, são provavelmente devido ao maior teor de água do solo em + W que poderia reduzir a difusividade dos gases, enquanto as emissões não foram afetadas. No tratamento + W, o alto teor de água no perfil do solo pode induzir a saturação do espaço intersticial pela água e causar uma lenta difusão dos gases de efeito estufa para a atmosfera (Maier et al., 2017;Wang et al., 2018). A estrutura de poros e agregados do solo está diretamente relacionada à liberação de gases de efeito estufa, mas também ao armazenamento de carbono [START_REF] Smith | Siberian peatlands a net carbon sink and global methane source since the early Holocene[END_REF][START_REF] Mangalassery | The effect of soil aggregate size on pore structure and its consequence on emission of greenhouse gases[END_REF].

As produções de CO2, CH4 e N2O não foram significativamente diferentes entre os tratamentos + W e -W até uma profundidade de 15.5 m. No entanto, observamos que a produção pode diminuir nas camadas superiores e aumentar nas camadas profundas. Nós mostramos que a biomassa de raízes e o índice de área de raiz aumentaram em aproximadamente 25% e 24%, respectivamente, no tratamento de exclusão de chuva comparado com a parcela de controle a uma profundidade de 17 m, e que a biomassa das raízes aumentou principalmente nas profundidades > 7 m. Portanto, a mudança nas produções de CO2 nas camadas mais profundas observadas em nosso estudo pode ser devido à uma mudança nas atividades das raízes para horizontes mais profundos, indicando um aumento da captação de água na profundidade pelas raízes (Sotta et al., 2007;[START_REF] Schwendenmann | Effects of an experimental drought on the functioning of a cacao agroforestry system, Sulawesi, Indonesia[END_REF].

Também observamos uma mudança no consumo de CH4 nas camadas profundas no tratamento de exclusão de chuva. A mudança no consumo de CH4 para camadas mais profundas pode ser devido às condições do solo mais favoráveis à metanotrofia, mas menos à metanogênese. Mais estudos são necessários para avaliar os efeitos da exclusão de chuva nas comunidades microbianas, suas atividades e interações, e particularmente nas camadas profundas do solo.

Efeito do corte raso das árvores

Descobrimos que poucas raízes foram perdidas pela mortalidade (<10% de todas as raízes observadas ao longo de 3 anos), sugerindo que a maior parte do sistema radicular permanece funcional após o corte raso das árvores conduzidas em talhadia. O nosso estudo sugere que árvores de Eucalyptus grandis de 6 anos de idade têm reservas suficientes no sistema radicular e que as condições apropriadas do solo para manter a biomassa radicular estabelecida até o lençol fréatico após o corte tenha, provavelmente, também contribuído para o crescimento inicial das rebrotas (Drake et al., 2013;Brunner et al., 2015).

A assincronia no sistema radicular, atrasando o crescimento das raízes nas camadas mais profundas do solo poderia ser uma estratégia para maximizar a absorção de água e nutrientes necessárias para atender a alta demanda das árvores de rápido crescimento. O crescimento das raízes ocorreu a uma profundidade de 14 m em menos de um ano após o corte das árvores conduzidas em talhadia, enquanto a profundidade máxima atingida pelas raízes de E. grandis é de aproximadamente 7 m um ano após o plantio em solos muito profundos (Christina et al., 2011;Laclau et al., 2013). As raízes profundas permitem o acesso à grandes quantidades de água armazenada no subsolo após o corte e, apesar da baixa densidade de raízes finas nas camadas mais profundas do solo, são suficientes para absorver grandes quantidades de água (Christina et al., 2017). A baixa mortalidade de raízes finas após o corte sugerem que o manejo em talhadia das plantações de eucalipto pode ser uma opção promissora para lidar com a seca, uma vez que o sistema de radicular existente permite o acesso à água armazenada nos horizontes profundos.

Contrariamente às nossas expectativas, o corte das árvores não levou ao aumento de emissões e produção de CO2, CH4 e N2O, independentemente do regime hídrico. A colheita de eucaliptos em plantações manejadas em rotações curtas leva a grandes alterações no ambiente do solo, provavelmente aumentando o processo de decomposição da matéria orgânica, como o aumento da temperatura do solo e umidade do solo, bem como acúmulo de resíduos de colheita na superfície do solo (Mendham et al., 2002;O'connell et al., 2004;Rocha et al., 2016;Christina et al., 2017). Nós mostramos que o corte das árvores não levou à um aumento da mortalidade das raízes no primeiro ano após o corte, quando a plantação foi conduzida em talhadia, independentemente do regime hídrico. Portanto, assumimos que o corte raso resultando em emissões da mesma intendisidade que antes do corte das arvores em nosso experimento pode resultar de uma diminuição na respiração das raízes após a colheita, compensa-se a um aumento na decomposição da matéria orgânica na superfície do solo.

Conclusão geral

A fenologia das raízes finas do eucalipto em talhadia submetidas à regimes hídricos contrastantes revelou taxas de mortalidade muito baixas. O crescimento inicial da parte aérea após o corte das árvores beneficiou-se do sistema radicular estabelecido na rotação anterior, e o crescimento assíncrono das raízes finas com a profundidade revelou a plasticidade das árvores em resposta às condições do solo. O estabelecimento de sistemas radiculares profundos em florestas tropicais plantadas poderia ajudar as árvores a resistir aos longos períodos de seca esperados em muitas regiões tropicais num contexto de mudanças climáticas.

Além disso, mostramos que o corte raso das árvores não aumentou significativamente as emissões de CO2, N2O e CH4 quando o plantio é conduzido em talhadia em comparação com uma plantação não cortada. As emissões de gases pós-corte são consistentes com as baixas taxas de mortalidade de raízes observadas. Por outro lado, raízes profundas também poderiam contribuir para sequestrar grandes quantidades de C no solo. As alocações subterrâneas de carbono representam cerca de 20-30% da produtividade primária bruta nas plantações de eucalipto (Ryan et al., 2010;Epron et al., 2012;Nouvellon et al., 2012). O carbono das raízes é geralmente retido por mais tempo no solo do que da serapilheira, que é mais afetada por processos físico-químicos e também devido às diferenças na composição estrutural entre as folhas e as raízes (Rasse et al., 2005;Schmidt et al., 2011;Menichetti et al., 2015). Mais estudos são necessários para determinar se o manejo em talhadia das plantações de eucalipto em solos muito profundos pode ser uma opção efetiva para mitigar o aumento de gases de efeito estufa na atmosfera e aumentar o armazenamento de C no solo. Solos tropicais muito profundos cobrem grandes áreas do mundo e é fundamental aumentar nossa compreensão sobre a dinâmica espaço-temporal das concentrações de gases de efeito estufa nas camadas profundas, a fim de quantificar com mais precisão fontes / armazenamento de C para estimar o orçamento global de carbono, melhorar os atuais modelos biogeoquímicos para a previsão de emissões de gases de efeito estufa e identificar práticas silviculturais mais sustentáveis para florestas tropicais plantadas no contexto das mudanças climáticas.

RESUME ETENDU EN FRANÇAIS

Introduction

La croissance des arbres dépend fortement de la fonction d'absorption des racines fines pour l'eau et les nutriments. Les racines fines jouent également un rôle important dans le cycle global du carbone (C), principalement dans les processus de production, de respiration, d'exsudation et de décomposition. Améliorer la compréhension de la dynamique spatio-temporelle des racines fines sur tout le profil de sol jusqu'à la nappe phréatique est important pour identifier des pratiques sylvicoles plus durables pour les forêts plantées.

Après une forte expansion au cours des 20 dernières années, les plantations forestières représentent 7% de la superficie forestière totale du monde (Keenan et al., 2015). Dans les régions tropicales et subtropicales, les plantations d'essences à croissance rapide stockent de grandes quantités de carbone et contribuent à réduire l'exploitation des forêts naturelles en fournissant une proportion croissante de la demande mondiale en bois (Keenan et al., 2015).

Les plantations d'eucalyptus à croissance rapide couvrent environ 20 millions d'hectares dans le monde (Booth, 2013), dont environ 5.67 millions d'hectares au Brésil (IBA, 2016). Les forêts tropicales ont une forte influence sur les concentrations de dioxyde de carbone (CO2), d'oxyde nitreux (N2O) et de méthane (CH4) dans l'atmosphère. Les pratiques sylvicoles dans les forêts plantées affectent les efflux de gaz à effet de serre à la surface du sol parce qu'elles modifient les principaux facteurs qui déterminent la production de gaz à effet de serre dans les sols forestiers (substrat, température, teneur en eau) qui varient en fonction de la profondeur.

Au Brésil, la plupart des plantations forestières sont établies dans des zones à faible fertilité du sol et caractérisées par de longues périodes de sécheresse. Les projections climatiques futures prévoient des périodes sèches plus longues et plus fortes en Amérique du Sud (Solomon et al., 2009). Dans ce contexte, la gestion sylvicole en taillis des plantations d'Eucalyptus peut être un avantage contre le stress hydrique parce que les arbres bénéficient d'un système racinaire déjà développé et explorant les couches profondes du sol où l'eau y est plus disponible. Les conséquences de la coupe des arbres sur la dynamique des racines lors de la première année de rotation des plantations menée en taillis posent des questions spécifiques jamais étudiées, notamment sur les effets dans les couches profondes du sol. De plus, la récolte des parties aériennes des arbres a un impact important sur le bilan de carbone et les émissions de gaz à effet de serre de l'écosystème. Après la coupe, la mortalité racinaire conduit à un apport de matière organique fraiche à différentes profondeurs (Berhongaray et al., 2015). La décomposition de la matière organique fraîche peut favoriser la dégradation de la matière organique préexistante (Fontaine et al., 2007;Derrien et al., 2014) grâce à un "priming effect" (Kuzyakov et al., 2000). Le "priming effect" pourrait affecter le stockage de carbone par l'écosystème et influer indirectement sur le cycle de l'azote. Peu d'études portent sur les cycles biogéochimiques dans des plantations forestières avec une gestion sylvicole en taillis, et aucune comparant expérimentalement un stress hydrique (exclusion de pluie) et une pluviométrie non perturbée sous climat tropical. L'évaluation de la contribution des racines fines profondes et de la dynamique spatio-temporelle des concentrations de gaz à effet de serre dans les couches profondes du sol est un véritable défi métrologique et un verrou scientifique majeur qu'il est important de lever pour étudier la durabilité des plantations forestières, ainsi que leur résilience dans le contexte des changements globaux. L'objectif principal de la thèse est d'évaluer l'effet de la coupe et d'une réduction de pluie sur la production de racines fines, de CO2, de CH4 et de N2O le long du profil du sol jusqu'à la nappe phréatique. Ces effets ont été suivis avant et après la coupe des arbres dans une plantation d'Eucalyptus grandis menée en taillis, soumis à deux régimes hydrique contrastés.

Les objectifs spécifiques de la thèse sont :

-D'améliorer la compréhension de l'influence des précipitations sur la production et la mortalité des racines fines sur l'ensemble du profil de sol dans les plantations menées en taillis ; -D'évaluer l'effet de la coupe et d'une gestion en taillis sur la dynamique des racines fines jusqu'à 17 m de profondeur ; -D'évaluer la dynamique des racines fines, du CO2, du CH4 et du N2O près de la nappe phréatique (17 m de profondeur) soumis à deux niveaux de précipitations contrastés ; -Déterminer la production de CO2, de CH4 et de N2O de la surface à une profondeur de 17 m

Stratégie de recherche

Les expérimentations de ce doctorat se sont déroulées au Brésil sur la station expérimentale d'Itatinga (Etat de São Paulo). Ce site expérimental est destiné à la description, la quantification et la modélisation du fonctionnement des écosystèmes forestier tropicaux. Les précipitations annuelles moyennes sur cette zone sont de 1390 mm, la végétation dominante est l'eucalyptus, le sol est très profond (> 15m) et de type ferralitique sableux (Laclau et al., 2010). Une plantation d'Eucalyptus grandis de plus de deux hectares a été mise en place en 2010 sur un dispositif en parcelles divisées (split plot) avec 3 blocs. Le facteur principal étudié est la réduction de pluie. Les travaux de thèse se sont focalisés sur les modalités avec fertilisation potassique non limitante comme dans les plantations commerciales au Brésil, en comparant pluviométrie non perturbée et exclusion partielle par un système de gouttière permettant de récolter et d'exclure 37% des pluviolessivats.

Deux fosses profondes de 17 m de profondeur et 1.5m de diamètre ont été creusées début 2014 sur les traitements avec et sans exclusion de pluies, et équipées de paliers facilitant l'instrumentation et les mesures à différentes profondeurs.

Les arbres ont été coupés sur le dispositif en Juin 2016 à l'âge de 6 ans, et la plantation a été ensuite menée en taillis. Une parcelle de référence (NH) est toutefois maintenue avec les arbres en place (fertilisation et pluies non perturbées). Sur cette parcelle une troisième fosse de 3 m de profondeur a été creusée et instrumentée.

Depuis leur création en 2014, les deux fosses profondes ont été équipées de minirhizotrons pour le suivi de la dynamique racinaire (Maeght et al., 2013). 24 tubes transparents de 180 cm de longueur ont été installés à 45° depuis l'intérieur des fosses permanentes (12 par fosse) et permettent l'observations des racines sur 130 cm en dessous de chaque point d'installation en surface, et à 1, 3.5, 5.5, 7.5, 9 .5, 11.5, 13.5, 15.5 Les émissions de gaz à la surface du sol ont été mesurées en plaçant une cloche (diamètre 40 cm, hauteur 10 cm) sur une base de prélèvement installée sur le site expérimental. Quatre chambres ont été placées aléatoirement à quatre distances des arbres sur chaque traitement. Les chambres sont fermées pendant 30 min. Une aliquote de l'air de la chambre est collecté avec une seringue, à 4 temps consécutifs (0, 10 min, 20 min et 30 min) après la fermeture. Les mesures ont été réalisé toutes les deux semaines : 3 mois avant la coupe et 1.5 ans après la coupe. Des chambres de respiration du sol (9 par traitements et par blocs) ont également été connectées à un analyseur Li-Cor 8100 (Li-cor, Lincoln, Ne, USA) permettant le suivi des émissions de CO2 à la surface du sol, avec une mesure toutes les deux semaines. Afin de collecter régulièrement les gaz du sol, les fosses ont été équipées de micro-enceintes installées aux mêmes profondeurs que les minirhizotrons (0.1, 0.5, 1, 3.5, 7.5, 11.5 et 15.5m), et mesurées deux fois par mois depuis 3 mois avant la coupe jusqu'à 1.5 an après la coupe. Les concentrations en gaz sont déterminées par chromatographie en phase gazeuse (CPG-ECD). Un modèle de diffusivité a ensuite été utilisé à partir des données pour estimer les efflux de CO2, N2O et CH4, ainsi que la production de chaque couche de sol à partir des concentrations mesurées dans les fosses.

Principaux résultats

Le dispositif de réduction de pluie mis en place a entrainé une forte diminution du contenu en eau du sol avec en moyenne une réduction de 12.9% dans -W par rapport à +W depuis la surface jusqu'à une profondeur de 16 m. Ce dispositif s'est avéré efficace pour étudier deux régimes de précipitations contrastés. Les sols se sont rechargés en eau suite à une interruption de la transpiration de la partie aérienne après la coupe des arbres. Le contenu en eau du sol était inférieur dans le traitement -W par rapport au traitement +W avant la coupe, et cette différence a persisté un an et demi après la coupe.

Dans un premier temps, nous nous sommes intéressés à l'impact de la réduction de pluie et de

Discussion générale

Dans cette thèse, nous avons réalisé pour la première fois des mesures in situ de phénologie des racines fines et de concentrations de CO2, N2O et CH4 à des profondeurs de plus de 10 m dans une plantation d'eucalyptus menée en taillis. Les conséquences de la coupe des arbres ainsi qu'une réduction de pluie sur la dynamique de production des racines fines et des gaz à effet de serre dans des plantations menée en taillis soulèvent des questions spécifiques qui n'ont jamais étudiées auparavant sur un profil de sol profond en climat tropical.

Effet de la réduction de pluie

Face à une sécheresse induite, les Eucalyptus ont augmenté la densité de leurs racines fines en grande profondeur. La croissance des racines dans les couches profondes du sol augmente l'espace exploré par les arbres, et peut donc augmenter la quantité d'eau disponible nécessaire pour assurer leur croissance. Cet effet pourrait constituer un avantage essentiel pour les arbres en cas de sécheresse intense (Christina et al., 2017). Après la coupe, une croissance racinaire spectaculaire a été observé à plus de 4 m de profondeur à la fin de la saison sèche, peu importe le traitement. La croissance des racines fines dans les couches profondes du sol a commencé lorsque la teneur en eau dans la couche de sol de 0-2 m est tombée en dessous d'un seuil d'environ 80 mm, ce qui suggère que la teneur en eau du sol dans une couche de sol particulière n'était pas le principal facteur responsable de la croissance des racines fines. Les flushs successifs de croissance des racines de la couche superficielle jusqu'aux couches les plus profondes du sol à la fin de la saison sèche et dans les premiers mois qui ont suivi le début de la saison des pluies dans les traitements + W et -W seraient dus à un épuisement rapide des ressources en eau de la couche superficielle, qui induirait les racines des arbres à s'enfoncer plus profondément dans le sol (Schenk and Jackson, 2002;Billings, 2015).

De plus nous avons montré que les eucalyptus confrontés à la sécheresse ont adapté leur morphologie racinaire afin de maximiser la surface racinaire en contact avec le sol pour absorber les ressources limitées. Les valeurs de SRL et SRA étaient plus élevées dans -W par rapport à +W, ce qui, combiné à des densités de racines fines plus élevées, conduirait à un indice de surface racinaire beaucoup plus élevé. Notre étude a montré que les eucalyptus peuvent modifier les traits des racines fines pour améliorer la capture des ressources et l'exploration de couches de sol très profondes afin de survivre dans un contexte de changement climatique en contribuant au maintien de l'absorption d'eau pendant les périodes sèches (Brunner et al., 2015;Christina et al., 2017).

De plus, l'exclusion de pluie n'a eu aucun effet sur les efflux de CO2, N2O et CH4 mesurés à la surface ou calculés en profondeur avec le modèle de diffusivité. Les différences de concentration de gaz dans le sol, mesurées entre +W et -W proviennent probablement de la teneur plus élevée en eau dans le sol en +W, ce qui pourrait par la suite réduire la diffusivité des gaz du sol alors que les émissions n'ont pas été affectés. Dans le traitement +W, la teneur élevée en eau dans le profil de sol pourrait induire une saturation de l'espace interstitiel par l'eau et entraîner une lente diffusion des gaz à effet de serre vers l'atmosphère (Maier et al., 2017;Wang et al., 2018). La structure des pores et des agrégats du sol est directement liée à la libération de gaz à effet de serre mais également au stockage de carbone [START_REF] Smith | Siberian peatlands a net carbon sink and global methane source since the early Holocene[END_REF][START_REF] Mangalassery | The effect of soil aggregate size on pore structure and its consequence on emission of greenhouse gases[END_REF].

La production de CO2, de CH4 et de N2O n'était pas significativement différente entre les traitements +W et -W jusqu'à une profondeur de 15.5 m. Cependant, nous avons observé que la production peut diminuer dans les couches supérieures et augmenter dans les couches profondes. Nous avons montré que la biomasse racinaire ainsi que l'indice de surface racinaire augmentaient d'environ 25% et 24% respectivement dans le traitement d'exclusion de pluie par rapport à la parcelle témoin jusqu'à une profondeur de 17 m, et que la biomasse racinaire augmentait principalement à des profondeurs supérieures à 7 m. Par conséquent, le déplacement de la production de CO2 vers la couche plus profonde observé dans notre étude pourrait être dû à un déplacement de l'activité racinaire vers les horizons plus profond, indiquant une augmentation de l'absorption d'eau par les racines profondes (Sotta et al., 2007;[START_REF] Schwendenmann | Effects of an experimental drought on the functioning of a cacao agroforestry system, Sulawesi, Indonesia[END_REF].

Nous avons également observé un déplacement de la consommation de CH4 vers les couches profondes du traitement d'exclusion de pluie. Le déplacement de la consommation de CH4 vers les couches plus profondes pourrait être dû à des conditions de sol plus favorables à la méthanotrophie mais défavorable à la méthanogénèse. Des études complémentaires sont nécessaires pour évaluer les effets de l'exclusion de pluie sur les communautés microbiennes, leur activité ainsi que leurs interactions, en particulier dans les couches profondes du sol.

Effet de la coupe des arbres

Nous avons mis en évidence que relativement peu de racines ont été perdues par mortalité, avec moins de 10% de mortalité sur toutes les racines observées sur 3 ans, ce qui suggère que la plus grande partie du système racinaire reste fonctionnelle après la coupe des arbres quand la plantation est menée en taillis. Notre étude suggère que les Eucalyptus grandis âgés de 6 ans disposent de réserves suffisantes dans le système racinaire pour maintenir la biomasse racinaire établie jusqu'à la nappe phréatique après la coupe, ce qui a probablement contribué à la croissance précoce des rejets (Drake et al., 2013;Brunner et al., 2015).

L'asynchronisme au sein du système racinaire, retardant la croissance des racines dans les couches profondes du sol, pourrait être une stratégie employée pour maximiser l'absorption d'eau et de nutriments nécessaire pour répondre à la forte demande de ces arbres à croissance rapide. La croissance des racines s'est produite à une profondeur de 14 m moins d'un an après la coupe des arbres quand ils sont menés en taillis, tandis que la profondeur maximale atteinte par les racines de E. grandis est d'environ 7 m un an après la plantation dans des sols très profonds (Laclau et al., 2013;Christina et al., 2017). Les racines profondes permettent un accès à de grandes quantités d'eau stockées dans le sous-sol après la coupe et malgré la faible densité de racines fines dans les couches profondes du sol, elles suffisent à absorber des quantités importantes d'eau (Christina et al., 2017). Les faibles taux de mortalité des racines fines après la coupe suggèrent que la gestion en taillis des plantations d'Eucalyptus peut être une option prometteuse pour faire face à la sécheresse, étant donné que le système racinaire préexistant permet un accès à l'eau stockée dans les horizons profonds.

Contrairement à ce que nous espérions, la coupe des arbres n'a pas entraîné d'augmentation des émissions et de la production de CO2, de CH4 et de N2O, quel que soit le régime hydrique. La récolte de la biomasse aérienne entraîne une réduction de l'absorption de carbone par la photosynthèse immédiatement après la coupe, mais également des modifications substantielles de l'environnement physique du sol, telles qu'une augmentation de la température [START_REF] Smethurst | Distribution of carbon and nutrients and fluxes of mineral nitrogen after clear-felling a Pinus radiata plantation[END_REF]) et de l'humidité [START_REF] Cortina | Effects of clearfelling on forest floor accumulation and litter decomposition in a radiata pine plantation[END_REF], qui influencent les processus de décomposition. En effet, nous avons montrés que la coupe des arbres n'entraînait pas d'augmentation de la mortalité racinaire la première année après la coupe lorsque la plantation était menée en taillis. Par conséquent, nous supposons que la décomposition des racines mortes ne s'est pas accélérée après la coupe. Nous pouvons supposer que la diminution de la respiration des racines après la coupe, associée à l'augmentation de la décomposition des litières à la surface du sol se compensent, entraînant des émissions similaires à celles d'avant la coupe.

Conclusion générale

La phénologie des racines fines d'eucalyptus menée en taillis soumis à des régimes hydriques contrastés a révélé des taux de mortalité très faible. La croissance précoce des pousses après la coupe des arbres a bénéficié du système racinaire établi au cours de la rotation précédente, et l'asynchronisme de la croissance des racines fines en fonction de la profondeur a mis en évidence la plasticité des arbres en réponse aux conditions du sol. La mise en place de systèmes racinaires profonds dans les forêts tropicales plantées pourrait aider les arbres à résister aux longues périodes de sécheresse attendues dans de nombreuses régions tropicales dans un contexte de changement climatique.

De plus, nous avons montré que la coupe des arbres n'entraine pas de manière significative l'augmentation des émissions de CO2 et de CH4 quand la plantation est menée en taillis par rapport à une plantation non exploitée. Les émissions de gaz après la coupe sont cohérentes avec les faibles taux de mortalité racinaire observés. D'autre part, les racines profondes pourraient également contribuer à la séquestration de grandes quantités de C dans le sol. Les allocations de carbone vers les parties souterraines représentent environ 20 à 30% de la productivité primaire brute dans les plantations d'Eucalyptus (Ryan et al., 2010;Epron et al., 2012;Nouvellon et al., 2012). Le C des racines est généralement retenu plus longtemps dans le sol que celui de la litière aérienne, qui est davantage affectée par les processus physicochimiques et qui comporte une composition structurelle différente (Rasse et al., 2005;Schmidt et al., 2011;Menichetti et al., 2015). Des études complémentaires sont nécessaires pour déterminer si la gestion des plantations d'eucalyptus dans des sols très profonds pourrait constituer une option efficace pour atténuer l'augmentation du CO2 dans l'atmosphère et augmenter le stockage du C.

Les sols tropicaux très profonds couvrent de vastes régions du monde et il est essentiel d'améliorer notre compréhension de la dynamique spatio-temporelle des concentrations de gaz dans les couches profondes du sol afin de quantifier plus précisément les source / puits de C pour estimer le budget global du carbone, améliorer les modèles biogéochimiques actuels pour la prédiction des émissions de gaz à effet de serre, et identifier des pratiques sylvicoles plus durables pour les forêts tropicales plantées dans le contexte des changements climatiques. 3 m, 1-2.3 m, 3.5-4.8 m, 5.5-6.8 m, 11.5-12.8 m, 13.5-14.8 m and 15.5-16.8 3 m, 3.5-4.8 m, 5.5-6.8 m, 11.5-12.8 m, 13.5-14.8 m and 15.5-16.8 A) Time course of soil extractable water (mm) in soil layers 0-1 m and 1-2 m, in the -W (37% of throughfall excluded by plastic sheets) coppice of block 1, from March 2017 (10 months after the clear-cut) to December 2017. The mean daily values of soil extractable water were estimated from semi-hourly SWC measurements. B) Daily living root length production on the surface of minirhizotron tubes (cm m -2 of minirhizotron area day -1 ) estimated over the same period and same plot as a), at two-week intervals, in soil layers 0-1.3 m, 1-2.3 m, 3.5-4.8 m, 5.5-6.8 m, 11.5-12.8 m, 13.5-14.8 m and 15.5-16.8 clear-cutting on mean specific root area (yellow), total root biomass (orange), mean diameter (green), mean root area index (purple), total root necromass (black) and mean specific root length (blue) across deep soil profiles. The size of the circles is not at scale, the idea is only to visualize trends between soil layers 0-1 m, 2-6 m and 10-16 m, and between treatments +W, -W and NH. Table V. 1: Mean diameter (mm), maximum elongation rate of individual roots (cm day -1 ), number of roots observed and root mortality over 3 years in the minirhizotron images across all the soil layers, from the surface to the water table at a depth of about 17 m, in the undisturbed rainfall plot (+W) and the plot with 37% of throughfall excluded by plastic sheets (-W). .... 126 Table V. 2: Total living fine root biomass (g m -2 ), total fine root necromass (g m -2 ), mean specific root length (m g -1 ), mean specific root area (cm 2 g -1 ) and mean root diameter down to a depth of 17 m in the undisturbed rainfall plots +W, in the plot with 37% of throughfall excluded by plastic sheets (-W), both in coppices and 1.5 years after the clear-cut, and in the non-harvested plot (NH), i.e. a 7.5-year-old tree plantation. Standard deviations are indicated. Different lower-case letters indicate significant differences between treatments +W and -W (p < 0.05). NH was not included in statistical analyses because the three soil coring replicates were located in the same plot. Table IX. 1: Main characteristics of the stands at 39 months (mean and standard deviation between blocks, n=3). Different uppercase letters indicate significant differences between treatments, and different lowercase letters indicate significant differences between the monospecific stands and the mixed stands for each species (p < 0.05). The methods used to estimate the aboveground biomass are described in Nouvellon et al. (2012b) [START_REF] Vogt | Review of root dynamics in forest ecosystems grouped by climate, climatic forest type and species[END_REF][START_REF] General Discussion Alexandratos | World food and agriculture: outlook for the medium and longer term[END_REF][START_REF] Cassman | Ecological intensification of cereal production systems: yield potential, soil quality, and precision agriculture[END_REF]. The research work of the IPCC (Intergovernmental Panel on Climate Change), created in 1988, highlights the impact of climate change, mainly anthropogenic, on ecosystems [START_REF] Metz | Climate change 2007: Mitigation of climate change[END_REF]. The Kyoto treaty was signed in 1997 to fight against the increase in the atmospheric concentration of greenhouse gases. The increase of carbon dioxide (CO2) and other greenhouse gases (GHG) contents in the atmosphere, mainly methane (CH4) and nitrous oxide (N2O), and their role in global warming are undeniable (Graefe et al., 2008;Solomon et al., 2009).

LIST OF FIGURES

LIST OF TABLES

Reducing those emissions to avoid a temperature increase of more than 2°C above pre-industrial era is a real challenge recognized by the entire scientific community (IPCC, 2014). In this perspective, the emission of greenhouse gases into the atmosphere can be directly reduced (or offset) by the sequestration of carbon in some compartments participating in its cycle. Soil represents the largest reservoir of continental organic carbon [START_REF] Jacobson | Earth System Science: from biogeochemical cycles to global changes[END_REF]. It is estimated that soil sequester approximately 800 Gt over the first 30 cm and about 1500 Gt when considering the first meter [START_REF] Post | Soil carbon pools and world life zones[END_REF][START_REF] Eswaran | Organic carbon in soils of the world[END_REF][START_REF] Batjes | Total carbon and nitrogen in the soils of the world[END_REF]. Therefore, a tiny variation of those stocks can have a strong effect on the global atmospheric carbon. In this context, the French Minister of Agriculture launched the "4 per 1000" initiative whose objective is to develop agronomic research in order to increase soil organic carbon stocks by 4‰ per year. Such an increase would make it possible to offset greenhouse gases emissions and mitigate climate change [START_REF] Lal | Soil health and carbon management[END_REF][START_REF] Chabbi | Aligning agriculture and climate policy[END_REF][START_REF] Dignac | Increasing soil carbon storage: mechanisms, effects of agricultural practices and proxies. A review[END_REF][START_REF] Minasny | Soil carbon 4 per mille[END_REF][START_REF] Corbeels | The 4 per 1000 goal and soil carbon storage under agroforestry and conservation agriculture systems in sub-Saharan Africa[END_REF]. Agriculture is the first source of greenhouse gas emissions (FAO, 2015) when combined with land-use change and forestry, which both represent approximately 17.4%

of worldwide GHG emissions. While many studies have been carried out to estimate the carbon balance in boreal and temperate forests [START_REF] Falge | Seasonality of ecosystem respiration and gross primary production as derived from FLUXNET measurements[END_REF][START_REF] Baldocchi | Predicting the onset of net carbon uptake by deciduous forests with soil temperature and climate data: a synthesis of FLUXNET data[END_REF], comprehensive studies quantifying the main fluxes of the C cycle are scarce in tropical forest ecosystems. More study cases accounting for the interactive effects of (future) climate, soil, and management practices are needed in tropical regions to improve global biogeochemical models [START_REF] Penuelas | Human-induced nitrogen-phosphorus imbalances alter natural and managed ecosystems across the globe[END_REF]. Hence, it is important to assess the feasibility, timeliness, and effectiveness of a potential use of planted forests as a strategy to mitigate greenhouse gas emissions.

I.1 Forest plantations

The area of forest plantations has increased sharply in recent decades in response to the increase in global demand for timber, mainly as a result of population growth, rising living standards, and the emergence of new markets for wood products, such as the use of wood as a substitute for fossil fuels (e.g. iron and steel industry). A study based on the Global Forest Products Model [START_REF] Buongiorno | The global forest products model: structure, estimation, and applications[END_REF] predicts a 20% increase in world demand for wood by 2060, mainly driven by the increasing consumption of paper and wood for buildings [START_REF] Elias | Planting for the future: How demand for wood products could be friendly to tropical forests[END_REF]. While natural forests areas decreased from 3961 million hectares in 1990 to 3721 million hectares in 2015, forest plantation areas increased from 168 to 278 million hectares during the same period (Keenan et al., 2015;[START_REF] Payn | Changes in planted forests and future global implications[END_REF]. Thus, forest plantations account for 7% of the total of forest area in the world in 2015, compared to 4.1% in 1990. In 2000, they accounted for 5% of the global forest cover but provided 33% of roundwood harvested and reached 46% in 2012, with large disparities between regions in the world: 65% in tropical and subtropical regions, 45% in temperate regions and only 14% in boreal regions. In tropical and subtropical regions, plantations of fast-growing species (mainly Eucalyptus, Pinus and Acacia genera) store large amounts of carbon and contribute to reducing the exploitation of natural forests by providing an increasing proportion of the global demand of wood (Keenan et al., 2015), and accounted for 29% of global forest plantation areas [START_REF] Payn | Changes in planted forests and future global implications[END_REF]. Highest productivities are reached in tropical and subtropical regions. Plantation productivity is on average 4.6 m 3 ha -1 year -1 and greatly vary around the world from 1.4 m 3 ha -1 year -1 on average in boreal regions to 8.4 m 3 ha -1 year -1 in tropical regions [START_REF] Payn | Changes in planted forests and future global implications[END_REF]. South America with an average productivity of 24 m 3 ha -1 year -1 is the area with the highest productivity.

Indeed, in 2012, Brazil's forest plantations, despite an area of only 7.7 million hectares, produced 132 million m 3 , as much as the United States with an area of 79 million hectares that produced 141 million m 3 .

I.2 Eucalyptus plantations

Fast-growing Eucalyptus plantations (Figure I. 1) cover about 20 million hectares throughout the world (Booth, 2013) and are the most planted tree species in Brazil with about 5.6 million hectares, which represents 72.3% of the area of Brazilian forest plantations and 81% of the Brazilian wood production (IBA, 2016). Eucalyptus plantations play an important role in the supply of pulp, paper and power generation in Brazil, accounting for 5% of the country's GDP, in addition to 2.4 million direct and indirect jobs (IBA, 2016). These forests of great economic interest have a mean annual increment of 40 m 3 ha -1 year -1 on rotations of 6-8 years, ranging between 25 and 60 m 3 ha -1 year -1 depending on forest management practices and regions [START_REF] Oliveira | Caracterização da madeira de sete espécies de eucaliptos para a construção civil[END_REF]. With a gross primary productivity that can exceed 3500 g C m -2 year -1 (Ryan et al., 2010;Nouvellon et al., 2012), Eucalyptus plantations in Brazil are among the most productive forests in the world [START_REF] Luyssaert | CO2 balance of boreal, temperate, and tropical forests derived from a global database[END_REF]. The significant productivity gains over the last 25 years, from 25 m 3 ha -1 year -1 in the early 1990s to more than 40 m 3 ha -1 year -1 nowadays, resulted from improvements in silvicultural practices and breeding programs making it possible to identify highly performant clones from some Eucalyptus species and hybrids, in particular E. grandis, E. urophylla, E. saligna and E. camaldulensis. The diversity of Eucalyptus species planted in tropical regions has led to a wide range of products and management practices (Gonçalves et al., 2013). Although many Eucalyptus plantations are intensively managed to produce raw materials for industry (mainly pulp and paper, but also solid-wood products, fiberboards and charcoal for steel production), energy production from wood for domestic use also contributes to alleviating poverty in developing countries (Cossalter and Pye-Smith, 2003;[START_REF] Nambiar | Productivity of acacia and eucalypt plantations in Southeast Asia. 1. Bio-physical determinants of production: opportunities and challenges[END_REF]. The development of industries that use wood as raw materials has generated more attention from researchers to develop new techniques oriented towards the increase of productivity and wood quality. Highly productive industrial plantations are generally perceived as a threat to biodiversity, water resources or soil fertility.

The environmental impact of those highly productive forest plantations has raised many concerns in recent decades (Cossalter and Pye-Smith, 2003). Nevertheless, the problems associated with these plantations are often site-specific, and how they are managed is of paramount importance.

I.3 Consequences of climate change on the forest plantations management

In Brazil, most of Eucalyptus plantations are settled in areas with very deep soils (> 5m), low soil fertility and prolonged drought periods (Gonçalves et al., 2013). Even if future precipitation distributions are still difficult to predict at the local scale, studies have shown that global warming will be associated with an intensification of dry periods in many parts of the globe (Solomon et al., 2009), especially in sub-tropical areas already subject to severe droughts [START_REF] Meehl | Global climate projections[END_REF]. A throughfall exclusion experiment in the Amazon showed that a decrease in precipitation can have a considerable influence on the functioning of forest ecosystems [START_REF] Brando | Drought effects on litterfall, wood production and belowground carbon cycling in an Amazon forest: results of a throughfall reduction experiment[END_REF]. The dynamics of fine roots, litter fall, soil organic matter decomposition and nutrient mineralization, as well as soil aeration (affecting the diffusion of gases and microbial processes in the soil) are highly sensitive to rainfall (Van Straaten et al., 2010;Maier et al., 2017). In this context, it is important to better understand the factors influencing the response of forest ecosystems and their ability to improve their adaptation to drought conditions [START_REF] Choat | Global convergence in the vulnerability of forests to drought[END_REF]. In tropical and subtropical regions, the productivity of intensively-managed Eucalyptus plantations is mainly controlled by water availability in the soil [START_REF] Smethurst | Forest fertilization: trends in knowledge and practice compared to agriculture[END_REF]Gonçalves et al., 2013). The management of fast-growing Eucalyptus plantations should be adapted in the future to more frequent drought conditions to avoid tree mortality [START_REF] White | Managing productivity and drought risk in Eucalyptus globulus plantations in south-western Australia[END_REF]Battie-Laclau et al., 2014b;[START_REF] White | Managing for water-use efficient wood production in Eucalyptus globulus plantations[END_REF]. The selection of drought-tolerant clones and hybrids will be necessary to reduce tree water requirements, as well as a possible adjustment in planting density, fertilization regime and rotation duration (Booth, 2013).

(Figure I. 2)
Furthermore, the main criticism of industrial Eucalyptus plantations is their high-water consumption, which can affect the water resources of the regions concerned by large areas of afforestation [START_REF] Jackson | Trading water for carbon with biological carbon sequestration[END_REF]. Soil moisture monitoring down to a depth of 10 m in Brazilian eucalypt plantations showed no drainage beyond the root system, from the third year after planting onward, even though the annual precipitations was relatively high (about 1400 mm year -1 ) (Christina et al., 2011;Laclau et al., 2013). Silvicultural management also has a significant impact on the water cycle. The clear-cut of the trees allows a recharge of the deep horizons of the soil with a rise of several meters of the water table [START_REF] Almeida | Growth and water balance of Eucalyptus grandis hybrid plantations in Brazil during a rotation for pulp production[END_REF]Christina et al., 2017). Improving our understanding of soil water transfers after cutting the trees and their impact on the microbial processes involved in C and nutrient cycling is important for the management of these planted forests in a context of climate change [START_REF] Sheffield | Projected changes in drought occurrence under future global warming from multi-model, multi-scenario, IPCC AR4 simulations[END_REF]Solomon et al., 2009;IPCC, 2014).

I.4 The importance of fine roots for tree growth

Being the main organ for water and nutrient uptake by plants, fine roots (diameter ≤ 2 mm) play an essential role in plant growth (Hinsinger, 2001;Brunner et al., 2013;[START_REF] Upson | Soil organic carbon and root distribution in a temperate arable agroforestry system[END_REF]. The establishment of a deep root system can be a strategy for plant species to adapt to water stress. In poor soils, most of the fertility is concentrated in the surface horizon as a result of deposition and decomposition of aboveground litter, soil organic matter mineralization and fine root decomposition. The high root growth rate of Eucalyptus trees allows them to explore both the superficial soil layers and very deep soil horizons at early stages. Fine roots in eucalypt plantations can reach a depth of 7 m the first year after planting when there is no barrier for root growth (Christina et al., 2011;Laclau et al., 2013). However, the relative contribution of deep roots to mineral nutrition is still poorly documented in these plantations (Da Silva et al., 2011;Bordron et al., 2018).

Plant species use a large range of rooting patterns to cope with periodic drought, from "drought tolerant strategies" with fine roots surviving in periodically dry soil, to "drought avoiding strategies" shedding fine roots from dry soil horizons while rapidly developing roots in moister areas (Brunner et al., 2015;Vries et al., 2016;Bristiel et al., 2018). Drought can increase the root-to-shoot ratio, the root area or root length-to-leaf area ratio, as well as the proportion of fine roots in deep soil layers and/or the specific root area (Markesteijn and Poorter, 2009;Ma et al., 2018;Zhou et al., 2018). Root growth peaks have been shown in deep soil layers during or the first months just after dry periods for eucalypt and rubber trees in tropical soils (Maeght et al., 2015;Lambais et al., 2017). Drought tolerance strategies are common for herbaceous plants, while drought avoiding strategies are often adopted by trees in evergreen tropical forests (Brunner et al., 2015). Despite the crucial role of fine roots to cope with drought, root phenology remains poorly understood in comparison to leaf ecophysiology (Radville et al., 2016).

Fine root dynamics and turnover depend on the plant species, but also on biotic and abiotic parameters. For example, soil water contents and soil properties, such as pH, nitrogen and oxygen concentrations can strongly influence fine root dynamics [START_REF] Vogt | Review of root dynamics in forest ecosystems grouped by climate, climatic forest type and species[END_REF][START_REF] Satomura | Considerations in the study of tree fine-root turnover with minirhizotrons[END_REF][START_REF] Guo | Influence of root zone nitrogen management and a summer catch crop on cucumber yield and soil mineral nitrogen dynamics in intensive production systems[END_REF]. Indeed, observations in Eucalyptus plantations suggest a link between the vertical distribution of fine roots and nutrient acquisition by the trees [START_REF] Bouillet | Changes with age in the spatial distribution of roots of Eucalyptus clone in Congo: impact on water and nutrient uptake[END_REF]Da Silva et al., 2011;Laclau et al., 2013), which can itself develop a high plasticity of its root system to colonize preferentially nutrient-rich areas (Hodge, 2004).

I.5 How to study fine root dynamics

There is no consensus on the best method to measure fine root production in forest ecosystems, and most studies conclude that a combination of different methods gives the most reliable results [START_REF] Vogt | Review of root dynamics in forest ecosystems grouped by climate, climatic forest type and species[END_REF][START_REF] Hertel | A comparison of four different fine root production estimates with ecosystem carbon balance data in a Fagus-Quercus mixed forest[END_REF]Hendricks et al., 2006;Jourdan et al., 2008). Successive soil sampling with a sequential coring measurement is the most commonly used method to study fine root production in natural or planted forest ecosystems [START_REF] Persson | Root dynamics in a young Scots pine stand in central Sweden[END_REF]Mello et al., 2007;Jourdan et al., 2008). It is frequently associated with the installation of "ingrowth cores", both techniques are based on destructive soil samplings. In the last method, new fine roots produced in a root-free soil volume are regularly collected and quantified within mesh bags every month or more, during an entire year, to estimate the annual fine root production (Hendricks et al., 2006). However, several studies have shown that soil disturbances (in particular fine root cutting) that occurred during the installation of the mesh bags significantly changes fine root dynamics (Vogt et al., 1998;[START_REF] Hertel | A comparison of four different fine root production estimates with ecosystem carbon balance data in a Fagus-Quercus mixed forest[END_REF]Jourdan et al., 2008). Since the 1980s, the minirhizotron technique is widely used to study fine root dynamics and turnover [START_REF] Withington | The impact of material used for minirhizotron tubes for root research[END_REF]Graefe et al., 2008;Maeght et al., 2013).

This technique allows direct observation and measurement of fine root dynamics while minimizing soil disturbance if a long period of recovery is observed prior to root measurements.

It is a non-destructive method that involves the installation of transparent tubes, called minirhizotrons, in the soil near the studied plants [START_REF] Majdi | Longevity of mycorrhizal roots depends on branching order and nutrient availability[END_REF][START_REF] Tierney | Evaluating minirhizotron estimates of fine root longevity and production in the forest floor of a temperate broadleaf forest[END_REF][START_REF] Withington | The impact of material used for minirhizotron tubes for root research[END_REF]. With this transparent interface, fine roots can be measured at successive dates to study the dynamics of growth and mortality (Hendrick and Pregitzer, 1996;Anderson et al., 2003). The opportunity to study fine roots in a mildly disturbed environment is an important asset of this method [START_REF] Majdi | Longevity of mycorrhizal roots depends on branching order and nutrient availability[END_REF].

I.6 Specificities of fine roots in deep soil layers

Deep fine roots are fundamental organs for the growth and survival of plants. They help to avoid nutrient losses through deep drainage (Laclau et al., 2010;[START_REF] Mareschal | Nutrient leaching and deep drainage under Eucalyptus plantations managed in short rotations after afforestation of an African savanna: two 7-year time series[END_REF], and to withdraw water at great depth during dry periods [START_REF] Schwendenmann | Effects of an experimental drought on the functioning of a cacao agroforestry system, Sulawesi, Indonesia[END_REF]Battie-Laclau et al., 2014b;Christina et al., 2015). Fine root dynamics at the vicinity of very deep water tables have been little studied [START_REF] Soylu | Influence of groundwater on plant water use and productivity: development of an integrated ecosystem-variably saturated soil water flow model[END_REF], mainly due to technical difficulties, although the fine root behavior can be essential for plant survival during severe drought events [START_REF] Nepstad | Mortality of large trees and lianas following experimental drought in an Amazon forest[END_REF][START_REF] Malhi | Exploring the likelihood and mechanism of a climate-changeinduced dieback of the Amazon rainforest[END_REF]Markewitz et al., 2010;[START_REF] Ivanov | Root niche separation can explain avoidance of seasonal drought stress and vulnerability of overstory trees to extended drought in a mature Amazonian forest[END_REF]. Fine root lifespan depends on many factors such as root order [START_REF] Guo | Influence of root zone nitrogen management and a summer catch crop on cucumber yield and soil mineral nitrogen dynamics in intensive production systems[END_REF], diameter [START_REF] Joslin | Fine-root turnover patterns and their relationship to root diameter and soil depth in a 14 C-labeled hardwood forest[END_REF] and soil depth (Hendrick and Pregitzer, 1996;Baddeley and Watson, 2005;Germon et al., 2016). Most of the studies dealing with fine root production and turnover have been carried

out in the upper soil layers (depth <1 m) mainly due to the difficulty to realize such measurements at great depth (Billings, 2015). Improving our understanding of water and nutrient uptake processes at great depth will become more important for forest management in a context of climate change since trees will be more (Nepstad et al., 1994;[START_REF] Malhi | Exploring the likelihood and mechanism of a climate-changeinduced dieback of the Amazon rainforest[END_REF].

Studies carried out in Brazil showed that about 10% of the total fine root biomass is distributed below 3 m of depth in eucalypt plantations (Christina et al., 2011). Laclau et al. (2013) showed that the proportion of fine roots below 4 m deep increased with the age of Eucalyptus trees: fine roots below 4 m deep represented 5%, 10% and 20% of the fine root intersects on vertical pit walls in plantations of 1, 3.5 and 6 years old, respectively. In Brazil, the first estimates of the production and turnover of Eucalyptus fine roots were conducted in topsoil horizons limited to a depth of 1 m (Mello et al., 2007;Jourdan et al., 2008), while little is known about these processes at depth. Lambais et al. (2017) studied root production and mortality during the first rotation of Eucalyptus plantation down to a depth of 6 m. They showed that Eucalyptus fine roots colonized quickly the very deep soil horizons (depth > 5 m) and that the root elongation rate was higher between the depths of 5 and 6 m compared to the top soil from 2 to 4 years after planting. In addition, there was only 3.4% of root length lost by mortality in the 5-6 m soil layer during the 2 years of study, whereas 22.7% of the fine roots had died in the superficial layer.

There is little quantitative data on deep fine root dynamics (> 6 m) and literature tends to underestimate the depth of the root system distribution as well as its importance in ecosystems functioning and productivity (Schenk and Jackson, 2002;Markewitz et al., 2010;Freycon et al., 2015).

I.7 Relationships between fine root dynamics and GHG fluxes

Fine roots participate actively in the C fluxes in forest soils through the emission of C to atmosphere by respiratory processes and C storage in the soil from root mortality and exudation of carbonic compounds (Balesdent and Balabane, 1996;Strand et al., 2008). Then, it is challenging to compare the observations of fine root production and mortality with the dynamics of CO2, CH4 and N2O throughout deep soil profiles in the context of climate change.

Eucalyptus trees allocate about 30% of their gross primary productivity to root maintenance and production in highly productive plantations managed in short rotations (Ryan et al., 2010), but the difficulty to estimate fine root dynamics throughout the entire soil profile limits the estimation of the global soil carbon cycle and the total emissions of greenhouse gases (GHG), as well as the understanding of factors controlling them [START_REF] Wang | Concentration profiles of CH4, CO2 and N2O in soils of a wheat-maize rotation ecosystem in North China Plain, measured weekly over a whole year[END_REF].

Greenhouse gases (GHG) emissions from soils are the result of complex production, consumption and transport processes (Figure I. 3), and are affected by many factors such as microclimate, substrate availability for soil micro-organisms, aboveground photosynthetic supply to roots and management factors (Metay et al., 2007). CO2 effluxes at soil surface come from root respiration, anaerobic and aerobic microbial respiration and soil organic matter decomposition (Figure I. 3) [START_REF] Versini | The manipulation of organic residues affects tree growth and heterotrophic CO2 efflux in a tropical Eucalyptus plantation[END_REF][START_REF] Oertel | Greenhouse gas emissions from soils-A review[END_REF]. CH4 effluxes depend on the balance between production by methanogenesis under anaerobic conditions and consumption by methanotrophic microorganisms (Dutaur and Verchot, 2007;Tate, 2015)(Figure I. 3). N2O emissions from soil are driven by microbial nitrification (oxidation of NH4 + to NO3 -) and denitrification (reduction of NO3 -to N2O) (Figure I. 3) (Bai et al., 2014;Zhong et al., 2014;Ortiz-Gonzalo et al., 2018).

Production of greenhouse gases by soil microorganisms and roots can change rapidly temporally and spatially, which makes modeling efforts challenging (Drewitt et al., 2005;Courtois et al., 2018). While most studies dealing with soil greenhouse gas effluxes addressed the spatial and temporal variations, the vertical distribution of soil respiration is still little documented in very deep soils (Drewitt et al., 2005). Trees with roots at depths of more than 10 m are common in tropical forests (Nepstad et al., 1994;Saleska et al., 2007;Broedel et al., 2017). In a Brazilian Amazon forest, the consumption of CH4 occurred mainly in the upper 10 cm of the soil profile, the production of N2O mainly in the 0-25 cm soil layer whereas CO2 was produced down to at least a soil depth of 11 m (Davidson et al., 2004). In another Amazonian forest, CO2 production in the 0.5-3 m soil layer accounted for 17 % of the total soil CO2 production (Sotta et al., 2007). Even if microbial activity is low in deep soil layers (Fontaine et al., 2007), the huge soil volume explored by fine roots might lead to significant CO2, N2O and CH4 productions within the entire rooting soil profile.

Measurements of GHG emissions at the soil surface provide an integrative estimate of the net production in the soil, but information on the patterns of production, consumption and transport of CO2, CH4 and N2O within the soil profile remain poorly understood (Davidson et al., 2006;Hashimoto et al., 2007;Wiaux et al., 2015). Understanding these patterns can provide insights into the possibilities of reducing GHG emissions. Data on the time course of GHG concentrations throughout soil profiles can provide additional information on heterogeneous gaseous exchange processes at depth that may be involved in the control of such surface fluxes.

The comparison between the dynamics of CO2 contents at various depths and the dynamics of

I.8 Root dynamics in forest stands conducted in coppice

Coppice management could be an interesting option to face water deficit because the trees are likely to benefit from a root system already established preserving living biomass for the next generation and making it possible to access the deep soil layers where water availability can be higher than in the topsoil. Coppice-managed plantations, letting regenerate one or two shoots from the stump after the harvest, are common due to lower production costs, shorter cycle times and faster financial returns compared to replanting [START_REF] Gonçalves | Produtividade de plantações de eucalipto manejadas nos sistemas de alto fuste e talhadia, em função de fatores edafoclimáticos[END_REF]. The proportion of coppice-managed plantations has increased from 10 % of the total area of Eucalyptus plantations in 2008 to 25-35% in 2010. The effects of clear-cutting on fine root dynamics in coppiced-managed forest plantations are poorly documented and the trends are not clear.

Sequential coring in Brazilian eucalypt plantations conducted in coppice showed that fine root density decreased in the 0-1 m soil layer the first 60 days after harvesting while fine root decomposition was accelerated (Mello et al., 2007). Less intense root growth was observed in the first 10 cm of the soil at 90 days after cutting the trees. In addition, this study showed that the decomposition of fine roots was accelerated after the clear-cut (Mello et al., 2007). An earlier study suggested that the growth of fine roots continues during the period after the harvest of trees in coppice-managed plantations of E. camaldulensis Dehn in Morocco; however, radial root growth was interrupted after cutting the trees [START_REF] Riedacker | Influence du traitement en taillis sur la croissance et la morphogénèse aériennes et souterraines d'Eucalyptus camaldulensis dehn au Maroc[END_REF]. The most complete studies on root dynamics after regrowth have been carried out in coppice-managed Populus plantations. Dickmann et al. (1996) observed little changes in fine root production and mortality after clearcutting down to a depth of 1 m. Berhongaray et al. (2015) showed that before cutting the trees, the mortality of fine roots was much lower than the production, while after the harvest, mortality exceeded the root production. However, these results were obtained only in the upper 80 cm of the soil, while studies carried out in eucalypt plantations in the state of São Paulo showed that approximately 50% of the roots of diameter <1 mm were located below 1 m (Laclau et al., 2013). Cutting the trees leads to a significant production of organic matter via necromass and carbon compound exudates and therefore could be considerable at great depth [START_REF] Werner | Progress and challenges in using stable isotopes to trace plant carbon and water relations across scales[END_REF]Berhongaray et al., 2015) due to the amount of fine roots produced in these soil depths (Laclau et al., 2013).

I.9 Root inputs and changes in soil organic matter dynamics in coppice-managed stands

Coppice management may influence carbon sequestration in the superficial soil layers in Eucalyptus plantations, but also in very deep soil horizons where the influence of fresh organic matter inputs on carbon storage is still poorly understood (Fontaine et al., 2007;Derrien et al., 2014). Removing the aboveground parts of trees can have a great impact on the ecosystem carbon balance and greenhouses gases emissions. Clear-cutting increases the solar radiation transmitted to the soil, raising the soil temperature and soil water contents through an interruption of stand transpiration (Londo et al., 1999;Mello et al., 2007). This may induce an increase in microbial activity, the decomposition of harvest residues left at the soil surface and enhance fine root mortality and decomposition (Parfitt et al., 2001;Mello et al., 2007). When decomposed, a part of the former tissues from the roots is incorporated into the soil organic matter (Strand et al., 2008). Microorganisms are reactivated in response of the input of fresh organic matter. Specialized microorganisms develop rapidly and break down fresh organic matter. Their metabolites can activate a second class of specialized microorganisms, in dormancy, which can degrade the organic matter initially present and stored in the soil: this is the "priming effect" [START_REF] Fontaine | The priming effect of organic matter: a question of microbial competition?[END_REF]. Kuzyakov et al. (2000) emphasizes the importance of characterizing microbial communities, their biomass but also their functioning (e.g. catabolic profile or enzymatic activity), and their structure (e.g. bacteria / fungi ratio) as a prerequisite for the evaluation of the underlying mechanisms. The consumption of soil organic matter by microbes results in the emission of CO2 in aerobic conditions and CH4 in anaerobic conditions.

The "priming effect" could affect carbon storage in the soil and indirectly influence the nitrogen cycle. Indeed, CO2 emissions in the soil profile influence the oxygen partial pressure, which is one of the factors controlling the transformation reactions of nitrogen substrates in the soil.

Furthermore, the availability of carbon substrates is one of the main regulatory factors of the denitrification reaction [START_REF] Groffman | Ecology of nitrification and denitrification in soil evaluated at scales relevant to atmospheric chemistry[END_REF]. Diffusion and transport of gases are inversely proportional to the water-filled pore space (WFPS%). Therefore, when the soil water content decreases, CO2, CH4 and N2O reaches the surface quickly, the oxygen diffuses better throughout the soil profile, which influences important production and consumption processes [START_REF] Heincke | Effects of soil solution on the dynamics of N2O emissions: a review[END_REF][START_REF] Clough | A review of the movement and fate of N2O in the subsoil[END_REF]. Most of the studies dealing with soil carbon storage and greenhouse gas concentrations are limited to the upper meter of the soil profile (Harper and Tibbett, 2013). The consequences of tree harvesting on root dynamics and greenhouse gases production and consumption over the first year of the rotation in coppice-managed plantations ask specific questions never studied within the entire rooting profile in deep tropical soils.

A literature review pointed out the importance of fine roots in deep soil layers for the growth and survival of plants and their ability to adapt to biotic and abiotic stresses. The foraging strategy adopted by root systems is influenced by water availability, so plants tend to develop deeper root systems when they are subject to water stress (Christina et al., 2011;Bristiel et al., 2018). Coppice management could be an interesting option to face water deficit because the trees are likely to benefit from a deep root system already established before harvesting the previous stand to produce new shoots. Despite recent insights highlighting the importance of fine roots at great depth, current knowledge of their dynamics is still extremely limited.

Furthermore, root mortality supply organic matter at different soil depths, which is likely to affect greenhouse gas production and consumption processes. Therefore, improving our understanding of the spatiotemporal dynamics of GHG concentrations throughout deep soil profiles is an important issue to assess the environmental impact of silvicultural practices in tropical planted forests in a context of climate change.

CHAPTER 2: RESEARCH QUESTION AND SPECIFIC OBJECTIVES

The evaluation of the contribution of deep fine roots to the spatiotemporal dynamics of GHG concentrations throughout deep soil profiles is a metrological challenge and, in fact, a major scientific lock. The general objective of the thesis is to gain insight into fine root production and mortality in deep soil profiles with a joint characterization of greenhouse gases consumption and production. These effects have been monitored before and after harvesting all the trees in a highly productive Eucalyptus grandis plantation managed in coppice after clearcutting, under two contrasting water supply regimes in São Paulo state, Brazil.

The specific objectives of the thesis are:

-To gain insight into the influence of rainfall reduction on fine root production and mortality throughout the soil profile in coppice-managed plantations;

-To assess the effect of clear-cutting and coppice management on fine roots dynamics down to the water table, here located at a depth of 17 m;

-To determine the vertical profile of CO2, CH4, and N2O production rates from the topsoil to a depth of 17 m under two contrasting rainfall regimes.

CHAPTER 3: STUDY SITE

To meet our objectives, we used a field trial in a clonal plantation of Eucalyptus grandis W.

Hill ex Maiden located in the southeastern region of Brazil, in São Paulo state. Very simplified forest ecosystems such as monoclonal plantations offer interesting opportunities to understand more precisely some ecophysiological and biogeochemical processes impacting carbon and nutrient cycling. The studied field trial is particularly of interest to answer our questions because

Eucalyptus trees exhibit a remarkable deep root system in homogeneous tropical soils, and they have the capability to be coppice-managed.

III.1 Characteristics of the experimental area

The work presented in this thesis was performed between 2015 and 2017 in Brazil at the Itatinga The climate of this region was humid subtropical with a dry winter (Cwa) according to the Köppen classification. Over the 15 years prior to this study, the mean annual rainfall was 1390 mm, the mean air temperature was 20°C and the mean relative humidity was 77%. Two seasons can be distinguished, a dry and cold season from June to September with a mean monthly temperature of 15°C, and a wet and hot season from October to May, with a mean monthly temperature of 25°C and heavy rainfalls (about 75% of the total annual rainfall).

The experiment was located on the upper part of a hill (slope <3%) at an altitude of 850 m.

From 1945 to 1998, the area was planted with Eucalyptus saligna and since 1998 wooded with a highly productive plantation of Eucalyptus grandis W. Hill ex Maiden. E. grandis are native from the east coast of Australia, between latitudes 33°S (New South Wales) and 16°S (northern Queensland), in areas where precipitations are greater than 1000 m. In Brazil, the Eucalyptus grandis species is widely used due to the high quality of pulpwood, rapid growth and high productivity, and its suitability for coppice-management.

The soils were very deep (> 15 m) Ferralsols (IUSS Working Group WRB, 2015) developed on Cretaceous sandstone of medium texture. Clay contents were ranging from 160 mg g -1 in the topsoil to about 250 mg g -1 at a depth of 15 m. Soil mineralogy is dominated by quartz, kaolinite and oxyhydroxides. Maquere (2008) characterized in detail the soil chemical attributes down to a soil depth of 6 m (Table III. 1). showed that the amounts of N, P, Ca, Mg and micronutrients applied in this experiment were not limiting for tree growth [START_REF] Gonçalves | Soil fertility and growth of Eucalyptus grandis in Brazil under different residue management practices[END_REF]Laclau et al., 2009). Herbicides were applied to avoid the presence of understory species.

Since September 2010, throughfall was partially excluded in -W plots, using panels made of clear greenhouse plastic sheets mounted on wooden frames at heights ranging between 0.5 m and 1.6 m. Plastic sheets covered 37% of the area in the -W plots. A 50 cm deep trench was dug around the -W plots to limit the lateral development of Eucalyptus roots between + W and -W treatments. The dead leaves, branches and bark that fell on the plastic sheets were collected weekly and scattered under the gutters during the entire study. Water excluded from the gutters was collected weekly and samples were analyzed monthly to estimate the amounts of nutrients excluded during the study period. These amounts of dissolved nutrients in the water were replaced each year in each -W treatment (ammonium sulphate, KCl, NaCl, phosphorus ...) to distinguish the effect of water exclusion and nutrient deficiency. parameters accounting for the changes (Christina et al., 2015), photosynthetic physiology (Battie- Laclau et al., 2014a), phloem transport of photosynthates [START_REF] Epron | In situ 13 CO2 pulse labelling of fieldgrown eucalypt trees revealed the effects of potassium nutrition and throughfall exclusion on phloem transport of photosynthetic carbon[END_REF], wood formation (Ployet et al., 2019), water use efficiency (Battie- Laclau et al., 2016), tree water use and water seepage (Christina et al., 2018), canopy conductance, sapwood area: leaf area ratio (Huber value) and sap flow driving force [START_REF] Asensio | Potassium supply enhances hydraulic constraints on water use in eucalyptus trees[END_REF] and deep root functioning through rhizosphere versus bulk soil analysis (Pradier et al., 2017). The incorporation of these results in process-based models, as well as further studies dealing with long-term effect of water availability on soil properties might contribute to evaluate adaptive changes induced by global changes in tropical Eucalyptus plantations.

K deficiency and water deficit affect traits involved in catching light resources, traits controlling CO2 assimilation, traits related to transport via xylem and phloem and soil water and nutrient resources (Table III. 2). Indeed, K fertilization through drastic modifications in leaves physiology greatly increased gross primary productivity and above ground biomass production.

A modeling approach revealed that soil water uptake parameters and leaf photosynthetic parameters were the main drivers of gross primary productivity and light-use efficiency for carbon assimilation. Photosynthesis, anatomical and biochemical leaf treats in E. grandis had a functional relationship between K and Na supply. Osmotic adjustment, stomatal closure, higher phloem sugar concentration, higher velocity of C transfer in phloem and a decrease in leaf area index were observed when trees were subjected to water restriction and K deficiency. K fertilization and water availability modified xylem metabolome and transcriptome and impacts greatly wood structure, and notably vessel properties. Water deficiency also increased the mean soil depth of water withdrawal, decreased the residual soil water content in deep soil layers and lead to a drop in the water table.

Furthermore, reduced rainfall significantly increase exchangeable K and H3O + within the rhizosphere and enhanced at great depth. A complementary study showed for the first-time ectomycorrhizal symbiosis in deep soil layers and the population of Pisolithus sp., the dominated genus, was strongly dependent on soil depth (Robin et al., 2019). Those results combined suggest a different root functioning in response to drought condition and especially in deep soil layers.

However, the influence of nutrient and water availability on root traits and root dynamics at depth remains poorly known despite its role in: i) microclimate, ii) tree growth during drought periods, iii) the potential for carbon sequestration in the deep layers of tropical soils, iv) the recycling of nutrients. Improving the understanding of the environmental control of rooting strategies in trees is of interest beyond the scope of Eucalyptus plantations in Brazil.

Furthermore, the huge soil volume explored by fine roots might lead to significant CO2, N2O and CH4 productions, and improving our understanding of the spatiotemporal dynamics of gas concentrations in deep soil layers is essential to quantify more accurately C source/sink fluxes in tropical soils. Comprehensive experimental studies are needed to improve the current biogeochemical models used to predict the effect of drought periods on greenhouse gas effluxes. (Balesdent and Balabane, 1996;Strand et al., 2008). Root systems are known to be very heterogeneous and plastic, both architecturally and functionally, depending on plant age and its phenology, soil conditions and climate [START_REF] Hodge | Plant root growth, architecture and function[END_REF]. Roots have the capacity to expand over large soil volume, particularly with shrubs and trees, and can be found at very great depths in xeric and drought ecosystems (Canadell et al., 1996;Schenk and Jackson, 2002).

Fine root dynamics are defined as fine root production and mortality [START_REF] Hendrick | The dynamics of fine root length, biomass, and nitrogen content in two northern hardwood ecosystems[END_REF]McCormack and Guo, 2014), finer root turnover and survivorship (Anderson et al., 2003), senescence [START_REF] Huck | Soybean Root Senescence under Drought Stress 1. Minirhizotron observation tubes: methods and applications for measuring rhizosphere dynamics[END_REF] and fine root elongation rate (Germon et al., 2016;Lambais et al., 2017). Fine root dynamics are driven by both endogenous and exogenous factors like soil temperature and water content [START_REF] Coll | Fine root seasonal dynamics, plasticity, and mycorrhization in 2 coexisting Mediterranean oaks with contrasting aboveground phenology[END_REF]

IV.2 Defining deep fine roots

The importance of deep root system has been highlighted in several reviews (Canadell et al., 1996;Maeght et al., 2013;Pierret et al., 2016) , but their dynamics and specificities are still poorly known. Numerous rooting depth characteristics have been examined since those studies, yet studies often claim that physiological and morphological characteristics of deep root systems are poorly understood. Recently defined by Maeght et al. (2013), deep roots are roots growing below a depth of 1 m. More and more studies highlight that rooting depth has been underestimated, particularly for shrubs and trees (Canadell et al., 1996). Even if a small number of roots are found at great depth, deep roots likely have a key role in many processes of plant physiology, community ecology and geochemical cycles. Studies have demonstrated that deep roots are found in many biomes, where drought conditions are commonly exhibited (Nepstad et al., 1994;Canadell et al., 1996;Jackson et al., 2000;Schenk and Jackson, 2002), but maximum rooting depth reported in the scientific literature is underestimated because few studies have focused on deeper horizons (Schenk and Jackson, 2002) and have artificially truncated the root distribution. [START_REF] Stone | On the maximum extent of tree roots[END_REF] reported 37 examples of tree root colonization between 10 and 60 m below the soil surface, indicating that the maximum rooting depth varies considerably with climatic and soil conditions and between species. Canadell et al. (1996) Once that considerable rooting depth has been highlighted, deep root distribution and dynamics need to be better described as it is still poorly studied compared to shallow root distribution.

Indeed, deep root studies are scarce despite the recent technical advances and innovations because it is still difficult to access, time-consuming, expensive and requires a combination of several methods to obtain the most reliable results (Maeght et al., 2013). Methods for monitoring deep roots are grouped into direct and indirect techniques depending on the equipment needed, research aim and their respective advantages and drawbacks (Vogt et al., 1998;Hendricks et al., 2006). N budget, ecosystem carbon balance, starch and carbon fluxes approaches have been used to study and quantify indirectly deep root functioning at considerable soil depths and are described in detail by Vogt et al. (1998). As for the direct methods, excavation, trenches, sequential coring, ingrowth cores, rhizotron, and minirhizotrons have been used to monitor root dynamics in situ and have been described in detail by Maeght et al. (2013). Both indirect and direct approaches present potential biases leading to overestimation or underestimation of root growth and decomposition. Despite all these methods, there is no scientific consensus on which the most effective and reliable method is determining the dynamics of fine roots. Understanding spatial and temporal fine root distribution and functioning in deep soil layers is crucial for a better understanding of biosphereatmosphere interactions [START_REF] Zeng | The role of root distribution for climate simulation over land[END_REF][START_REF] Kleidon | Assessing the role of deep rooted vegetation in the climate system with model simulations: mechanism, comparison to observations and implications for Amazonian deforestation[END_REF], and hence for terrestrial biosphere models. Deep roots improve tree tolerance to drought (McDowell et al., 2008;Nardini et al., 2016) and store C in deep soil layers (Laclau et al., 2013). Their importance in the C cycle and water flow has been demonstrated through modeling simulations (Saleska et al., 2007;[START_REF] Christoffersen | Mechanisms of water supply and vegetation demand govern the seasonality and magnitude of evapotranspiration in Amazonia and Cerrado[END_REF]. Therefore, to understand and predict in the proper way water cycles, C sequestration, and primary production and many others ecosystem services we should consider deep soil layers as dynamics and functional systems where fine roots may be different along the soil profile.

IV.3 Deep fine root morphology, architecture and anatomy

Root morphology and architecture are important in determining a plant's availability to survive in stressful soil conditions and can influence considerably tree growth and ecosystem processes.

Root system morphology and architecture vary largely between species but also within species [START_REF] Cannon | A tentative classification of root systems[END_REF][START_REF] Nibau | Branching out in new directions: the control of root architecture by lateral root formation[END_REF]. Functional traits also vary with environmental conditions and resource distribution (Ostonen et al., 2007). Root diameter and root length are two of the main criteria taken into account to evaluate root function and behavior. Fine roots have been classified into distinct classes for different functions and metabolic activity: i) root for acquisition and uptake of soil resources, therefore classified as absorptive roots are extremely fine and are the most distal roots; ii) root for transport and storage of nutrients are larger roots higher up in the branching order, which are the main structural part of the fine root system. The high variability of the environmental conditions such as soil moisture and temperature or nutrient availability along the soil depth result in contrasting fine root functional traits among depths.

Deep fine root exploration also leads to an important metabolic cost for plants [START_REF] Iversen | Digging deeper: fine-root responses to rising atmospheric CO2 concentration in forested ecosystems[END_REF] which affect changes in fine root traits (Prieto et al., 2015). The specific root length (SRL) and specific root area (SRA) are the two main root traits affected by depth (Maurice et al., 2010;Prieto et al., 2015;Pinheiro et al., 2016). They represent together the volume of the root in contact with the soil, and indirectly describe the capacity to take up limited soil resources by the plant (Maurice et al., 2010). There are few studies on the variation of specific root length and specific root area according to soil depth (Makita et al., 2011;Prieto et al., 2015;Pinheiro et al., 2016) species require a rapid and efficient acquisition of above and belowground resources; therefore, they generally have a higher specific root area and specific root length compared to slow growing species particularly in deep soil layers [START_REF] Ryser | The mysterious root length[END_REF][START_REF] Reich | The world-wide 'fast-slow'plant economics spectrum: a traits manifesto[END_REF][START_REF] Jo | Linking above-and belowground resource use strategies for native and invasive species of temperate deciduous forests[END_REF].

Roots of high SRL and thinner diameter are often associated with a better exploitation capacity (Hodge, 2004), and they increase the amount of root surface area in contact with soil water.

Establishing a deep root system with a high surface area allows the extraction of water from a larger soil volume (Jackson et al., 2000). Deep roots are mainly oriented toward water shown that fine root elongation rates in deep soil are more intense than in the topsoil, reaching several centimeters per day (Laclau et al., 2013;Germon et al., 2016;Lambais et al., 2017;Germon et al., 2019). A near-symmetrical above and below ground growth rates were observed by Christina et al. (2011) in Eucalyptus plantations reaching 10.4 and 19.2 m in height and a maximum rooting depth of 9.2 and 15.8 m at ages of 1.5 and 3.5 years, respectively. Those results are in line with the growth rates of Eucalyptus observed by Lambais et al. (2017) in nutrient-poor soil of Brazil with a mean fine root elongation rate increasing with soil depth up to 3.6 cm day -1 below a depth of 3 m. Increasing root growth rate is often seen as another feature of drought adaptation [START_REF] Annerose | Approche physiologique de l'adaptation à la sécheresse des espèces cultivées pour l'amélioration de la production en zones sèches[END_REF]. This high root elongation rate in deep soil layers could be a response to improve water and nutrients uptake, which confirm the positive feedback from developing roots to develop shoot [START_REF] Friend | Carbon allocation to root and shoot systems of woody plants[END_REF]. Fast root growth requires fast and efficient nutrient and water acquisition and thus a fast exploration of the deep soil layer. Environmental conditions and plant growth regulators may control those mechanisms [START_REF] López-Bucio | The role of nutrient availability in regulating root architecture[END_REF]. Deep soil layers are assumed to have higher soil water content and low-temperature variations compared to shallow layers [START_REF] Du | Linking belowground and aboveground phenology in two boreal forests in Northeast China[END_REF]Radville et al., 2016). Thus, climatic factors being more buffered in the deep soil layer, fluctuating less during day and season, are not affecting equally root phenology along with the soil profile. Deep fine root phenology could be also controlled by other factors. Indeed, deep roots are more distant from the shoot and the time to receive photosynthates would take longer to occur. A slow process phloem transport could also explain the delay between shallow and deep root growth currently observed. Yet there are still major uncertainties about the mechanisms controlling fine root phenology in deep soil layers.

IV.5 Mycorrhizal associations

Root systems are also characterized by their likelihood of association with mycorrhizal fungi.

Interactions between plant root system and mycorrhizal fungi have many beneficial effects. It can provide a source of C for mycorrhizal respiration in exchange for increased exploitation and transfer of water and nutrient from soil to the plant. Soil depth influence the diversity of microorganism and community composition as nutrient supply and oxygen is less favorable for microbial decomposition [START_REF] Eilers | Digging deeper to find unique microbial communities: the strong effect of depth on the structure of bacterial and archaeal communities in soil[END_REF]Santos et al., 2016). However, an abundant and diverse microbial community and high level of bacterial biomass have been found in very deep soil layers [START_REF] Dodds | Biological properties of soil and subsurface sediments under abandoned pasture and cropland[END_REF][START_REF] Gocke | Disentangling interactions between microbial communities and roots in deep subsoil[END_REF][START_REF] Zheng | Occurrence and abundance of ammonia-oxidizing archaea and bacteria from the surface to below the water table, in deep soil, and their contributions to nitrification[END_REF]. and shallow roots had a different form of mycorrhizal symbioses [START_REF] Rosling | Vertical distribution of ectomycorrhizal fungal taxa in a podzol soil profile[END_REF][START_REF] Clemmensen | Roots and associated fungi drive long-term carbon sequestration in boreal forest[END_REF]. However, as for deep root functioning, studies on mycorrhizal symbiosis in deep soil are still very limited partly due to the difficulty to collect soil at such depths. Studying biological activities in deep soil layers is crucial for the scientific community and become increasingly important to address in future studies, yet it remains a methodological and technical challenge [START_REF] Gocke | Disentangling interactions between microbial communities and roots in deep subsoil[END_REF].

IV.6 Influence of soil resources and environmental parameters

Soil resources and environment parameters are constantly changing. Deep roots are highly plastic in response to heterogeneous resource distributions [START_REF] Hodge | Plant root growth, architecture and function[END_REF]. They have the ability to adapt to changing resource availability and in particular to water availability, nutrients availability, soil texture, and atmospheric constituents. The variability of environmental factors affecting root growth are buffered in deep soil condition compared to the considerable variability observed at the soil surface [START_REF] Voroney | The soil habitat[END_REF]. Differences in root structure, architecture, and production in deep soil layers might be attributed to differences in soil resources and physical properties.

Soil water content is maybe the main driver for root production in the deep soil layers. Adriano et al. (2017) observed that fine root mass of Citrus sinensis (L.) Osbeck increased in drought conditions, particularly in deep soil layers. Schenk and Jackson (2002) reported that rooting depths were correlated with the length of the dry season and annual precipitation in tropical climates. The longer dry season and lower annual precipitation, the deeper was the root system. [START_REF] Wang | Root tip morphology, anatomy, chemistry and potential hydraulic conductivity vary with soil depth in three temperate hardwood species[END_REF] also found a strong correlation between root mass and soil water content down to a depth of 21 m in planted grassland and shrubland in China. Drought can increase the proportion of fine roots in deep soil layers and/or the specific root area (Markesteijn and Poorter, 2009;Ma et al., 2018;Zhou et al., 2018). In a survey of 62 tropical tree species, Markesteijn and Poorter (2009) showed that trees increase the belowground biomass and the proportion of deep roots in response to dry conditions. Germon et al. (2019) showed an increase in SRL and SRA under drought conditions for Eucalyptus trees in Brazil. Root growth peaks have been shown in deep soil layers during dry periods for eucalypt and rubber trees in tropical soils (Maeght et al., 2015;Lambais et al., 2017). Plant species use a large range of rooting patterns to cope with periodic drought, from "drought tolerant strategies" with fine roots surviving in periodically dry soil to "drought avoiding strategies" shedding fine roots from dry soil horizons while rapidly developing roots in moister areas (Brunner et al., 2015;Vries et al., 2016;Bristiel et al., 2018).

Root dynamics are also strongly correlated to the depth of the water [START_REF] Stave | Seedling growth of Acacia tortilis and Faidherbia albida in response to simulated groundwater tables[END_REF][START_REF] Canham | The response of Banksia roots to change in water table level in a Mediterranean-type environment[END_REF].

Soil texture also influences morphological acclimation of a deep root system. Root distribution has been showed to be shallower in sandy soils than in soil with a finer texture as shown in a tropical evergreen forest by Schenk and Jackson (2002). [START_REF] Xu | Rooting depth and leaf hydraulic conductance in the xeric tree Haloxyolon ammodendron growing at sites of contrasting soil texture[END_REF] found that fine root intersects on vertical pit walls were lower in coarse-textured soils (e.g.

Arenosols) than in fine-textured soils (e.g. Ferralsols). However, Canadell et al. (1996) cited some examples of roots reaching great depths in rocky soils.

In most plant-soil systems, the amount of available nutrients is a growth-limiting factor. Indeed, et al. (2004) studied fine roots and nutrient distribution down to a depth of 10 m in five semi-arid and arid sites in the southwestern USA. They found that roots responded through morphological and physiological adjustment in response to nutrient availability within the soil profile. [START_REF] Bordron | Fertilization increases the functional specialization of fine roots in deep soil layers for young Eucalyptus grandis trees[END_REF] found that fertilization increased the capacity of fine roots of Eucalyptus grandis to take up nutrients down to a depth of 3.2 m. They also found that adding nutrients increased root mass density, specific root length and specific root area along with the soil profile down to 3 m. On the contrary, Jourdan et al. (2008) showed that an increase in N content did not influence fine root biomass down to 3.0 m. Root growth and functioning are inhibited by high pH values due to nutrient deficiencies and specific ion toxicities (Hinsinger, 2001;[START_REF] Hinsinger | Origins of root-mediated pH changes in the rhizosphere and their responses to environmental constraints: a review[END_REF][START_REF] Jacobs | Fertilizer-induced changes in rhizosphere electrical conductivity: relation to forest tree seedling root system growth and function[END_REF]. The response of fine root production and mortality on nutrient availability in deep soil layers is not completely understood and further studies are needed.

McCulley
Many studies have focused on the impact of elevated CO2 concentrations in the atmosphere on plant growth. Fine root responses in changing CO2 conditions are still poorly known but some trends have emerged. [START_REF] Iversen | Digging deeper: fine-root responses to rising atmospheric CO2 concentration in forested ecosystems[END_REF] reviewed that rising atmospheric CO2 concentration tends to deeper rooting distributions of forested ecosystems. However, the set of studies used to focus on the upper soil profile down to usually a depth of 1 m. To our knowledge, only one study reached the threshold of 1 m depth concerning the influence of elevated atmospheric CO2 on root properties. Indeed, [START_REF] Duursma | Rooting depth explains [CO2]× drought interaction in Eucalyptus saligna[END_REF] found that root water uptake of Eucalyptus saligna plantation in Australia was higher at depth > 1 m when trees are subjected to higher atmospheric CO2 concentrations. Studies on the influence of elevated CO2 on root biomass production and distribution need to be carried in much greater detail, and particularly in deep soil layers.

IV.7 Deep fine root biomass and carbon sequestration

It is essential to assess more precisely the capacity of ecosystems to store carbon to predict their potential role on the mitigation of the future economic and ecological challenges linked to climate changes. More and more research effort focused on C accounting across ecosystems.

Fine roots play a major role in the global carbon cycle. They represent a significant C input to the soil by the incorporation of exudates and root necromass and generate a return of C to the atmosphere through respiration and decomposition processes (Balesdent and Balabane, 1996;Strand et al., 2008). Estimating fine root production, biomass and turnover throughout the entire soil profile is therefore compulsory in this context.

Even if root density decrease with depth, some studies evidenced that total root biomass below the threshold of 1 m depth can account for more than currently admitted. Indeed, Maeght et al. (2015) found that more than 50% of the overall fine root biomass was below 1 m depth in a rubber plantation in Thailand. Fine root biomass between 1.0 and 4.0 m was 5.8 t ha -1 and was only 4.8 t ha -1 in the soil layer 0-1 m. In line with those results, Pinheiro et al. (2016) found that fine root length below 0.5 m represented 61-77% of the total fine root length down to the root front in Eucalyptus plantations. In an agroforestry system in the south of France, Cardinael et al. (2015) found that 35% of the total fine root intersection densities of walnut trees were below a depth of 2 m. In the same site, using the minirhizotron technique, Germon et al. (2016) measured that 25% of total fine root production was observed below a depth of 4 m. et al. (2013) found that fine roots below a depth of 4 m represented 5%, 10% and 15% of total fine roots in year 1, 3.5 and 6 after planting of Eucalyptus plantation in Brazil. [START_REF] Li | Deep soil water extraction by apple sequesters organic carbon via root biomass rather than altering soil organic carbon content[END_REF] observed that rooting depth increased with increasing stand age, reaching 23.2 m in a 22-yearold apple orchard stand in a sub-humid region of China, and roots below a depth of 1 m accounted for 49% of the total root biomass. Therefore, deep roots represent a high proportion of the total root system and might contribute to sequestrating large amounts of C in soil [START_REF] Matamala | Impacts of fine root turnover on forest NPP and soil C sequestration potential[END_REF]Rasse et al., 2005) especially in deep soil layers (Kell, 2012).

Several studies have shown that root lifespan generally increases with soil depth (Hendrick and Pregitzer, 1996;Baddeley and Watson, 2005). [START_REF] Wells | Changes in the risk of fine-root mortality with age: a case study in peach, Prunus persica (Rosaceae)[END_REF] found that root longevity of Prunus persica L. significantly increased with soil depth down to 1.6 m. Germon et al. (2016) also found a higher proportion of walnut root mortality in the topsoil that in the deep soil layers with a median life span of 167 days within the first soil meter and 208 days at 2.5-4.7 m depth in an agroforestry system in the south of France. But on the contrary, Maeght et al. (2015) found that root life span decreased with soil depth down to a depth of 4.5 m in a rubber tree plantation in Thailand. Maeght et al. (2015) found that roots between the depth of 1 and 2.5 m had a turnover of about 180-250 days and roots below 3 m of soil depth had a turnover of about 120 days. Lambais et al. (2017) found no significant differences in root lifespan of Eucalyptus trees between the topsoil and a depth of 6 m in Brazil, but root mortality represented almost 20% in the topsoil and only 3.4 % between 5 and 6 m depth. It is known that environmental parameters (e.g., temperature, water content, N availability, CO2 and probably O2 partial pressure) influence fine root turnover to variable degrees (Vogt et al. 1996), which could explain the opposite trends observed by those studies. Fine root decomposition rate affects the ability of ecosystems to store organic C and act as a sink for CO2. The capacity of a different ecosystem to sequestrate carbon is related to the depth where roots are being decomposed. When roots are decomposed, parts of the former tissues are incorporated into the soil organic matter (Strand et al., 2008[START_REF] De Camargo | Soil carbon dynamics in regrowing forest of eastern Amazonia[END_REF] found that fine roots were being decomposed at least down to a depth of 5 m in eastern Amazon. Nepstad et al. (1994) estimated using isotopic tracers that C stocks below a depth of 1 m exceed organic soil C in the topsoil layer down to 1 m and the above-ground organic C in an Amazonian tropical forest. Indeed, the deep root system of this Amazonian forest input a large amount of organic carbon into the soil by root exudations, mycorrhizal associations and dead root tissues (Nepstad et al., 1994). Moreover, the microbial biomass is lower in deep soil layers than in the topsoil, which in combination with oxygen limitations could enhance organic C sequestration as a result of low mineralization rates (Taylor et al., 2002;Rumpel and Kögel-Knabner, 2011). Organic C derived from roots is generally more sequestered in the soil than organic C coming from the aboveground litter. The latter is more affected by physicochemical processes and has a different structural composition (Rasse et al., 2005;Schmidt et al., 2011;Menichetti et al., 2015). It is therefore essential to estimate fine root production, biomass and turnover, and associated microbial communities throughout the entire soil profile according to its environment to estimate adequately the overall C sequestration.

IV.8 Deep fine root functioning and nutrient mobilization

In addition to their importance for water uptake, deep fine roots may be essential to supply trees' nutrient requirements. Yet deep root functioning may vary over soil depth and the presence of roots in a given soil layer may not always correspond to root activity [START_REF] Phillips | A belowground perspective on the drought sensitivity of forests: Towards improved understanding and simulation[END_REF]. Indeed, [START_REF] Göransson | Estimating the relative nutrient uptake from different soil depths in Quercus robur, Fagus sylvatica and Picea abies[END_REF] showed that equal root abundance does not mean equal uptake of nutrients in Quercus robur L. plantations and that there is a contrasting potential uptake between deep and shallow layers. The depth of nutrient uptake performed by tree roots is commonly estimated using tracers. [START_REF] Bordron | Fertilization increases the functional specialization of fine roots in deep soil layers for young Eucalyptus grandis trees[END_REF] showed a functional specialization of Eucalyptus fine roots to take up cations varying over depth from 15 NO3 -, Rb + (K + analog)

and Sr 2+ (Ca 2+ analog) tracers injected at depths of 10, 50, 150 and 300 cm in a sandy Ferralsol soil in Brazil. They demonstrated that potential uptake of fine roots of 2-year-old Eucalyptus trees was significantly higher at a depth of 3 m than in the topsoil for Rb + and Sr 2+ . Da Silva et al. (2011) also found an increase of the uptake rates at depth for K + and Ca 2+ analogs compared to the topsoil in a 6-year-old Eucalyptus plantation, and on the contrary, they found that NO3 - uptake was higher in the topsoil than at 3 m. Therefore, trees show great flexibility in root development and on their capability to adjust resource uptake in layers where the resources are available [START_REF] Jackson | Rapid physiological adjustment of roots to localized soil enrichment[END_REF][START_REF] Hutchings | Foraging in plants: the role of morphological plasticity in resource acquisition[END_REF][START_REF] Robinson | Resource capture by localized root proliferation: why do plants bother?[END_REF]. The functional specialization of deep roots is important to reduced nutrient losses through deep drainage (Laclau et al., 2010). The previous estimations of nutrient leaching may therefore be overestimated, as they were not considering nutrient uptake by deep roots when measuring only soil water concentration and fluxes at depth.

Deep roots strongly influence the water cycles and are essential to sustain high tree transpiration in the dry season [START_REF] Kleidon | Assessing the role of deep rooted vegetation in the climate system with model simulations: mechanism, comparison to observations and implications for Amazonian deforestation[END_REF]Saleska et al., 2007). Soil water content monitoring and the use of hydrogen and oxygen isotopes allow to estimate at which depth root water uptake is performed [START_REF] Guderle | Using measured soil water contents to estimate evapotranspiration and root water uptake profiles-a comparative study[END_REF][START_REF] Beyer | A deuterium-based labeling technique for the investigation of rooting depths, water uptake dynamics and unsaturated zone water transport in semiarid environments[END_REF][START_REF] Koeniger | Review on soil water isotope-based groundwater recharge estimations[END_REF][START_REF] Trogisch | Spatio-temporal water uptake patterns of tree saplings are not altered by interspecific interaction in the early stage of a subtropical forest[END_REF][START_REF] Beyer | Examination of deep root water uptake using anomalies of soil water stable isotopes, depth-controlled isotopic labeling and mixing models[END_REF]. [START_REF] Stahl | Depth of soil water uptake by tropical rainforest trees during dry periods: does tree dimension matter?[END_REF] showed that 46.1% of the trees were extracting water at or below a depth of 1.2 m in a tropical rainforest. Trees developed efficient strategies for water resource acquisition in deep soil layers using deep roots, which may also help sustain shallow root functioning during drought through hydraulic redistribution [START_REF] Burgess | The redistribution of soil water by tree root systems[END_REF][START_REF] Domec | Native root xylem embolism and stomatal closure in stands of Douglas-fir and ponderosa pine: mitigation by hydraulic redistribution[END_REF][START_REF] Bleby | Water uptake and hydraulic redistribution across large woody root systems to 20 m depth[END_REF]. [START_REF] Burgess | Tree roots: conduits for deep recharge of soil water[END_REF] have demonstrated that Eucalyptus species have the capacity to redistribute water from wetter deep layers into shallow soil layers through roots. Furthermore, a modeling approach showed that the occurrence of rainfall events, changing from a week to another, had a strong impact on which depth water uptake occurs (Christina et al., 2017). Recently, [START_REF] Li | Deep soil water extraction by apple sequesters organic carbon via root biomass rather than altering soil organic carbon content[END_REF] showed that the extraction of deep soil water by the root system of apple orchard stands was mainly occurring at depths below 12 m in a sub-humid region of China. They also found that roots in the 1-12 m layer remained alive mainly to transport the water absorbed below 12 m as they might not extract additional water [START_REF] Li | Deep soil water extraction by apple sequesters organic carbon via root biomass rather than altering soil organic carbon content[END_REF]. Therefore, modeling processes need to consider deep root functioning to estimate net ecosystem productivity as a deep-water loss might contribute equivalently to the evaporation at the global scale than sallow soil water loss.

IV.9 Deep fine root and modeling approaches

Modeling architecture development and dynamics of the deep fine roots is hindered by the limited data available in the literature, yet indispensable to parametrize and evaluate the models.

Root number, root diameter, root volume, and root radial distances are the main parameters of root system biomechanics (Nicoll and Ray, 1996;Danquechin Dorval et al., 2016) However, most root functioning rules are still not completely understood, especially for the ones occurring at great depth due to the extreme difficulty of measuring those processes in situ.

Therefore, model calibration must cope with this knowledge and experimental limits.

Architectural models can also be coupled with models simulating nutrient uptake (Mayer, 1999;Bonneu et al., 2012;Mayer et al., 2012), water transport (Doussan et al., 1998) or rhizospheric processes (Kim and Silk, 1999) or even reactive transport model (Mayer, 1999;Mayer et al., 2012;[START_REF] Gérard | Modelling the interactions between root system architecture, root functions and reactive transport processes in soil[END_REF]. Nevertheless, it can be convenient to simulate accurately the overall architecture and any specialized functions of deep roots compared to shallow roots.

Furthermore, deep roots have a strong influence on deep carbon stocks, which represent a significant amount of carbon (Jobbágy and Jackson, 2004) and can be partially renewed at the 10-year scale [START_REF] Baisden | Bomb 14 C enrichment indicates decadal C pool in deep soil?[END_REF][START_REF] Koarashi | Dynamics of decadally cycling carbon in subsurface soils[END_REF]. Models predicting soil organic carbon stocks through a single soil layer modeling approach [START_REF] Hansen | Simulation of nitrogen dynamics and biomass production in winter wheat using the Danish simulation model DAISY[END_REF][START_REF] Sallih | Modelling of soil carbon forms after organic amendment under controlled conditions[END_REF][START_REF] Petersen | CN-SIM-a model for the turnover of soil organic matter. I. Long-term carbon and radiocarbon development[END_REF][START_REF] Pansu | Modeling organic transformations by microorganisms of soils in six contrasting ecosystems: Validation of the MOMOS model[END_REF][START_REF] Oelbermann | An evaluation of the century model to predict soil organic carbon: examples from Costa Rica and Canada[END_REF] are therefore not considering deep soil and their roots that play an active role in carbon cycling. In recent years, an awareness of the importance of deep carbon stocks by the modeling community has led to the development of different discretized models depending on the soil depth [START_REF] Braakhekke | SOMPROF: A vertically explicit soil organic matter model[END_REF][START_REF] Braakhekke | Modeling the vertical soil organic matter profile using Bayesian parameter estimation[END_REF][START_REF] Guenet | The relative importance of decomposition and transport mechanisms in accounting for soil organic carbon profiles[END_REF][START_REF] Taghizadeh-Toosi | C-TOOL: A simple model for simulating whole-profile carbon storage in temperate agricultural soils[END_REF]. However, modeling accurately deep root dynamics and their active role for carbon allocation, nutrient and water uptake according to the plant development over time remains a major challenge for the next decades. Table IV. 1: Root traits at depth compared to the top soil. indicates a predominantly positive trend, indicates a predominantly negative trend and indicates predominantly no effect. Categories of root traits and individual root traits are adapted from Brunner et al. 2015, Brunner et al. 2009, McCormack et al. 2012, Prieto et al. 2015.

Conclusion

CHAPTER 5: CONSEQUENCES OF CLEAR-CUTTING AND DROUGHT ON FINE ROOT DYNAMICS DOWN TO 17 M IN COPPICE-MANAGED EUCALYPT PLANTATION

We saw in chapter 4 that despite the actual insights about the importance of fine roots in depth, current knowledge of their dynamics is still extremely limited. The evaluation of the contribution of fine roots in deep soil layers is a real metrological challenge and, in fact, a major scientific lock, which is important to raise to study the sustainability of agroecosystems and forest plantation, as well as their resilience, in the context of global changes.

The central objective of this following chapter is to assess the effect of clear-cutting and drought on fine-root production throughout deep soil profiles down to the water table in coppicemanaged Brazilian eucalypt plantations. These effects were monitored before and after trees harvest in a coppice-managed Eucalyptus grandis plantation under two contrasting water

V.1 Introduction

Future climate projections predict longer and more severe dry periods in tropical and subtropical regions (Dai, 2011;He & Soden, 2017;Solomon et al., 2009). Extensive tree mortality triggered by drought and changes in rainfall patterns has been reported worldwide [START_REF] Allen | Climate-induced forest dieback: an escalating global phenomenon[END_REF][START_REF] Mcdowell | Drivers and mechanisms of tree mortality in moist tropical forests[END_REF][START_REF] Williams | Temperature as a potent driver of regional forest drought stress and tree mortality[END_REF]. Tree survival greatly depends on rooting system behavior and functioning (Christina et al., 2017b;Markewitz et al., 2010;Nepstad et al., 1994;[START_REF] Pierik | The art of being flexible: how to escape from shade, salt, and drought[END_REF], as plant growth is highly dependent on the absorptive function of fine roots for water and nutrients (Hinsinger, 2001). Fine roots also play a major role in the global carbon (C) cycle, representing significant C input into the soil by the incorporation of exudates and root necromass, and also generating a return of C to the atmosphere through respiration and decomposition processes (Balesdent & Balabane, 1996;Strand et al., 2008). Improving our understanding of how root systems respond to drought is therefore crucial for terrestrial biosphere models to predict the effect of climate change on tree survival and carbon sequestration in forest and tree-based ecosystems.

Plant species use a large range of rooting patterns to cope with periodic drought, from "drought tolerant strategies" with fine roots surviving in periodically dry soil, to "drought avoiding strategies" shedding fine roots from dry soil horizons while rapidly developing roots in moister areas (Bristiel et al., 2018;Brunner et al., 2015;Vries et al., 2016). Drought can increase the root-to-shoot ratio, the root area or root length-to-leaf area ratio, as well as the proportion of fine roots in deep soil layers and/or the specific root area (Ma et al., 2018;Markesteijn & Poorter, 2009;Zhou et al., 2018). Root growth peaks have been shown in deep soil layers during dry periods for eucalypt and rubber trees in tropical soils (Lambais et al., 2017;Maeght et al., 2015a). Drought tolerance strategies are common for herbaceous plants, while drought avoiding strategies are often adopted by trees in evergreen tropical forests (Brunner et al., 2015). Despite the crucial role of fine roots in coping with drought, root phenology remains poorly understood in comparison to leaf ecophysiology (Radville et al., 2016a).

Deep roots commonly reported as roots growing beyond 1 m in depth can play an important role in supplying water to trees (Kell, 2012;Pierret et al., 2016a). Trees can be deeply rooted (Canadell et al., 1996;Schenk & Jackson, 2002), and some studies suggest that very deep roots (at depths > 10 m) are common in highly weathered tropical soils (Broedel et al., 2017;Nepstad et al., 1994;Saleska et al., 2007). Even though low fine root densities are generally found at great depth (Pierret et al., 2016a), they can take up substantial amounts of water needed for tree survival during drought periods (McDowell et al., 2008;Nardini et al., 2016). Deep roots can also contribute to closing the biogeochemical cycles in tropical forests through nutrient uptake in deep soil layers (Bordron et al., 2018;Da Silva et al., 2011;Jobbágy & Jackson, 2004;[START_REF] Lehmann | Subsoil root activity in tree-based cropping systems[END_REF], which reduces nutrient losses by deep leaching (Laclau et al., 2010;Lehmann & Schroth, 2003). While many studies show that the role of very deep roots in tropical forest functioning and productivity has been greatly underestimated (Freycon et al., 2015;Jackson et al., 2000;Markewitz et al., 2010), as far as we are aware, fine root dynamics and mortality have never been studied at depths > 10 m.

Eucalyptus plantations cover more than 20 million hectares and account for around 8% of forest plantations in the world (Booth, 2013). The diversity of Eucalyptus species planted in tropical regions has led to a wide range of products and management practices (Gonçalves et al., 2013).

Although many Eucalyptus plantations are intensively managed to produce raw materials for industry (mainly pulp and paper, but also solid-wood products, fiberboards and charcoal for steel production), used as a domestic source of energy and also contributes to alleviating poverty in developing countries (Cossalter & Pye-Smith, 2003). Most eucalypt plantations are located in areas with low soil fertility and prolonged drought periods (Keenan et al., 2015).

Coppice management could be an adaptive solution to cope with water deficit in these plantations, because the sprouts growing on stumps are likely to benefit from the pre-existing root system that explores deep soil layers where water availability is generally higher than in the topsoil. The effects of clear-cutting on fine root dynamics in coppiced-managed forest plantations are poorly documented and tendencies are not clear. Sequential coring in Brazilian coppiced-managed eucalypt plantations showed that fine root density decreased in the 0-1 m soil layer in the first 60 days after harvesting, while fine root decomposition was accelerated (Mello et al., 2007). Fine root mortality exceeded fine root production after clear-cutting in Populus stands (Berhongaray et al., 2015). In contrast, Dickmann et al. (1996) observed little change in fine root production and mortality in the 0-1 m soil layer after clear-cutting in other Populus stands. While 50% of fine root biomass can be found below a depth of 1 m in tropical eucalypt plantations (Christina et al., 2011b;Laclau et al., 2013a), fine root dynamics in coppice-managed forests have only been studied in the upper meter of the soil profile.

Our study was carried out in Eucalyptus grandis (Hill ex. Maid) stands planted in a throughfall exclusion experiment in Brazil (Battie- Laclau et al., 2014b). We aimed to gain insight into the effects of contrasting rainfall regimes on fine root dynamics in coppice-managed eucalypt plantations after tree clear-cutting in very deep tropical soils. We put forward the hypothesis that trees invest in belowground biomass in response to throughfall exclusion, in order to increase the exploration of fine roots in deep soil layers (H1), and that they adjust fine root traits to increase the specific root area, in order to capture more resources per gram of C invested in fine roots (H2). In addition, we put forward the hypothesis that Eucalyptus grandis stands with clear-cutting and tree regrowth in coppices stimulate fine root growth in both shallow and deep soil layers (H3) and increase root mortality throughout the soil profile (H4).

V.2 Materials and Methods

V.2.1 Study site

The experiments were conducted at the research station owned by the Luiz de Queiroz College of Agriculture (ESALQ) near Itatinga (São Paulo, Brazil, 23°02′S 48°38′W). The study area, located 300 km from the sea, has a relief typical of the São Paulo Western Plateau, with a topography varying from flat to hilly (slopes < 3%). The altitude is 850 m, and the climate is humid subtropical with a dry winter (Cwa) according to the Köppen classification. Over the 15 years prior to this study, the mean annual rainfall was 1390 mm (with 74% between October and May), and the mean air temperature and relative humidity were 20°C and 77%, respectively. A dry and cool (15°C) season occurs between June and September. The total rainfall over the study period (from May 2015 to July 2018) was 5629 mm. The annual rainfall was 1,557 mm and 2,303 mm in 2016 and 2017, respectively. The soils are very deep Ferralsols (IUSS Working Group WRB, 2015) developed on Cretaceous sandstone. Clay content ranges from 160 mg g -1 soil in the topsoil to about 250 mg g -1 soil at a depth of 15 m, and clay minerals are mainly kaolinite (Christina et al., 2015).

V.2.2 Experimental layout

A split-plot experimental design was set up in June 2010 with a Eucalyptus grandis clone used in commercial plantations by the Suzano Company (São Paulo, Brazil). The experimental layout with 6 treatments and 3 blocks was described in detail by Battie- Laclau et al. (2014b).

We studied two treatments out of all those available in the experimental design: one treatment with undisturbed rainfall (+W) and one treatment with throughfall exclusion (-W), which was equipped with plastic sheets installed since September 2010, allowing the exclusion of 37% of throughfall (Battie- Laclau et al., 2014b). Treatments -W and +W were used to determine the water deficit effect. The trees were planted in June 2010 at a spacing of 3 m x 2 m with a stocking density of 1666 trees per hectare. The plots received a standard commercial fertilizer (at planting: 3.3 g P m -2 , 200 g m -2 of dolomitic lime and trace elements; at 3 months of age: 12 g N m -2 , 0.45 mol K m -2 applied as KCl) and herbicides were applied to avoid the presence of other understory species. In +W and -W, the eucalypt stands were harvested six years after planting, in June 2016, and the plantation was coppice-managed thereafter. Several new shoots were regenerated from the stumps after the clear-cut and 1 or 2 shoots per stump were selected to maintain the same stocking density and prevent the growth of additional new shoots. A third treatment served as a control, with undisturbed rainfall and no harvest (NH), to assess the clearcutting effect. Tree height and circumference at breast height were recorded each year after the clear-cut on 36 central trees per plot during the first rotation (May 2010 -June 2016) and during the second rotation in coppice (starting in June 2016).

V.2.3 Soil water monitoring

The volumetric soil water content (SWC) was monitored in the +W and -W treatments throughout the study period at half-hourly intervals using CS616 probes (Campbell Scientific Inc., Logan, UT, USA) installed at the following depths: 0.15, 0.5, 1, 2, 3,4,6,8,10,12,14 and 16 m, with 3 probes at each depth in block 1. Extractable water (mm) was calculated as the difference between the current soil water stock (mm) and the minimum soil water stock (i.e. lower limit of soil water content in mm) [START_REF] Granier | A lumped water balance model to evaluate duration and intensity of drought constraints in forest stands[END_REF].

V.2.4 Deep permanent pits for root phenology observations

Between February and March 2014, two deep permanent pits were excavated in +W and -W in block 1 to gain access to the complete soil profile from the top soil down to the water table. The pits were 1.5 m in diameter and reached a depth of 17 m and were located between four Eucalyptus trees (Figure V. 1) at a distance of 90 cm, 90 cm, 130 cm and 130 cm from each four trees respectively. The pit walls were made of concrete rings in direct contact with the soil.

Clear-colored roofs of the same diameter as the pits were used to prevent light and rain entering the pits. Platforms were set up at two-meter intervals in the pits, equipped with artificial lighting and fans used during working sessions, allowing access and safe work down to the water table (Figure V. 1). The high cost of opening up and securing these pits prevented further replications in the other two blocks. However, other measurements, including deep fine root sampling and tree growth were carried out in all three blocks, making it possible to extrapolate some of the observations made in the two deep pits. In October 2015, a third pit was excavated in the nonharvested treatment (NH) down to 3.5 m to determine the clear-cut effect.

V.2.5 Minirhizotrons

Fine root dynamics were studied through transparent polyvinyl chloride tubes (length:180 cm; inner diameter: 6.5 cm), commonly called minirhizotrons (Maeght et al., 2013). In October 2014, twenty-four transparent minirhizotrons were installed using a powerhead drill in the +W and -W treatments of block 1. Outside the pits, three minirhizotrons were inserted into the soil surface in the same plots a minimum of 10 m apart and at a distance of 90 cm from the trunk (Figure V. 1). Nine tubes were inserted into the pit walls down to a depth of 17 m: two tubes at a depth of 1 m and one tube at depths of 3.5,5.5,7.5,9.5,11.5,13.5,15.5 m (Figure V. 1). The tubes were inserted at a 45-degree angle and allowed an observation depth of 1.3 m below the depth at which they were inserted into the soil profile. In October 2015, 3 additional tubes were installed at the soil surface in the +W and -W treatments of blocks 2 and 3 (12 tubes in total) to increase the number of replications in the top meter. In October 2015, seven tubes were installed in the NH treatments (3 into the soil surface, 2 tubes inserted at depths of 1 m and 3.5 m into the pit walls).

Root dynamics were recorded using a circular scanner system (CI-600 Root Growth Monitoring System, CID, USA). This scanner was selected for the quality of the images it produces, an essential element for the analysis (Graefe et al., 2008). In order to have a significant stabilization period after soil disturbance from the installation, fine root monitoring began eight months after minirhizotron installation (Germon et al., 2016;Graefe et al., 2008). Eight images (21.59 x 19.56 cm, 100 dpi) per tube (43 tubes in total) were taken every two weeks for more than three consecutive years from May 2015 to July 2018: over one year before the clear-cut and two years after harvesting, in a coppice. Images were taken at a resolution of 100 dpi, as we obtained the same root lengths and diameter compared to images of 300 dpi and 600 dpi, and it was less time-consuming in the field than with a higher resolution.

V.2.6 Root image processing

WinRhizoTron™ software (Régent Instrument Inc., Quebec, Canada) was used to analyze more than 24,000 root images taken in the minirhizotrons. This software was chosen as it allowed the analysis of large number of images and overlayed the images to visualize the time evolution of the roots throughout the tubes. This manual root measurement program estimated the length and diameter of each root observed and stored each data item in a text file. By comparing two consecutive images chronologically, it was possible to estimate changes in root length and phenology features. Root mortality was evaluated based on the absence of growth over the entire study period up to the last images, when roots turned black and presented clear signs of decomposition (Germon et al., 2016;Lambais et al., 2017). For each fine root (diameter < 2 mm) we recorded the time of the first appearance, the diameter, the length over time, and the time of disappearance. In this study, we considered only root appearing during the study period.

V.2.7 Root length calculations

As described in Germon et al. (2016) and Lambais et al. (2017) the following metrics were used to estimate root production and the root elongation rate: living and dead root length production (LP, cm m -2 ) was calculated for each root as the individual root length (living or dead) at time t divided by the observed soil area of each image. The cumulative living or dead root length production (CLP, cm m -2 ) was calculated summing, at each time t, the individual length of all the roots observed, divided by the observed soil area of each image. The individual root elongation rate (RER, cm day -1 ) was calculated as the difference in individual root length observed between two consecutive sessions (t and t-1) divided by the time in days between t and t-1. The daily root elongation rate (DRER, cm m -2 day -1 ) was calculated by summing, at each time t, each individual root elongation rate of all the roots observed, divided by the observed soil area of each image. The mean root elongation rate (MeanRER, cm day -1 ) and the maximum root elongation rate (MaxRER, cm day -1 ) were calculated as the mean and the maximum of individual root elongation rates considering all the roots growing during the study period. LLP, CLP, RER, DRER, MeanRER and MaxRER were estimated for each treatment (+W, -W and NH), each soil layer and between consecutive image sessions over the entire study period.

V.2.8 Root sampling

In order to check the consistency of fine root dynamics in deep soil layers observed by the minirhizotron method, total fine root biomass, fine root length and fine root area down to the water table were measured in October 2017, i.e. 1.5 years after the clear-cut in the coppices (+W and -W) and 7.5 years after planting in NH. Fine roots (diameter < 2 mm) were sampled down to 17 m in the two treatments (+W and -W) inside the three blocks and in the nonharvested (NH) treatment inside one block. Four trees were randomly selected in each plot and soil samples were collected around each tree between the topsoil and a depth of 2 m and around 2 other trees between depths of 2 and 17 m (i.e. 12 sampling points down to a depth of 2 m and 6 further down to a depth of 17 m in the +W and -W treatments and 4 sampling points down to a depth of 2 m and 2 down to a depth of 17 m in the NH treatment). At each sampling position, soil layers at 0-0.2, 0.2-0.5, 0.5-1, 1-1.5, 1.5-2 m were collected using a cylindrical auger with an inner diameter of 4.5 cm. The Brazilian "cavadeira" tool, a cylindrical auger with an inner diameter of 9 cm and a length of 30 cm, was used to collect soil cores every 50 cm from 2 m down to a depth of 17 m. From each soil core, about 1.5 and 2 kg of soil was collected using the same methodology as described in Germon et al. (2018) and Christina et al. (2011b). To avoid contamination of the collected soil samples, only soil blocks from the inner part of the auger were considered. Total fresh soil mass was measured, and a sub-sample of 5 g was weighed in the laboratory to estimate the soil water content by drying the sample at 105°C for 72 h. Each soil sample was identified and stored at 4°C before being processed a maximum of 1 week after sampling. Living roots (i.e. living stele, bright color and elasticity) and dead roots (i.e. by sight, touch and flotation) > 1 cm long were carefully separated by hand after gentle washing away of the soil with tap water on a sieve with a mesh size of 0.5 mm. For the 0-0.2, 0.2-0.5 and 0.5-1 m soil layers, 10 % of the weight of each soil sample was used to estimate the mass of extremely fine roots (i.e. length < 1 cm). For the other soil layers 100% of the weight was considered. Living and dead roots more than 1 cm in length were scanned using a doublesided scanning procedure at a resolution of 800 dpi. Then, living roots and dead roots over > 1 cm in length and fragments of living and dead roots less than 1 cm in length were dried for 72h at 65° C and weighed (±0.1 mg). For the upper layers where only 10% of the weight of the soil was screened for living and dead roots < 1 cm in length, the mass of fragments was multiplied by 10 to estimate the mass of fragments of the whole soil sample. Root weight was then obtained for each soil layer, sampling position, treatment and block.

V.2.9 Root trait calculations

The fine root scans obtained where analyzed using WinRhizo Version Pro V. 2009c software (Régent Instruments Inc., Quebec, Canada) to estimate root lengths and areas per soil layer, sampling position, treatments (+W, -W and NH) and blocks. As described in Germon et al. (2018) the following metrics were used to estimate fine root traits. The specific root length (SRL, m g -1 , i.e. total length of scanned roots divided by their dry mass) and specific root area (SRA, cm 2 g -1 , i.e. total area of scanned roots divided by their dry mass) were calculated for each soil sample. Fine root mass density (g kg -1 soil) was calculated as the total root dry mass divided by the dry weight of the soil used for root separation. Fine root density (FRD, g dm -3 soil) was obtained by multiplying fine root mass density by the soil bulk densities (measured by the standard core method down to a depth of 17 m in each treatment). Fine root biomasses (FRB, g m -2 ) were calculated in each soil layer multiplying the mean fine root density by the soil layer volume (dm 3 ). The root area index (RAI, m 2 m -2 ) was calculated as the surface area and length of fine roots divided by the sampled soil area respectively. FRD, FRB, SRL, SRA, and RAI were obtained for each soil layer from the soil surface down to a depth of 17 m, for the sampling position, +W, -W and NH treatments, and blocks.

V.2.10 Statistical analyses

Linear mixed-effect models were used to test the effect of soil depth, treatment and the interaction between depth and treatment on cumulative length production (CLP), root elongation rate (RER), daily root elongation rate (DRER), mean root elongation rate (MeanRER), maximum root elongation rate (MaxRER), fine root density (FRD), fine root biomass (FRB), specific root length (SRL), specific root area (SRA), root area index (RAI) and root diameter for the whole soil profile. Blocks were considered as random effects and residues were modeled by a first-order autoregressive correlation model to account for the correlations between soil depths. Two-way analyses of variance (ANOVAs) were used to assess the effect of treatments and blocks for individual soil layers on CLP, RER, DRER, MeanRER, MaxRER, FRD, FRB, SRL, SRA, RAI and root diameter. Measurements within a given soil layer were considered independent, since the sampling positions were located near different trees in each treatment and plot. The homogeneity of variances was verified, and log-transformations were used when the residuals did not follow a normal distribution. Tukey's post-hoc Honest Significant Difference (HSD) was used to determine the significant differences between treatments. R software version 3.4.4 (Team R 2013) was used for all the calculations and statistical analyses with a 5% significance level. The "lmerTest" package was used to perform the linear mixed-effect models (Kuznetsova et al., 2017).

V.3 Results

V.3.1 Tree growth

Initial vertical growth was faster in the coppices than in the replanting: nine months after harvesting (in February 2011 for the replanting, and February 2017 for the coppices), mean tree height was 1.3 m and 1.5 m in the +W and -W replanted plots and was 2.7 m and 3.1 m in the +W and -W coppice plots, respectively (Figure V. 2). There were no significant differences in vertical growth between the +W and -W treatments for either replanting or coppice in the first 3 years after harvesting.

V.3.2 Volumetric soil water contents (SWCs)

In both the +W and -W treatments, rainfall events led to large variations in SWC (Figure V. 3).

At a depth of 0.5 m, SWC ranged from 5.9% to 15.8% in -W and from 7% to 19.4% in +W. At a depth of 14 m, SWC ranged from 9.9% to 10.9% in -W and from 11.3% to 18.1% in +W.

Over the study period, throughfall reduction led to a sharp decrease in SWC, on average, by 12.9 ± 4.9% from the topsoil to a depth of 16 m. The design turned out to be efficient in mimicking two contrasting rainfall regimes. At the end of the rainy season, the mean SWC values of the soil profile in April 2016, i.e. 2 months before the clear-cut, were 12.5% and 14.0% in -W and +W, respectively and in April 2017, i.e. 10 months after the clear-cut, there were 14.4% and 16.2% in -W and +W, respectively. After clear-cutting, the soil profiles were recharged with water due to the interruption of tree transpiration. In +W, the gravitational soil solutions reached a depth of 16 m only 10 months after clear-cutting, while in -W they reached a maximum depth of only 12 m 13 months after clear-cutting. Gravitational soil solutions did not reach the water table in -W over the study period (one year before the clear-cut and the first 2 years of coppice management).

V.3.3 Fine root length production

The highest cumulative root length production (CLP) over the study period was at depths > 4 m, in both +W and -W (Figure V. 4). In -W, CLP reached about 19 m m -2 at a depth of 13.5-14.8 m, and only 3.9 m m -2 in the upper 2.3 m of the soil profile. In +W, the highest CLP was found in an intermediate soil layer (5.5-6.8 m deep) with a CLP of 18.9 m m -2 . CLP reached about 12 m m -2 in very deep soil layers (13.5-14.8 m deep) and only about 2 m m -2 in the upper 2.3 m of the soil profile in +W. DRER peaks ranged from 1.5 cm m -2 day -1 in the topsoil to 94.7 cm m -2 day -1 at a depth of about 12 m in +W, and from 3.5 cm m -2 day -1 in the topsoil to 83.7 cm m -2 day -1 at a depth of about 14 m in -W. The maximum elongation rate of individual roots (MaxRER) reached 4.3 cm day -1 in -W and 3.0 cm day -1 in +W (Table V. 1) and was much higher at great depths than in the topsoil (data not shown). DRER values peaked at the end of the dry season in all the soil layers at depths > 6 m when SWC decreased in the upper soil layers ( Thus, DRER values were not necessarily correlated with soil water contents for a given soil layer. A synchrony between the decrease in cumulated extractable water in the topsoil and DRER peaks was observed in -W (Figure V. 6) after the clear-cut. Successive DRER peaks appeared more and more deeply at the end of the dry season when the extractable water stocks in the 0-2 m layer fell below about 80 mm. Table V. 1: Mean diameter (mm), maximum elongation rate of individual roots (cm day -1 ), number of roots observed and root mortality over 3 years in the minirhizotron images across all the soil layers, from the surface to the water table at a depth of about 17 m, in the undisturbed rainfall plot (+W) and the plot with 37% of throughfall excluded by plastic sheets (-W). ), total fine root necromass (g m -2 ), mean specific root length (m g -1 ), mean specific root area (cm 2 g -1 ) and mean root diameter down to a depth of 17 m in the undisturbed rainfall plots +W, in the plot with 37% of throughfall excluded by plastic sheets (-W), both in coppices and 1.5 years after the clear-cut, and in the non-harvested plot (NH), i.e. a 7.5-year-old tree plantation. Standard deviations are indicated. Different lower-case letters indicate significant differences between treatments +W and -W (p < 0.05). NH was not included in statistical analyses because the three soil coring replicates were located in the same plot.

V.3.6 Fine root traits

The total root area index (RAI) was significantly higher in -W (32.8 m 2 m -2 ) than in +W ( 26 In the NH, +W and -W treatments, depth had little effect on specific root length (SRL), specific root area (SRA) and fine root diameter (data not shown). SRL and SRA were significantly higher in -W than in +W, and similar values were observed in +W and NH, although the sampling in NH (pseudo-replication on one block) did not allow a confirmation with statistics (Table V

V.3.7 Fine root mortality

Cumulative dead root length in the minirhizotron images over the study period of 3 years across all soil layers accounted for only 6-7% of cumulative root length production, in both +W and -W (Table V. 1). Surprisingly, dead fine root length did not increase after clear-cutting and did not differ between depths and between the +W and -W treatments. Dead fine root mass estimated 1.5 years after clear-cutting amounted to 163.2 g m -2 in +W and 167.9 g m -2 in -W (Table V. 2).

V.4 Discussion

The main novelty of our results lies in the first direct observation of fine root phenology at depths of more than 10 m and derived knowledge raised from a comparison between the treatments. The consequences of tree harvesting on fine root dynamics in coppice-managed plantations raise specific questions never studied before along a deep tropical soil profile. Since the 1980s, the minirhizotron technique has been widely used to study fine root dynamics and turnover (Graefe et al., 2008;Maeght et al., 2013). Many studies have shown that the soil environment close to minirhizotrons can be modified relative to undisturbed soil [START_REF] Majdi | Does liquid fertilization affect fine root dynamics and lifespan of mycorrhizal short roots?[END_REF], which is likely to influence fine root dynamics. However, in our study the very low root mortality rates after clear-cutting revealed by minirhizotron monitoring was consistent with the small amounts of dead fine roots measured by soil coring. Despite some unavoidable limitations, direct observations from minirhizotron tubes or field rhizotrons is for now the most accurate way of studying fine root phenology in situ [START_REF] Dipesh | Estimating fine-root production and mortality in the biomass plantations[END_REF]Radville et al., 2016a).

V.4.1 Root behavior in response to drought

The main purpose of our study was to investigate whether fine roots explore very deep soil layers and do so more intensively when trees are subjected to prolonged drought periods. This study, carried out in a throughfall exclusion experiment and including a non-harvested plot, made it possible to assess the effect of clear-cutting under two contrasting rainfall regimes. In agreement with our first hypothesis, Eucalyptus trees responded to drought by increasing fine root densities at great depth. Previous studies in Brazil showed that Eucalyptus trees have the ability to explore very deep layers in soils without hindrance to root growth (Christina et al., 2011b;Pinheiro et al., 2016b). In a survey of 62 tropical tree species, Markesteijn and Poorter (2009) showed that trees increase belowground biomass and the proportion of deep roots in response to dry conditions. Root growth in deep soil layers can increase the amount of water available to sustain tree growth, which could be a key advantage for eucalypt trees in coping with severe drought events (Christina et al., 2017b).

After clear-cutting, fine root growth at more than 4 m deep was spectacular at the end of the dry season, whatever the water supply regime. Lambais et al. (2017) also showed flushes of fine root growth down to a depth of 6 m at the end of dry periods in a Brazilian eucalypt plantation. Fine root growth in deep soil layers was initiated when the extractable water content in the 0-2 m soil layer fell below a threshold of about 80 mm, which suggests that soil water content in a particular soil layer was not the main driver of fine root growth. Endogenous and exogenous factors are major drivers of fine root phenology [START_REF] Abramoff | Are above-and below-ground phenology in sync?[END_REF][START_REF] Moroni | Root distribution of Eucalyptus nitens and E. globulus in irrigated and droughted soil[END_REF][START_REF] Tierney | Environmental control of fine root dynamics in a northern hardwood forest[END_REF], but are difficult to disentangle in deep soil layers. The successive flushes of fine root growth from the topsoil to the deepest soil layers at the end of the dry season and the first months after the onset of the rainy season in +W and -W might have resulted from a rapid exhaustion of water resources in the topsoil, inducing tree roots to grow deeper in the soil (Billings, 2015;Schenk & Jackson, 2002). Furthermore, a strong increase in sugar sap concentration and sugar allocation belowground has been shown in forests during dry periods [START_REF] Pate | δ 13 C analysis of phloem sap carbon: novel means of evaluating seasonal water stress and interpreting carbon isotope signatures of foliage and trunk wood of Eucalyptus globulus[END_REF][START_REF] Scartazza | Combining stable isotope and carbohydrate analyses in phloem sap and fine roots to study seasonal changes of source-sink relationships in a Mediterranean beech forest[END_REF], which could be a physiological response to a rapid exhaustion of water in the top soil and could help to explain the root growth in deep soil layers at the end of dry periods in our study.

In agreement with our second hypothesis, Eucalyptus trees facing drought adapted their root morphology to maximize the root surface area to take up limited resources. SRL and SRA were higher in -W than in +W, which in combination with higher fine root densities led to a much higher root area index. In a meta-analysis, Ostonen et al. (2007b) showed that SRL response to drought varies greatly between species. While [START_REF] Arend | Provenance-specific growth responses to drought and air warming in three European oak species (Quercus robur, Q. petraea and Q. pubescens)[END_REF] did not observe any significant change in SRL, root area index and root tissue density for oak trees (Quercus sp.) exposed to drought, [START_REF] Olmo | Drought changes the structure and elemental composition of very fine roots in seedlings of ten woody tree species. Implications for a drier climate[END_REF] showed an increase in SRL and root tissue density under drought conditions for 10 tree species. Eucalyptus grandis trees coped with drought in our experiment by increasing their capacity to take up soil resources for a relatively low investment in belowground biomass. A large increase in SRL and SRA was recently shown throughout deep soil profiles down to 17 m deep for Acacia mangium Wild and E. grandis roots in response to the mixture relative to monospecific stands (Germon et al., 2018). Our study showed that Eucalyptus trees can modify fine root traits to enhance resource capture and the exploration of very deep soil layers to survive in a context of climate change, which contributes to maintaining water uptake during dry periods (Brunner et al., 2015;Christina et al., 2017b).

V.4.2 Key role of deep roots in coppice management

Contrary to our fourth hypothesis, relatively few roots were lost by mortality (< 10% out of all the roots observed over 3 years), which suggested that most of the root system remained functional after clear-cutting. The effect of clear-cutting on fine root mortality remains unclear in coppice-managed forest plantations. Unlike our observations, sequential coring in the 0-1 m soil layer showed a decrease in fine root density after harvesting coppice-managed E. grandis stands in Brazil (Mello et al., 2007). [START_REF] Wildy | Quantifying above-and below-ground growth responses of the western Australian oil mallee, Eucalyptus kochii subsp. plenissima, to contrasting decapitation regimes[END_REF] also showed high fine root mortality rates after cutting the trees in plantations of Eucalyptus kochii Maiden & Blakely subsp.

plenissima Gardner (Brooker), but the root system superstructure was sustained down to a depth of at least 4 m. [START_REF] Teixeira | Eucalyptus urophylla root growth, stem sprouting and nutrient supply from the roots and soil[END_REF] showed from sequential coring in the 0-0.6 m soil layer that fine-, medium-and coarse-root biomasses increased over time after harvesting coppicemanaged Eucalyptus urophylla S. T. Blake trees. Using the minirhizotron technique, Dickmann et al. (1996) showed an absence of root mortality for coppice-managed poplar clones. Our study suggested that 6-year-old Eucalyptus grandis trees have enough reserves within the root system and the appropriate edaphic surrounding conditions to maintain the fine root biomass established down to the water table after clear-cutting, which probably contributed to promoting early shoot growth (Brunner et al., 2015;Drake et al., 2013).

Fine root growth after clear-cutting started in the topsoil, then continued successively in deeper and deeper soil layers, which confirmed our third hypothesis, even though the lapse of several months after clear-cutting was not expected. This pattern might have resulted from high nutrient and water availabilities in the upper layers after harvesting Eucalyptus stands due to an interruption of tree water uptake and fertilizer application (Laclau et al., 2010). The asynchrony within the root system, delaying root growth in deep soil layers, might be a strategy for maximizing the water and nutrient uptake needed to meet the high demand of these fast-growing trees. Root growth occurred at a depth of 14 m less than one year after clear-cutting of coppicemanaged E. grandis trees, while the maximum depth reached by E. grandis roots one year after planting is about 7 m in very deep soils (Christina et al., 2011b;Laclau et al., 2013a). Deep roots can provide access to large amounts of water stored in the subsoil after clear-cutting and small fine root densities in deep soil layers can be sufficient to take up substantial amounts of water (Christina et al., 2017b). Low fine root mortality rates after clear-cutting suggest that coppice-management of Eucalyptus plantations might be a promising option for coping with water scarcity, since the pre-existing root system can provide access to water stored throughout deep soil profiles.

V.4.3 Carbon sequestration and implication for the management of eucalypt plantations Surprisingly, cutting the trees did not lead to an increase in root mortality throughout the soil profile, whatever the water supply regime. Fine roots play an active role in carbon (C) cycling in forest ecosystems, through respiratory processes, exudation and root mortality (Balesdent & Balabane, 1996;Marsden et al., 2008;Strand et al., 2008). The consequences of deep rooting on subsoil C stocks in tropical planted forests and other forest ecosystems remain poorly known [START_REF] Gao | Identifying a suitable revegetation technique for soil restoration on water-limited and degraded land: Considering both deep soil moisture deficit and soil organic carbon sequestration[END_REF]Harper & Tibbett, 2013;[START_REF] Meyer | Nitrogen and phosphorus supply controls soil organic carbon mineralization in tropical topsoil and subsoil[END_REF]Nepstad et al., 1994). On the one hand, the supply of fresh carbon might promote the activity of microbes and affect the stability of pre-existing organic matter through a "priming effect" (Derrien et al., 2014a;Fontaine et al., 2007;Kuzyakov et al., 2000). Promoting the mineralization of ancient C would result in high emissions of carbon dioxide (CO2) under aerobic conditions and of methane (CH4) under anaerobic conditions. However, a complementary study in our plots showed that CO2 and CH4 emissions did not increase significantly after clear-cutting in the coppice-managed stands compared to the non-harvested stand (Germon et al. in prep.). Gas emission rates after clearcutting in our experiment were therefore consistent with the low rates of root mortality observed. On the other hand, deep roots might also contribute to sequestrating large amounts of C in soil. Total below-ground carbon allocations account for about 20-30% of gross primary production in Eucalyptus plantations (Epron et al., 2012;Nouvellon et al., 2012a;Ryan et al., 2010). Fine root elongation rates were higher at great depth compared to the topsoil, with an increase in fine root density after the clear-cut in very deep horizons. Moreover, microbial biomass is lower in deep soil layers than in the topsoil, which in combination with oxygen limitations could enhance C sequestration as a result of low mineralization rates (Rumpel & Kögel-Knabner, 2011;Taylor et al., 2002). C from roots is generally retained more in the soil than C from aboveground litter, which is more affected by physicochemical processes and also due to structural composition differences between leaves and roots (Menichetti et al., 2015;Rasse et al., 2005;Schmidt et al., 2011). Further studies are needed to assess whether the management of Eucalyptus plantations in very deep soils could be an effective option to help mitigate the increase in CO2 in the atmosphere.

V.5 Conclusions

The fine root phenology of coppice-managed Eucalyptus trees under contrasting water supply regimes revealed unexpected low rates of root mortality. The early growth of the sprouts after cutting the trees benefited from the root system established over the previous rotation cycle, and the asynchrony of fine root growth depending on depth highlighted tree plasticity in response to soil conditions. Establishing deep root systems in tropical planted forests could help trees withstand the long drought periods expected under climate change in many tropical regions. Our study suggested that coppice management might be an interesting option in tropical Eucalyptus plantations, both to improve tree tolerance to drought and store carbon at great depth in the soil.

Appendix V. 2: Images scanned in minirhizotron tube comparing different image quality (100 dpi, 300 dpi and 600 dpi).

What to remember from Chapter 5?

The main results of this chapter are summarized in the following Table V. Specific root length (m g -1 )

Specific root area (cm 2 g -1 )

Fine root diameter (mm) .

CHAPTER 6: CONSEQUENCES OF CLEAR-CUTTING AND DROUGHT ON CO2, CH4 AND N2O PRODUCTIONS THROUGHOUT DEEP SOIL PROFILES IN COPPICE-MANAGED EUCALYPT PLANTATIONS

We saw in chapter 5 that harvesting did not lead to an increase in root mortality in the stands coppice-managed, whatever the water supply regime. Fine root biomass and root area index increased about 25 and 24 % respectively in the throughfall exclusion plot compared to the control plot down to a depth of 17 m. The changes in root distribution occurred mainly at depth > 7m. Therefore, the huge soil volume explored by fine roots might lead to significant CO2, N2O and CH4 productions within the entire rooting soil profile. A deeper root system could increase greenhouse gases emissions through an increase in production, respiration, exudation and decomposition processes.

The central objective of this following chapter is to assess the effect of clear-cutting and drought on greenhouse gases production throughout deep soil profiles down to the water table in coppice-managed Brazilian eucalypt plantations. These effects were monitored before and after trees harvest in a coppice-managed Eucalyptus grandis plantation under two contrasting water supply regimes.

This chapter presents the results of 1.8 years of greenhouse gases monitoring and is titled is "Consequences of clear-cutting and drought on CO2, CH4 and N2O productions throughout deep soil profiles in coppice-managed eucalypt plantations". Co-authors associated with this project are Lydie Chapuis-Lardy, Yann Nouvellon, Christophe Jourdan, Agnès Robin, Joannès Guillemot, Ciro Antonio Rosolem, José Leonardo de Moraes Gonçalves, Iraê Amaral Guerrini and Jean-Paul Laclau.

VI.1 Introduction

Climate changes are expected to increase the contrast between dry and wet seasons in tropical and subtropical regions (Dai, 2011;He & Soden, 2017;Solomon et al., 2009). Climate models predict longer and more severe seasonal droughts in the future, as well as more frequent extreme rainfall events during rainy seasons [START_REF] Chen | Soil nitrogen transformation responses to seasonal precipitation changes are regulated by changes in functional microbial abundance in a subtropical forest[END_REF]. Changes in precipitation regimes may also have important feedback effects on climate through a modification of carbon dioxide (CO2), methane (CH4) and nitrous oxide (N2O) fluxes in forest soils (Davidson et al., 2004;Hashimoto et al., 2007). Understanding how precipitation changes, and especially extended drought periods, influence greenhouse gas effluxes in forest soils is crucial to improve the prediction of terrestrial biosphere models.

The balance between production and consumption of CO2, CH4 and N2O in forest soils can be greatly affected by precipitation changes (Davidson et al., 2000b). Throughfall exclusion in tropical and subtropical forests has either decreased [START_REF] Cleveland | Experimental drought in a tropical rain forest increases soil carbon dioxide losses to the atmosphere[END_REF] or increased [START_REF] Van Straaten | Simulated drought reduces soil CO2 efflux and production in a tropical forest in Sulawesi, Indonesia[END_REF][START_REF] Wood | Strong spatial variability in trace gasdynamics following experimental drought in a humid tropical forest[END_REF] soil CO2 emissions, either increased consumption [START_REF] Wood | Strong spatial variability in trace gasdynamics following experimental drought in a humid tropical forest[END_REF] and production [START_REF] Cattânio | Unexpected results of a pilot throughfall exclusion experiment on soil emissions of CO2, CH4, N2O, and NO in eastern Amazonia[END_REF] of CH4 and either lowered (Davidson et al., 2004) and increased [START_REF] Cattânio | Unexpected results of a pilot throughfall exclusion experiment on soil emissions of CO2, CH4, N2O, and NO in eastern Amazonia[END_REF] soil N2O emissions. An increase in soil water contents inhibits gas diffusion within soil profiles to the atmosphere as well as microbial production and consumption of greenhouse gases [START_REF] Qi | Drying-Wetting Cycles: Effect on Deep Soil Carbon[END_REF]Sotta et al., 2007).

Root:shoot ratios generally increase in response to dry conditions as well as the proportion of deep roots (Germon et al., 2019;Markesteijn & Poorter, 2009), which can increase CO2 production due to higher root respiration.

Production of greenhouse gases by soil microorganisms and roots can change rapidly temporally and spatially, which makes modelling efforts challenging (Courtois et al., 2018;Drewitt et al., 2005). While most studies dealing with soil greenhouse gases effluxes address the spatial and temporal variations, the vertical distribution of soil respiration is little documented in very deep soils (Drewitt et al., 2005). Trees with roots at depths of more than 10 m are common in tropical forests (Broedel et al., 2017;Nepstad et al., 1994;Saleska et al., 2007). In a Brazilian Amazon forest, the consumption of CH4 occurred mainly in the upper 10 cm, the production of N2O mainly in the 0-25 cm soil layer whereas CO2 was produced down to at least a depth of 11 m (Davidson et al., 2004) . In another Amazonian forest, CO2 production in the 0.5-3 m soil layer accounted for 17 % of the total soil CO2 production (Sotta et al., 2007).

Even if microbial activity is low in deep soil layers (Fontaine et al., 2007), the huge soil volume explored by fine roots might lead to non-neglectable CO2, N2O and CH4 productions.

Fast-growing Eucalyptus plantations cover more than 20 million hectares and are expanding rapidly to produced raw material for the industry (paper, wood panels, and biofuel) as well as firewood and charcoal in developing countries (Booth, 2013). In Brazil, Eucalyptus plantations cover about 5.6 million hectares and are mainly established on deep soils with low fertility and many plantation areas are subjected to prolonged drought periods (Keenan et al., 2015). The management of Eucalyptus plantations through coppice has been practiced by forestry companies due to lower production costs, shorter rotations and faster financial returns compared to replanted stands (Gonçalves et al., 2013). The root system established during previous rotations makes possible a rapid regrowth from the stump after harvesting. Eucalyptus fine roots can explore rapidly after planting both the superficial soil layers and very deep soil horizons (Germon et al., 2019;Laclau et al., 2013) and allocate about 30% of the gross primary productivity belowground, for root growth, root respiration and C exudation (Epron et al., 2012;Nouvellon et al., 2012;Ryan et al., 2010). Coppice management constitutes an advantage over sites with pronounced stress conditions, as the established root system preserves carbon for the next generation. However, removing the aboveground parts of trees has a great impact on carbon balance and greenhouses gases emissions of the ecosystem. Clear-cutting increases the solar radiation transmitted to the soil, raising the soil temperature and soil water contents through an interruption of stand transpiration (Londo et al., 1999;Mello et al., 2007). This may induce an increase in microbial activity, the decomposition of harvest residues left at the soil surface and enhance fine root mortality and decomposition (Mello et al., 2007;Parfitt et al., 2001).As far as we know, concentrations of greenhouse gas in deep soil layers have never been quantified in tropical planted forests in response to throughfall exclusion and coppice management.

Our study aimed to assess the consequences of contrasting rainfall regimes on CO2, CH4 and in the topsoil to about 250 mg g -1 at a depth of 15 m (Christina et al., 2015). The local climate is humid subtropical (Cwa according to the Köppen classification) with a rainy season from October to May and a dry and slightly cold season from June to September. Over the last 15 years, the mean air temperature was 20°C, the relative humidity was 77% and the mean annual precipitation was 1390 mm.

VI.2.2 Experimental Layout

A split-splot experimental design was installed on 2 hectares in June 2010, with the planting of a Eucalyptus grandis clone used in commercial plantations (Suzano Company). Three fertilization regimes and two rainfall regimes were compared in 3 blocks to gain insight into the interaction between tree nutrition and water availability on tree functioning (Battie-Laclau et al., 2014a;Christina et al., 2015;Christina et al., 2018;Ployet et al., 2019). The experimental layout was described in detail in Battie- Laclau et al. (2014b). Each plot was made of 144 trees (12 rows with 12 trees per row, spacing 3 x 2 m) and each experimental unit consisted of 36 trees (excluding 3 buffer rows to avoid bordure effect). We studied two treatments out of the 6 treatments in the experimental design as well as a non-harvested control plot in the same stand:

• -W: plots were equipped with plastic sheets in September 2010 to exclude 37% of throughfall and fertilizers were applied to avoid any nutritional limitation of tree growth.

• +W: undisturbed rainfall and same fertilization as in -W plots

• NH: undisturbed rainfall and same fertilization as in -W and +W plots. Contrary to -W and +W, the trees were not harvested in June 2016.

Trees were planted in June 2010 and received at planting 3.3 g P m -2 and 200 g m -2 of dolomitic lime and trace elements. At 3 months of age, 0.45 mol K m -2 were applied as KCl and 12 g N m -2 . These fertilizers inputs are not limiting for the tree growth (Laclau et al., 2009). Herbicides were applied to avoid the presence of understory species. The Eucalyptus stands were harvested six years after planting, in June 2016, and coppice-managed thereafter. Several new shoots were regenerated from the stumps after the clear-cut and 1 or 2 shoots per stump were selected to maintain the same stocking density and prevent the growth of additional new shoots.

VI.2.3 Soil water monitoring and soil bulk density

Between February and March 2014, two deep permanent pits were excavated in the +W and -W treatments to set up sensors and to measure soil properties from the top soil down to the water table (Germon et al., 2019). The volumetric soil water content (SWC, m 3 water m -3 soil)

was monitored through the study period at half-hourly intervals using CS616 probes (Campbell Scientific Inc., Logan, UT, USA). Probes were installed in the +W and -W treatments at a depth of 0.15, 0.5, 1, [START_REF]IX.2.4 Root ingrowth bags[END_REF]3,4,6,8,10,12,14 and 16 m, with 3 probes at each depth in block 1. Soil bulk densities were measured by the standard core method down to a depth of 17 m in the +W and -W treatments. The total porosity was calculated from bulk density:

𝑇𝑜𝑡𝑎𝑙 𝑝𝑜𝑟𝑜𝑠𝑖𝑡𝑦 = 1 - 𝐵𝐷 𝑃𝐷
where BD is measured bulk density and PD is an assumed particle density of 2.65 g cm -3 (Davidson et al., 2006;[START_REF] Oerter | Greenhouse gas production and transport in desert soils of the southwestern United States[END_REF]Sotta et al., 2007). The soil water content was expressed as the percentage of water filled pore space (WFPS, %) and was calculated for each depth as the volumetric water content (SWC) divided by the total porosity.

VI.2.4 Gas sampling at the soil surface

Soil CO2 efflux was monitored in the +W and -W treatments using a dynamic closed-path Li8100 system equipped with a 20 cm diameter Li8100-103 respiration chamber (LiCor Inc., Lincoln, NE, USA). 54 PVC collars (9 per plot in treatments +W and -W and 3 blocks) were installed in May 2010 to sample different distances from the tree (Figure VI. 1), using the methodology described in [START_REF] Nouvellon | Soil CO2 effluxes, soil carbon balance, and early tree growth following savannah afforestation in Congo: comparison of two site preparation treatments[END_REF]. Soil CO2 efflux was measured every 14 days over 3 years from December 2014 to December 2017, which represented 1.5 year before the clear-cut and 1.5 year after the clear-cut. In October 2016, 27 PVC collars were installed in the NH treatment to measure soil CO2 efflux from November 2016 to December 2017.

Soil CO2, N2O and CH4 fluxes were measured simultaneously to the Li8100 measurements in the same plots. Chamber (diameter 40 cm, height 10 cm) collars were permanently set up in the +W, -W and NH plots (Metay et al., 2007). Four anchors were placed randomly in each plot at four distance from the trees, one month before the beginning of greenhouse gas efflux measurements (Figure VI. 1). Anchors were temporarily removed during stand harvest, then they were returned to the same location. Measurements were made every 14 days over one year from March 2015 to March 2016, then once a month between April 2016 and December 2017.

Soil CO2, N2O and CH4 fluxes were monitored over 3 months before the clear-cut and over 19 months after the clear-cut in the coppice-managed treatments +W and -W, as well as over 22 months in the NH treatment. The chamber atmosphere was sampled 4 consecutive times (0, 10 min, 20 min and 30 min after closure) during this period with 5 mL syringes previously purged.

Gas samples were analyzed using electron capture gas chromatography (CPG-ECD, at the Plant Production Department -FCA, UNESP, Botucatu, Brazil). Gas samples were analyzed in less than 36 hours after sampling (the validity of this period was verified in a preliminary study).

Concentrations of CO2, N2O and CH4 in soil air were calculated by comparison of integrated peak areas of samples with standard gases, which were used to make a four-point calibration.

Calibration was done for each sampling date. More than 4000 gas samples have been analyzed in our study.

Gas fluxes at the soil surface were calculated from the following equation:

𝐹𝑠 = ∆[𝐺𝑎𝑠] ∆𝑡 × 1 𝑆 × 𝑃𝑉 𝑅𝑇
where Fs is gas flux (µmol m -2 s -1 or nmol m -2 s -1 ),

∆[𝐺𝑎𝑠]
∆𝑡 is the slope of the regression line of gas concentrations (ppm or ppb) over time (s), S is the chamber surface (m 2 ), V the chamber volume (m 3 ), P the atmospheric pressure (Pa), R the perfect gas constant (8.3143 J K -1 mol -1 ) and T the temperature (K).

Cumulative soil CO2, N2O and CH4 fluxes were estimated for each PVC collar and each chamber using linear interpolations of fluxes between each measurement date for all treatments. [START_REF] Gana | Sampling and interpolation strategies derived from the analysis of continuous soil CO2 flux[END_REF] checked in a nearby eucalypt stand the validity of this method for CO2 effluxes in comparison with monitoring every hour using automatic Li-cor chambers. Annual estimates of gas fluxes were made for each individual flux chamber.

VI.2.5 Gas sampling at different soil depths

The permanent pits in the +W and -W treatments were 1.5 m in diameter and reached a depth of 17 m (Figure VI. 1). They were maintained by concrete rings to reduce potential soil collapse and disturbances of the soil system. To prevent light and rain entering the pits, clear-colored roofs of the same diameter as the pits were used. Platforms were set up at two-meter intervals in the pits, equipped with artificial lighting and fans used during working sessions, allowing access and safe work down to the water table (Germon et al., 2019). The high cost of opening and securing these pits prevented further replications in the other two blocks. However, other measurements, including CO2, N2O and CH4 effluxes, were made in the three blocks, making it possible to extrapolate some of the observations made in the two deep pits. In October 2015, a third pit was excavated in the non-harvested treatment (NH) down to a depth of 3.5 m to study the clear-cut effect.

Soil CO2, N2O and CH4 concentrations were measured at a depth of 0.1, 0.5, 1.0, 3.5, 7.5, 11.5 and 15.5 m (3 repetitions per depth, Figure VI. 1) in the +W and -W treatments and at 0.1, 0.5, 1.0 and 3.5 m depths (3 repetitions per depth) in the NH treatment. Soil-gas samples were collected using a passive method: a 20 mL syringe was driven into the ground at 1.2 m from the lateral pit wall for each sampling depth (to be sure to sample an undisturbed soil area) and remained permanently in the soil throughout the study period [START_REF] Chapuis-Lardy | Nitrous oxide fluxes from Malagasy agricultural soils[END_REF]Metay et al., 2007). Additional 1 m deep pits (3 per treatment in +W, -W and NH) were excavated to collect soil-gas samples at depths of 0.1, 0.5 and 1 m to increase the number of replications in the top meter, and then backfilled with soil horizons in their correct order. Soil gas was pumped from the inside of the pit (for permanent deep pits) or from the soil surface into a 5 mL syringe (after several "micropurge" to prevent gas sample from contamination).

This equipment was installed into the soil more than one month prior to the first soil gas measurement to allow for passive diffusion from the soil into the syringe. Soil CO2, N2O and CH4 concentrations were measured on the same days as CO2, N2O and CH4 effluxes at the soil Gas production at each depth was calculated as the difference between the flux across soil layers [START_REF] Risk | Soil CO2 production and surface flux at four climate observatories in eastern Canada[END_REF]. To estimate soil gas fluxes within the soil profile we used CO2, N2O and CH4 concentrations, soil physical properties and soil textural properties. Interlayer flux was determined from Fick's Lax in one dimension.

𝐹(𝑔𝑎𝑠) = -𝐷𝑠 𝛿𝐶 𝛿𝑧

where Ds is the gas diffusivity in the soil, C is the concentration and z is the depth. This approach assumes that the concentration profile is momentarily at steady state. This model provides an estimate of the production that occurred below the depth of the calculated flux. The flux rates from soil gas concentrations depend on the soil gas diffusion coefficient. Effective diffusivity was estimated using the model of [START_REF] Moldrup | Modeling diffusion and reaction in soils: IX. The Buckingham-Burdine-Campbell equation for gas diffusivity in undisturbed soil[END_REF], recommended for soils with clay contents < 30%:

𝐷𝑠 𝐷𝑜 = 𝜀 2.5

√𝜑

where Do is the diffusivity of gas in air assumed to be 0.138, 0.144 and 0.195 cm 2 s -1 for CO2, N2O and CH4, respectively, according to [START_REF] Massman | A review of the molecular diffusivities of H2O, CO2, CH4, CO, O3, SO2, NH3, N2O, NO, and NO2 in air, O2 and N2 near STP[END_REF], 𝜀 is air-filled porosity and 𝜑 is the total porosity [START_REF] Moldrup | Modeling diffusion and reaction in soils: IX. The Buckingham-Burdine-Campbell equation for gas diffusivity in undisturbed soil[END_REF][START_REF] Oerter | Greenhouse gas production and transport in desert soils of the southwestern United States[END_REF]. Air-filled porosity was calculated by difference between total porosity and soil volumetric water content at each depth.

VI.2.7 Statistical analyses

Linear mixed-effect models were used to test the effects of soil depth, treatment (+W and -W)

and the interaction between depth and treatment on CO2, N2O and CH4 concentrations in soil air, as well as CO2, N2O and CH4 productions for the whole soil profile at each measurement date. Blocks were considered as random effects and residues were modelled by a first-order autoregressive correlation model to account for the correlations between soil depths. Two-way analyses of variance (ANOVAs) were used to assess the effect of treatments (+W, -W and NH)

for individual soil layers on CO2, N2O and CH4 soil concentrations. CO2, N2O and CH4 fluxes at the soil surface were tested for statistical significance at each measurement date. The same analysis was made for cumulative CO2, N2O and CH4 fluxes over the study period. The homogeneity of variances was verified, and log-transformation were used when the residuals did not follow a normal distribution. Tuckey's post-hoc Honest Significant Difference (HSD)

were used to determine the significant differences between treatments. Linear regressions were used to identify the correlation between CO2 production and root biomass as well as soil CO2

effluxes measured with the closed chamber method and the close-path Li8100 system. R software version 3.4.4 (Team R 2013) was used for all the calculations and statistical analyses with a level of significance of 5%. The lmerTest package was used to perform the linear mixedeffect models (Kuznetsova et al., 2017). to December 2017 was 38.5 ± 12.7 % in the +W treatment and 31.7 ± 8.5 % in the -W treatment.

VI.3 Results

VI

At a depth of 0.5 m, WFPS ranged from 15.6% to 41.1% in the +W treatment and from 14.0% to 34.0% in the -W treatment. At a depth of 14 m, WFPS ranged from 34.7% to 53.7% in treatment +W and from 28.5% to 30.9% in treatment -W. At the end of the rainy season, mean WFPS in the 0-14 m soil layer were 37.9% and 30.7% in the +W and -W treatments, just before the clear-cut (June 2016), respectively, and 42.1% and 36.1%, 1 year after the clear-cut (June 2017). The soil profiles were refilled with water after the clear-cut as a result of an interruption in tree transpiration in coppice-managed stands. Water contents were lower in the -W treatment than in the +W treatment before the clear-cut and the difference between the two treatments persisted over the first 1.5 year after the clear-cut. effluxes over the study period ranged from 1.5 to 7.0 µmol m -2 s -1 in treatment -W and from 1.5 to 7.3 µmol m -2 s -1 in treatment +W. Cumulative surface effluxes the last year before the clearcut were 136.5 ± 21.8 and 130.3 ± 24.8 mol m -2 year -1 in treatments +W and -W, respectively, and they were 108.0 ± 15.8 and 119.3 ± 22.5 mol m -2 year -1 the first year after the clear-cut in coppice-managed stands (Figure VI. 3). These cumulative soil CO2 effluxes were not significantly different between treatments +W and -W. Soil CO2 effluxes measured with the home-made closed-chamber system exhibited the same seasonal pattern and similar range of values as the soil CO2 effluxes measured using the closed-path Li8100 system. The correlation between soil CO2 effluxes measured from October 2016 to October 2017 by the two methods was high (r 2 = 0.80), which suggests accurate estimates of N2O and CH4 fluxes using the closedchamber method at our site (Appendix VI. 1). The clear-cut did not significantly (p = 0.379) affect soil CO2 effluxes measured using the Li-8100 device (0.58 ± 0.19 and 0.47 ± 0.14 kg CO2 m -2 months -1 in NH and +W, respectively, from June 2016 to December 2017). Overlapping notches between boxplots suggest that the medians did not significantly differ. C) Cumulative soil CO2 effluxes (mol m -2 year -1 ) at yearly time scale in treatments +W (blue) and -W (orange), the last year before the clear-cut (between 5 and 6 years after planting) and the first year after the clear-cut in coppice-managed stands.

Soil CH4 effluxes ranged from -6.1 to -1.4 nmol m -2 s -1 in treatment +W (-3.7 ± 1.5 nmol m -2 s - 1 on average) and from -5.6 to -1.2 nmol m -2 s -1 in treatment -W (-3.3 ± 0.8 nmol m -2 s -1 on average) throughout the study period (Figure VI. 4). Negative effluxes of CH4 at soil surface indicated a net consumption of atmospheric CH4 by the soil. Similar cumulative soil CH4 effluxes over 1.5 year after the clear-cut between treatments +W and -W (F = 4.002, P = 0.465), as well as between treatments +W and NH (F = 3.262, P = 0.116), showed that throughfall exclusion and clear-cutting did not significantly influence soil CH4 effluxes (data not shown).

Soil N2O effluxes ranged from -0.09 to 1.68 nmol m -2 s -1 in treatment +W (0.48 ± 0.46 nmol m - 2 s -1 on average) and from -0.08 to 1.27 nmol m -2 s -1 in -W (0.43 ± 0.33 nmol m -2 s -1 on average) (Figure VI. 4). Similar cumulative soil N2O effluxes over 1.5 year after the clear-cut between treatments +W and -W (F = 0.675, P = 0.412), as well as between treatments NH and +W (F = 2.748, P = 0.616), showed that throughfall exclusion and clear-cutting did not significantly influence soil N2O effluxes (data not shown). productions were highest and CH4 production lowest in the upper soil layer (0-1 m), as a result of a large gradient of concentrations in the topsoil and high effective diffusivity. CO2 and N2O

productions at depths of more than 4 m were close to 0 throughout the study period, and CH4

productions were generally slightly positive in very deep soil layers (Figure VI. 6). At a depth of 0.1 m, CO2 production ranged from 0.4 to 4.6 µmol m -2 s -1 in treatment -W and from 0.9 to 6.7 µmol m -2 s -1 in treatment +W, CH4 production ranged from -26.4 to 21.3 nmol m -2 s -1 in treatment -W and from -41.1 to 5.2 nmol m -2 s -1 in treatment +W, and N2O production ranged from -5.2 to 3.8 nmol m -2 s -1 in treatment -W and from -4.4 to 6.4 nmol m -2 s -1 in treatment +W.

At a depth of 11.5 m, CO2 production ranged from -0.06 to 0.08 µmol m -2 s -1 in -W and from -0.04 to 0.03 µmol m -2 s -1 in +W, CH4 production ranged from -0.63 to 1.41 nmol m -2 s -1 in -W and from -0.13 to 0.41 nmol m -2 s -1 in +W and N2O production ranged from -0.20 to 0.04 nmol m -2 s -1 in -W and from -0.04 to 0.04 nmol m -2 s -1 in +W. CO2 production and fine root biomass

VI.4 Discussion

VI.4.1 Effect of depth on soil CO2, CH4 and N2O productions

The main novelty of our results lies in the first in situ measurements of CO2, N2O and CH4 concentrations at depths of more than 10 m in tropical planted forests, which made it possible to estimate the dynamics of production of major greenhouse gases in response to contrasting management and environmental conditions. While CO2 and CH4 concentrations increased sharply with depth throughout the soil profile, N2O concentrations where much less influenced by the depth. A strong increase in soil CO2 concentration with depth has been reported in deep tropical soils with an order of magnitude consistent with our results. Soil CO2 concentrations reached 80,000 ppm in a Brazilian Amazon rainforest (Davidson et al., 2004;Sotta et al., 2007;[START_REF] Trumbore | Belowground cycling of carbon in forests and pastures of Eastern Amazonia[END_REF], 30,000 ppm in a tropical rainforest in Costa Rica [START_REF] Schwendenmann | Long-term CO2 production from deeply weathered soils of a tropical rain forest: Evidence for a potential positive feedback to climate warming[END_REF] and 140,000 ppm in an agroforestry system in Indonesia (Van Straaten et al., 2010). The highest soil CO2 concentration reached 25,000 ppm in our study at a depth of 15.5 m. Physical, chemical, mineralogical and biological properties can change considerably throughout deep soil profiles (Davidson et al., 2006;Fierer et al., 2003;[START_REF] Oerter | Greenhouse gas production and transport in desert soils of the southwestern United States[END_REF]Wiaux et al., 2015). In our study, higher soil water contents in deep soil layers than in the topsoil led to a low proportion of air-filled pore space in deep soil layers and therefore a slow diffusion rate of the greenhouse gases to the atmosphere. Eucalyptus fine roots have been found down to the water table at a depth of 17 m in our experiment (Germon et al., 2019), and the deepest roots have an important functional role to withdraw water during dry periods (Christina et al., 2018).

The sharp increase in CO2 concentrations with soil depth might therefore reflect both CO2 production in deep soil layers through root respiration and microbial decomposition of organic matter (dead roots, exudates, dissolved organic matter,…) and slow upward diffusion rates of gas in soil layers with a high proportion of water-filled pore space (Davidson et al., 2004;[START_REF] Schwendenmann | Long-term CO2 production from deeply weathered soils of a tropical rain forest: Evidence for a potential positive feedback to climate warming[END_REF]Sotta et al., 2007). CO2 production estimates from Fick's law highlighted that CO2 production occurs mainly in the upper soil layers but small production rates occur down to a depth of 15 m. A low availability of microbial available C, very small nutrient concentrations in soil solutions and very low fine root densities in deep soil layers in our experiment (Germon et al., 2019;Laclau et al., 2010;Pradier, 2016) contributed to limiting the microbial activity (Fierer et al., 2003). The strong positive correlation between CO2 production and fine root biomass along the soil profiles suggest that Eucalyptus roots are probably the main source of CO2 in deep soil layers, both through root respiration and organic inputs decomposed by microbes. The same pattern was shown down to a depth of 7 m in a moist tropical forest (Davidson et al., 2004). The seasonality of CO2 production was stronger in the topsoil than in deep soil layers. CO2 production was close to 0 above a threshold of water filled pore space of 45% and small negative values of CO2 production were estimated in some deep soil layers. Negative values for CO2 production in deep soil layers have been reported in other studies (Davidson et al., 2004;[START_REF] Jong | Calculation of soil respiration and activity from CO2 profiles in the soil[END_REF][START_REF] Risk | Soil CO2 production and surface flux at four climate observatories in eastern Canada[END_REF]. We speculate that high transpiration rates of E. grandis trees in our experiment (Christina et al., 2018) might lead to a withdrawal of dissolved CO2 from deep soil layers to leaves through sap flow [START_REF] Aubrey | Root-derived CO2 efflux via xylem stream rivals soil CO2 efflux[END_REF][START_REF] Bloemen | Transport of root-respired CO2 via the transpiration stream affects aboveground carbon assimilation and CO2 efflux in trees[END_REF][START_REF] Ford | Soil DIC uptake and fixation in Pinus taeda seedlings and its C contribution to plant tissues and ectomycorrhizal fungi[END_REF][START_REF] Hanson | Root carbon flux: measurements versus mechanisms[END_REF]. Further studies are needed to quantify the flux of dissolved CO2 via the xylem as Eucalyptus transform almost all incoming energy into latent heat flux through transpiration [START_REF] Vezy | Measuring and modelling energy partitioning in canopies of varying complexity using MAESPA model[END_REF].

CH4 concentrations increase with soil depth in our study but they usually remain below the concentration in ambient air. CH4 concentrations higher than in ambient air were measured at a few sampling dates in deep soil layers. As in our study, Davidson et al. (2004) found some soil areas with high CH4 productions down to a depth of 11 m in a moist tropical forest. Spikes of CH4 concentration within the soil profile suggested that CH4 production occurred at various depths (down to 8 m) in a forest of the eastern Amazonia [START_REF] Verchot | Land-use change and biogeochemical controls of methane fluxes in soils of eastern Amazonia[END_REF]. We show a CH4 consumption in the topsoil and a weak CH4 production in deep soil layers whatever the water supply regime in our experiment. CH4 production primarily depends on the balance between two simultaneously occurring processes, production by methanogens and consumption by methanotrophic microorganisms (Dutaur & Verchot, 2007;Tate, 2015). Diffusion of gases are inversely proportional to the water-filled pore space. When the water-filled pore space decreases, the oxygen diffuses better and small changes in oxygen availability impact the balance between the two processes [START_REF] Sanz-Cobena | Do cover crops enhance N2O, CO2 or CH4 emissions from soil in Mediterranean arable systems?[END_REF]Wang et al., 2018). Indeed, drier soil condition enhance CH4 consumption whereas CH4 production is favored by microsites deprived of O2 in wet soil [START_REF] Davidson | Microbial processes of production and consumption of nitric oxide, nitrous oxide and methane[END_REF].

Surprisingly, soil N2O concentrations were little influenced by the depth in our eucalypt stands.

By contrast, [START_REF] Verchot | Land use change and biogeochemical controls of nitrogen oxide emissions from soils in eastern Amazonia[END_REF] showed a sharp gradient of N2O concentrations down to a depth of 8 m in a tropical forest of the eastern Amazonia, which suggested a low production in deep soil layers. N2O production in soils is driven by microbial nitrification (i.e. oxidation of NH4 + to NO3 -) and denitrification (i.e. reduction of NO3 -to N2O) (Bai et al., 2014;Ortiz-Gonzalo et al., 2018;Zhong et al., 2014). Soil microbes consuming N2O have been identified

recently [START_REF] Jones | The unaccounted yet abundant nitrous oxide-reducing microbial community: a potential nitrous oxide sink[END_REF][START_REF] Jones | Recently identified microbial guild mediates soil N2O sink capacity[END_REF][START_REF] Orellana | Detecting nitrous oxide reductase (nosZ) genes in soil metagenomes: method development and implications for the nitrogen cycle[END_REF][START_REF] Sanford | Unexpected nondenitrifier nitrous oxide reductase gene diversity and abundance in soils[END_REF], and the low changes in N2O concentrations with depth in our study might result from a simultaneous production and consumption throughout the soil profile. The diffusivity model estimated slightly negative N2O productions in some soil areas, which might a result of a reduction from dissolved N2O to N2 and/or a withdrawal from deep soil layers to leaves through sap flow [START_REF] Chapuis-Lardy | Soils, a sink for N2O? A review[END_REF].

VI.4.2 Effect of throughfall exclusion on soil CO2, CH4 and N2O productions Contrary to our first hypothesis, throughfall exclusion did not significantly influence CO2, N2O

and CH4 effluxes at the soil surface as well as the production throughout the soil profile estimated with the diffusivity model. In both treatments +W and -W, soil CO2 effluxes were within the range of measurements in tropical forest ecosystems [START_REF] Cattânio | Unexpected results of a pilot throughfall exclusion experiment on soil emissions of CO2, CH4, N2O, and NO in eastern Amazonia[END_REF]Davidson et al., 2004;[START_REF] Davidson | Effects of an experimental drought and recovery on soil emissions of carbon dioxide, methane, nitrous oxide, and nitric oxide in a moist tropical forest[END_REF]Nouvellon et al., 2012;Sotta et al., 2007). Higher CO2 effluxes in wet season than in dry season suggest that soil moisture could be a strong driver of soil CO2 emissions, as pointed out in other tropical and subtropical forests (Courtois et al., 2018;[START_REF] Davidson | Dissolved CO2 in small catchment streams of eastern Amazonia: A minor pathway of terrestrial carbon loss[END_REF]Davidson et al., 2004;Sotta et al., 2007). [START_REF] Davidson | Effects of an experimental drought and recovery on soil emissions of carbon dioxide, methane, nitrous oxide, and nitric oxide in a moist tropical forest[END_REF] also found strong seasonal variations and no significant differences between control and throughfall exclusion treatments on CO2 effluxes in an Amazonian forest. Unlike our observations, Sotta et al. (2007) showed in an Amazonian forest that CO2 effluxes were lower in a throughfall exclusion plot than in the control plot during the dry season, and no differences were found between the control plot and the throughfall exclusion plot during the wet season. Fine root area index in treatment -W (32.8 m 2 m -2 ) was significantly higher than in treatment +W (26.5 m 2 m - 2 ) in our 1.5-year-old coppice-managed Eucalyptus plantation (Germon et al., 2019), which may have offset the depressive effect of throughfall exclusion on microbial activity via a decrease in soil moisture.

In both treatments +W and -W, CH4 effluxes at soil surface were strongly negative over the entire study period, which shows a net consumption of atmospheric CH4 by the soil. CH4 consumption is common in nearly all types of aerated soils: in forests (Davidson et al., 2004;[START_REF] Davidson | Effects of an experimental drought and recovery on soil emissions of carbon dioxide, methane, nitrous oxide, and nitric oxide in a moist tropical forest[END_REF][START_REF] Nakano | Methane consumption and soil respiration by a birch forest soil in West Siberia[END_REF], deserts [START_REF] Hou | Growing season in situ uptake of atmospheric methane by desert soils in a semiarid region of northern China[END_REF][START_REF] Mclain | Moisture controls on trace gas fluxes in semiarid riparian soils[END_REF][START_REF] Oerter | Greenhouse gas production and transport in desert soils of the southwestern United States[END_REF], grasslands [START_REF] Fang | Low-level nitrogen deposition significantly inhibits methane uptake from an alpine meadow soil on the Qinghai-Tibetan Plateau[END_REF][START_REF] Mosier | Methane and nitrous oxide fluxes in native, fertilized and cultivated grasslands[END_REF] and tundra [START_REF] Whalen | Consumption of atmospheric methane by tundra soils[END_REF]. A wide diversity of methanotrophs in tropical soils might account for steady CH4 effluxes at the soil surface in treatments +W and -W despite strong seasonal changes in soil water contents [START_REF] Knief | Diversity of methanotrophic bacteria in tropical upland soils under different land uses[END_REF]. N2O effluxes at the soil surface were also similar in treatments +W and -W, with low seasonal variations. N2O effluxes were generally lower in dry season than in wet season in an Amazonian forest, and throughfall exclusion decreased the seasonal variability (Davidson et al., 2004). N2O production is favored in wet soils while dry conditions favor the production of NO (Davidson et al., 2000a;[START_REF] Firestone | Microbiological basis of NO and N2O production and consumption in soil. Exchange of trace gases between terrestrial ecosystems and the atmosphere[END_REF].

Interruption of tree transpiration after cutting the trees in our experiment led to high soil water contents in the topsoil over most of the study period, which might explain the low influence of treatments +W and -W on greenhouse gas effluxes.

While CO2, N2O and CH4 effluxes at the soil surface were not influenced by throughfall exclusion in our study, the concentrations of CO2 and N2O were 18.1 and 6.9% lower, respectively, and CH4 concentrations were 60% higher in treatment -W than in treatment +W.

Modeling effective diffusivity showed that the cumulated production rates of CO2, N2O and CH4 in each soil layer were similar in the two treatments. The effects of throughfall exclusion on gas concentrations throughout the soil profiles were mainly a result of the influence of soil water contents on soil gas diffusivity. High soil water contents in the +W treatment lead to a saturation of the pore-space with water, which results in a slow diffusion of greenhouse gases to the atmosphere also pointed out in other studies (Maier et al., 2017;Wang et al., 2018).

Throughfall exclusion experiments in tropical and subtropical forests show site-dependent responses to a decrease in throughfall for CO2, N2O and CH4 concentrations in very deep soil profiles (4 m deep or more). Throughfall exclusion can either decrease [START_REF] Cattânio | Unexpected results of a pilot throughfall exclusion experiment on soil emissions of CO2, CH4, N2O, and NO in eastern Amazonia[END_REF] or increase (Davidson et al., 2004), N2O concentrations in deep soil profiles and can lead to either similar (Davidson et al., 2004) or lower (Sotta et al., 2007;[START_REF] Van Straaten | Simulated drought reduces soil CO2 efflux and production in a tropical forest in Sulawesi, Indonesia[END_REF], CO2 concentrations than in control plots. CH4 concentrations in deep soil profiles were either similar (Davidson et al., 2004) or higher [START_REF] Cattânio | Unexpected results of a pilot throughfall exclusion experiment on soil emissions of CO2, CH4, N2O, and NO in eastern Amazonia[END_REF] in response to throughfall exclusion than in control plots.

VI.4.3 Effect of harvesting trees on soil CO2, CH4 and N2O effluxes Contrary to our third hypothesis, cutting all the trees did not lead to an increase in CO2, CH4 and N2O effluxes, whatever the water supply regime. Harvesting Eucalyptus trees in plantations managed in short rotations lead to huge changes in soil environment likely to enhance organic matter decomposition, with an increase in soil temperature and soil moisture as well as accumulation of harvest residues at soil surface (Christina et al., 2017;Mendham et al., 2002;O'connell et al., 2004;Rocha et al., 2016). Another study in our experiment showed that harvesting did not lead to an increase in root mortality in the stands managed in coppice, whatever the water supply regime (Germon et al., 2019). We speculate that the lack of effect of clearcutting on CO2 effluxes in our experiment may result from a decrease in root respiration after the harvest offsetting an increase in decomposition of organic matter at the soil surface.

Replanting present several drawbacks. Parfitt et al. (2001) showed that harvesting and replanting Pinus radiata resulted in a reduction of N status in soil, a loss of organic matter and an increase in soil respiration because roots from the previous rotation are decomposed and surface-soil microbial activity is enhanced following the clear-cut. Furthermore, harvesting and replanting are usually accompanied by considerable soil disturbance and also are longer exposed to wind and to erosion (Berhongaray et al., 2017). Coppice management might be an interesting option in Eucalyptus plantations managed in short rotation, to help mitigate the increase in CO2, CH4 and N2O in the atmosphere and to limit soil erosion compared to systematic replanting.

Very deep tropical soils cover large areas worldwide and improving our understanding of soilplant interactions throughout deep soil profiles is needed to improve the biogeochemical models used to predict the consequences of climate change on greenhouse gas effluxes in tropical planted forests. The dynamics of greenhouse gas concentrations in soil profiles result from the activity of microbial communities and can help gaining insight into the factors controlling biological activity in deep soil layers.

CHAPTER 7: GENERAL DISCUSSION AND PERSPECTIVES

The general objective of this study was to assess the effect of clear-cutting Eucalyptus stands managed in coppice on fine root production as well as CO2, N2O and CH4 fluxes throughout the entire soil profile, down to the water table, with a focus at great depth. The study was carried out in Eucalyptus plantations in Brazil, which has already been proven to be an excellent model to understand more precisely aboveground and belowground ecophysiological and biogeochemical processes (Laclau et al., 2010;[START_REF] Battie-Laclau | Potassium fertilization increases water-use efficiency for stem biomass production without affecting intrinsic water-use efficiency in Eucalyptus grandis plantations[END_REF]Pradier et al., 2017).

Two contrasting water regimes were studied to gain insight into the effects of drought periods that are predicted to be more frequent over the next decades. The current, natural water regime (+ W) was compared to a reduced water regime (-W), simulating a reduction in precipitation of about one third. Fine roots and greenhouse gases were sampled down to the water table (here located at a depth of 17 m) through large and deep wells, over one year before the clear-cut and two years after harvesting, in coppice-managed plantations as well as down to a depth of 4 m in a non-harvested plot (NH) serving as a control.

This study aimed to test four hypotheses: 1/ Eucalyptus trees are able to adapt their fine root dynamics depending on their environment to better access the soil resources, 2/ a change in fine root dynamics can occur between the topsoil and deep soil horizons when trees are subjected to drought conditions, 3/ throughfall exclusion can significantly affect greenhouse gas production and consumption within the soil profile by modifying gas diffusivity, 4/ coppice management increases the efflux of GHG as a result of fine root mortality and decomposition of harvest residues. The consequences of tree harvesting on fine root dynamics and the production of greenhouse gases over the first year of the rotation in coppice-managed plantations ask specific questions never studied in very deep soil layers.

Through this work, we wanted to answer four scientific questions:

1. What are the dynamics of eucalypt fine roots, CO2, N2O and CH4 concentrations throughout the entire soil profile down to a depth of 17 m?

2. Are fine root dynamics and fine root traits differently impacted by a change in water regime depending on soil depth?

3. What are the consequences of drought on greenhouse gas production in eucalypt plantations established in deep Ferralsols?

4. How clear-cutting affect root production and mortality but also greenhouse gas production in coppice-managed eucalypt plantations?

The work in this thesis consisted in collecting greenhouse gases down to a depth of 15.5 m, measuring greenhouse gas effluxes, collecting root samples down to the water table and monitoring root dynamics over 3 years (Chapters 5 and 6). This approach provided original results on fine root dynamics and greenhouse gas production in very deep soil layers in coppicemanaged Eucalyptus plantation subjected to two contrasted rainfall regimes. A modeling approach was then used to gain insight into the processes governing CO2 transfer at a local scale but revealed several issues that we could not overcome over the available time of 6 months at the end of the thesis (Additional work). Finally, this last chapter aims at discussing the results obtained throughout the thesis and is organized in two parts. In the first one, we discuss the contribution of deep roots in tree adaptation to drought conditions and the importance of considering the entire soil profile when evaluating stand-scale greenhouse gases emissions. In the second, we argue, according to an operational point of view, that coppice management might be an interesting option in tropical plantations to improve tree tolerance to drought and store carbon in deep soil layers. production in some parts of the world. Perennial plantations will be particularly affected by climate change, because a plot planted today must be able to cope with all the climatic conditions that will be encountered up to tree harvest, from a few years to several decades after planting. Predicting accurately the future climate is challenging. It requires complex models that consider many processes that can potentially greatly influence the predictions when the model is sensitive to some parameters. Yet, many processes are still not completely understood for deep rooted species, especially for the ones occurring at great soil depth. Deep rooting is common in tropical forests (Nepstad et al., 1994;Canadell et al., 1996;Jackson et al., 2000) where severe drought events are predicted to occur over the next decades. In tropical forest plantations, it is then crucial to focus the research efforts on the understanding of deep soil processes to assess the potential impacts of climate changes.

VII

Current climate models predict a reduction in rainfall associated with an intensification of dry seasons in many parts of the word, and in Brazil particularly. Assessing how trees will adapt to climate changes is a major challenge. Therefore, field experimentations simulating future climates are crucial to parameterize biogeochemical global models making it possible to predict how ecosystems will respond to climate changes.

Anthropogenic climate changes are caused mainly by greenhouse gas (GHG) emissions. GHGs refer to all gases of natural or anthropogenic origin that contribute to the greenhouse effect.

Potential efficiency of greenhouse gases regarding global warming is highly variable. By definition, the overall global warming potential of CO2 is equal to 1 and CH4 and N2O are 23 and 298 times more efficient to warm the earth over a 100-year period as compared to CO2, respectively. In the early 1990s, through the multiplication of scientific evidence and international conferences on climate (including the conference of Kyoto in 1997), the international community has become aware of the potential importance for climate changes of increasing concentrations of anthropogenic GHGs in the atmosphere (mainly CO2, N2O and CH4) and the need to reduce them. To reduce the concentrations of GHGs in the atmosphere, two types of actions can be considered:

1. Decrease sources, in other words, reduce the level of GHG emissions.

2. Increase sinks, in other words, favor the transfer and storage of GHGs in other compartments where they would be stabilized, for example, in the form of carbonate sediments, woody plant biomass and / or stabilized organic matter.

Our study puts forward the need to consider deep soil layers to evaluate both actions. Indeed, it is mandatory to study deep soil layers in order to quantify accurately C source/sink fluxes as part of the global carbon budget. Quantifying C fluxes in deep soil layers is needed to improve the biogeochemical models predicting the effect of drought periods on greenhouse gas effluxes, and to identify more sustainable silvicultural practices for tropical planted forests in a context of climate changes.

VII.1.2 Looking deeper to quantify sinks accurately

Our study in a 2-ha split-plot experimental design manipulating water availability contributed to evaluating the impact of rainfall reduction on the productivity and adaptability of Eucalyptus plantation in a context of global change. Our results clearly show that Eucalyptus trees facing drought invest more in belowground biomass to increase the exploration of fine roots in deep soil layers (Figure VII. 1). This adaptive strategy to drought stress of perennial plant species, investing assimilates to develop the deep root system, increases the availability of water stored in very deep soil layers to maintain tree growth during drought periods (Christina et al., 2017).

Furthermore, the increased surface of root in contact with soil through an adjustment of fine root morphology (SRA, SRL, diameter, Figure VII. 1) reflects a significant expression of root plasticity in response to limited soil resources (Hodge, 2004;[START_REF] Fort | Root functional trait syndromes and plasticity drive the ability of grassland Fabaceae to tolerate water and phosphorus shortage[END_REF][START_REF] Roumet | Root structure-function relationships in 74 species: evidence of a root economics spectrum related to carbon economy[END_REF].

A higher investment in deep roots in response to a rainfall reduction might also influence other key processes such as tree functional status (i.e. growth and senescence), C rhizodeposition and rhizosphere biogeochemical properties. For instance, we found a non-negligible production of greenhouse gases down to the water table, probably resulting from the respiration of fine roots

and their decomposition at depths of more than 10 m. On the other hand, deep roots might also contribute to sequestrating large amounts of C in soils (Pierret et al., 2016). We showed that fine root biomass increased in deep soil layers when the plantation was subjected to water deficit (Figure VII. 1). As long-term C sequestration is more likely to occur in deep soil horizons than in the topsoil [START_REF] Gill | Influence of soil depth on the decomposition of Bouteloua gracilis roots in the shortgrass steppe[END_REF], the increased C allocation to fine roots in deep soil layers could have significant role for mitigating global changes.

Consequently, because changing precipitations can greatly modify C allocation between soil layers, C sequestration must be studied not only the topsoil, but also throughout the whole soil profile explored by roots.

VII.1.3 Looking deeper to quantify sources accurately

Several studies reported that total below-ground carbon allocations account for 20-30% of gross primary production in Eucalyptus plantations (Ryan et al., 2010;Epron et al., 2012;Nouvellon et al., 2012). The results of our study emphasize that Eucalyptus roots do not only represent a non-negligible part of the biomass of the trees, but also that a large proportion is allocated at great depth, especially under drought conditions (Figure VII. 1). This is particularly of interest considering that plants play a major role in sequestrating CO2 from the atmosphere into the soil.

In order to assess the carbon fluxes from the soil to the atmosphere, we conducted measurements of CO2 fluxes along the soil profile and at the soil surface.

CO2 productions estimated with the diffusivity model were strongly correlated to the distribution of fine root biomass along the soil profile, down to a depth of 15.5 m. The CO2 production shifted to deep soil layer in response to throughfall exclusion, which could be due to a shift of root growth to deep layers likely to enhance tree water supply (Sotta et al., 2007;[START_REF] Schwendenmann | Effects of an experimental drought on the functioning of a cacao agroforestry system, Sulawesi, Indonesia[END_REF]. When decomposed, a part of the dead root tissues is incorporated into the soil organic matter (Strand et al., 2008). Microorganisms can be reactivated in response to the input of fresh organic matter. Specialized microorganisms develop rapidly and break down fresh organic matter. Their metabolites can activate a second class of specialized microorganisms, in dormancy, which can degrade the organic matter initially present and stored in the soil: this is the "priming effect" [START_REF] Fontaine | The priming effect of organic matter: a question of microbial competition?[END_REF]. We observed a decrease in greenhouse gas production in the upper layers and an increase in the deep layers in response to throughfall exclusion. Changes in deep soil conditions in response to water deficit might affect considerably the functioning and composition of microbial communities and therefore the production of CH4, CO2 and N2O. A study down to a depth of 4 m at the same site showed that total organic C and N concentrations in the rhizosphere increased with depth and in response to throughfall exclusion (Pradier, 2016). This increase can be explained by two major processes:

(i) the increase in the quantity of organic compounds released by deep roots, and/or (ii) an identical amount of organic compounds released but a difference in their residence time within the rhizosphere (Pradier, 2016). It is therefore essential to clarify the functional role of deep roots and associated microbial communities to estimate adequately the overall C sequestration and greenhouse gas emissions in tropical ecosystems.

Furthermore, the production of greenhouse gases shifted over depth under dry conditions in this study, showing that it is important to simulate the changes along the entire soil profile in biochemical models to estimate CO2 emissions under future conditions. Therefore, only considering greenhouse gas production in the topsoil layers will not be adequate to evaluate the impact of climate changes in tropical forest ecosystems over long time periods.

VII.2 Operational discussion: consequences for the management of tropical planted forests

Eucalyptus plantations are not natural forests and are devoted to the provision of wood products, as viticulture is devoted to wine production or coffee plantations to coffee production. The sustainability of Eucalyptus plantations requires the control of criteria and indicators of sustainable ecological and social management practices, but also economic and institutional aspects. Eucalyptus plantations cover large areas worldwide, with more than 20 million hectares. The large production of wood in fast-growing plantations helps to reduce the pressure on native forest to supply wood and especially the high emissions of greenhouse gases caused by deforestation. However, much remains to be done regarding environmental impacts, sustainable management and adaptation to global change in order to reconcile production issues and preservation of natural resources. In this perspective, our study contributes to demonstrating that coppice management of Eucalyptus plantations could be an interesting trade-off between economic, societal and environmental requirements.

VII.2.1 Coppice-managed forest plantations: an option to limit GHG emissions Regeneration of forest plantation by sprouting is a viable alternative for many production systems. More and more forest companies opt for coppice-managed Eucalyptus plantations instead of systematic replanting for cost and profitability reasons [START_REF] Gonçalves | Produtividade de plantações de eucalipto manejadas nos sistemas de alto fuste e talhadia, em função de fatores edafoclimáticos[END_REF].

About one third of commercial Eucalyptus plantations in Brazil have been managed in coppice management since 2010 (IBA, 2016). However, the consequences of this type of management on the functioning of deep roots have never been investigated in tropical planted forests.

Such a research effort is a prerequisite to orient the management of tropical planted forests toward a limitation of greenhouse gas emissions in the atmosphere. Our study shows that managing the eucalypt plantations in coppice after cutting the previous stand did not led to an increase in CO2, CH4 and N2O emissions (Figure VII. 2). Fine root mortality was very low the first year after the clear-cut when the plantation was coppice-managed (Figure VII. 1). The management in coppice after the clear-cut did not increase the production of dead roots and the subsequent release of CO2 resulting to fine root decomposition. Furthermore, coppicedmanaged plantations are less prone to erosion compared to replanted stands because the soil is exposed for a shorter period (Berhongaray et al., 2017). Hence, coppice management might be an interesting option in tropical Eucalyptus plantations, to help mitigate the increase in CO2, CH4 and N2O in the atmosphere and to limit soil erosion compared to systematic replanting.

VII.2.2 Coppice-managed forest plantations: an option for areas of climatic constraints

Our study also showed that coppice management for Eucalyptus plantation might be a promising option to face water scarcity. Indeed, we found an intensive root growth in very deep soil layers (depth > 14m) less than one year after the clear-cut, with only few roots lost by mortality. These findings are particularly impressive considering that E. grandis roots typically reach only a depth of 7 m at one year after planting in systematic replanting (Christina et al., 2011;Laclau et al., 2013). Root production and maintenance represent a significant cost to a plant's overall economy. The establishment of a deep root system requires the allocation belowground of large amounts of carbon, which is at the expense of the production of aboveground biomass. By maintaining the root system, coppice-managed Eucalyptus plantations preserve belowground biomass for the next generation. Our results suggest that the carbon cost to maintain the root system down to the water table could be lower than shedding roots and producing new roots when the plantation is coppice managed. Six-year-old Eucalyptus grandis trees in our experiment have enough reserves within the root system, with or without throughfall exclusion, and the appropriate edaphic surrounding conditions to maintain the fine root biomass after clear-cutting, which probably contributed to promoting the early shoot growth (Drake et al., 2013;Brunner et al., 2015).

The maintenance of a deep root system represents a double "safety net" for nutrients and for water uptake that are taken up throughout the entire soil profile before being lost for tree growth by deep drainage [START_REF] Mareschal | Nutrient leaching and deep drainage under Eucalyptus plantations managed in short rotations after afforestation of an African savanna: two 7-year time series[END_REF]. In tropical Eucalyptus plantations growing on highly weathered soils in regions with rainfall events of high intensity, deep roots can provide access to large amounts of water stored in the subsoil and can play a crucial role in nutrient capture, which is essential to avoid large losses of nutrients leached from the upper horizons (Laclau et al., 2010). Therefore, the pre-established root system in coppice-managed plantations can act as a safety net by catching up large amounts of nutrient released after tree harvest and probably contribute to reducing the risk of tree mortality during prolonged dry periods.

VII.3 Contributions of the study and perspectives

The outputs of this work are multiple (Figure VII. 1,Figure VII. 2) To our knowledge, it is the first time that fine root dynamics and greenhouse gas concentrations and productions are studied down to the water table (here at a depth of 17 m) in Eucalyptus plantations. The effects of water deficit in interaction with the consequences of clear-cutting in coppiced-managed Eucalyptus plantations have never been studied.

However, further studies dealing with the anatomical, architectural and functional characteristics of fine roots across very deep soil profiles should be carried out. These studies would help gain an insight into the potential impact of management practices on C, water and nutrient cycles in tropical regions. A better knowledge of microbial communities in terms of biomass and diversity, but especially in terms of metabolic capacity is also needed. Improving our understanding of the factors controlling microbial activity, nutrient and C availability and their interactions in deep soil layers is a major scientific lock to model the global biogeochemical cycles (Fierer et al., 2003;[START_REF] Jones | Role of substrate supply on microbial carbon use efficiency and its role in interpreting soil microbial community-level physiological profiles (CLPP)[END_REF][START_REF] Sosa-Hernandez | Subsoil arbuscular mycorrhizal fungal communities in arable soil differ from those in topsoil[END_REF].

From a methodological point of view, the field measurements in our study showed the great variability of GHG effluxes and the importance of monitoring the determinants of these emissions. Unlike micro-meteorological techniques, the closed-chamber method is simple, relatively inexpensive and can be installed on any type of field (forest, cultivated field, grassland ...). Problems related to the use of closed chambers (leaks, overpressure ...) can be avoided or minimized by an adapted methodology. The main limitation of this technique is the small area covered by the measurement, which may not encompass large-scale processes. A large number of samples in each treatment were set to catch the potential intra-plot variability, but those sampling efforts required a significant labor load and the measurements remained punctual in time and space. The use of automatic chambers allows to better capture the temporal fluctuations of greenhouse gas emissions [START_REF] Makita | Seasonal and diurnal patterns of soil respiration in an evergreen coniferous forest: Evidence from six years of observation with automatic chambers[END_REF]. This is particularly an advantage in places where environmental factors, contributing to the regulation of greenhouse gas emissions (such as soil temperature), lead to large differences in daytime / nighttime GHG effluxes.

In situ measurements are needed to explore the dynamics of greenhouse gas concentrations throughout soil profiles. However, manual in situ measurements require a lot of time and resources and are therefore often limited in time and space. Modeling makes it possible to interpolate in space and time the data acquired punctually. These interpolations are particularly interesting for the greenhouse gas effluxes that are characterized by strong spatial and temporal variations, as observed in this study. The sensibility of model outputs to specific processes can also be assessed by analyzing the differences between experimental and simulated data.

Moreover, models can be used to assess the consequences of contrasting scenarios on greenhouse gas production. Nevertheless, the mechanistic modeling of GHG effluxes still presents many uncertainties because the main factors used in the models (mineral N dynamics, water contents, organic C contents, soil temperatures, soil pH, …) and their interactions are not fully understood, in particular throughout deep soil profiles. Understanding how precipitation changes, and especially extended drought periods, influence greenhouse gas production in deep soils is crucial to improve the prediction of terrestrial biosphere models.

While many studies continue to consider only the upper 30 centimeters of soil, this work highlights the urgent need to study deep soil horizons in a context of climate change, not only for the evaluation of the changes in soil carbon sequestration, but also to quantify accurately the production of greenhouse gases. Comprehensive studies dealing with the microbial ecology of deep soil horizons in response to environmental changes and management practices are crucial to predict the behavior of huge soil volumes over the next decades.

VIII.1 Introduction

After a strong expansion in the last 20 years, forest plantations account for 7% of the total forest area in the world (Keenan et al., 2015). In tropical and subtropical regions, plantations of fastgrowing tree species store large amounts of carbon and contribute to reducing the exploitation of natural forests by providing an increasing proportion of the global demand of wood (Keenan et al., 2015). Fast-growing Eucalyptus plantations cover about 20 million hectares throughout the world (Booth, 2013) with about 5.6 million hectares in Brazil (IBA, 2016). In Brazil, most of Eucalyptus plantations are settled in areas with very deep soils (> 5m) with low fertility and prolonged drought periods (Gonçalves et al., 2013).

Future climate projections predict longer and stronger dry periods for eastern-south America (Solomon et al., 2009). In this context, coppice management of eucalypt plantations could be an interesting option to face water deficit because, after the harvest, the trees are likely to benefit from an already installed root system making it possible to access to deep soil layers where water availability is higher than in the topsoil. Our aim was to gain insight into the consequences of drought on fine root production and mortality as well as on the production of greenhouse gases down to the water table (at a depth of 17 m). These effects have been monitored before and after harvesting in a coppice-managed Eucalyptus grandis stand under two contrasting water supply regimes: the undisturbed rainfall as a control and 37% throughfall reduction to assess the effects of water deficit on tree and soil functioning.

The consequences of tree harvesting on root dynamics the first year of the rotation in coppicemanaged plantations ask specific questions never studied, particularly in deep soil layers. After the harvest, fine root mortality leads to an input of organic matter at different depths (Berhongaray et al., 2015). Decomposition of fresh organic matter may enhance the degradation of pre-existing organic matter, stabilized or not (Fontaine et al., 2007;Derrien et al., 2014) through a "priming effect" (Kuzyakov et al., 2000). The "priming effect" could affect carbon storage by the ecosystem and indirectly influence the nitrogen cycle. Most of the studies dealing with soil carbon storage are limited to the upper meter of the soil profile (Harper and Tibbett, 2013). The dynamics of CO2 concentrations across soil profiles down to a depth of more than 10 m have never been studied in tropical forest plantations.

We have studied fine root dynamics (production and mortality) using the minirhizotrons technique and measured the concentrations of CO2 down to the water table in the chapters 5 and 6. Root dynamics and gas concentrations were monitored before and after the harvest of After a careful evaluation of the reactive transport models in the literature and their advantages and constraints to be adapted to the specificity of our study site (in particular very deep soil and monitoring over a long period), we selected the Min3P model already in use at the UMR Eco&Sols. This model was used in order to try to carry out simulations of the biogeochemical processes coupled with the transport of water, solutes and gases in soil (Mayer et al., 2012).

Indeed, gas transport is highly dependent on soil moisture and modeling soil water fluxes is therefore compulsory. The fate of organic matter in very deep soil horizons remains poorly documented, which is a serious concern of the current modeling approaches of soil carbon dynamics (Fontaine et al., 2007;Rumpel and Kögel-Knabner, 2011;[START_REF] Mathieu | Deep soil carbon dynamics are driven more by soil type than by climate: a worldwide meta-analysis of radiocarbon profiles[END_REF].

A modeling approach was needed to answer to the following questions:

-What are the main transport and reaction processes accounting for the observed CO2 among models and infer their level of complexity [START_REF] Dunbabin | Modelling root-soil interactions using three-dimensional models of root growth, architecture and function[END_REF]. Root number, root diameter, root volume, and root radial distances are the main parameters of root system biomechanics (Nicoll and Ray, 1996;Danquechin Dorval et al., 2016). RootTyp model showed promising efficiency in modeling root system development of Quercu petraea [START_REF] Collet | Root system development of oak seedlings analysed using an architectural model. Effects of competition with grass[END_REF] but also several species with various structures [START_REF] Bingham | Simulation of wheat growth using the 3D root architecture model SPACSYS: validation and sensitivity analysis[END_REF][START_REF] Chen | Phenotypic variability and modelling of root structure of wild Lupinus angustifolius genotypes[END_REF][START_REF] Couvreur | A simple three-dimensional macroscopic root water uptake model based on the hydraulic architecture approach[END_REF]. RootTyp model is easy to calibrate while combining many processes of root system development: (1) emission of new roots from the shoot system, (2) elongation, (3) branching, (4) radial growth and (5) decay and self-pruning of existing roots.

This architectural model can also be coupled with models simulating nutrient uptake (Mayer, 1999;Bonneu et al., 2012;Mayer et al., 2012), water transport (Doussan et al., 1998) or rhizospheric processes (Kim and Silk, 1999) or even reactive transport model (Mayer, 1999;Mayer et al., 2012).

We aimed to couple a Numerical Model for the Analysis of the Geochemical Evolution of Mineral-Water-Air Systems (Min3P) with a simple root architecture model, Root-Typ (Pagès et al., 2004)

Definition of root types

The Root Typ parametrization started with the definition of root types. In order to represent the most accurately Eucalyptus root systems we defined 6 root types. They are described and listed The root segments are not indexed to the position, so we had to create each time intermediate types for the macrostructure to distinguish between proximal and distal systems.

• Type 1: Juvenile tap root, orthotropic root from the radicle.

• Type 2: Mature tap root, orthotropic root that follow the juvenile tap root by transformation, can be carried by plagiotropic roots.

• Type 3: Juvenile plagiotropic macrorhize, plagiotropic root from the juvenile tap root.

• Type 4: Mature plagiotropic macrorhize, plagiotropic root that follow the juvenile plagiotropic roots by transformation.

• Type 5: Intermediate roots between macrorhizes and brachyrhizes

• Type 6: brachyrhizes. Extremely fine roots.

Parameters needed for modeling

For each root type, several root parameters are needed for this dynamic developmental model.

There are listed below:

• Average and standard deviation of the insertion angle

Setting up a R routine for calculation of root length per volume of soil

In order to represent an accurate root system, we had to estimate the root length simulated per volume of soil. A R routine was coded using the output of the Root Typ model to compare the results simulated with the data obtained in the field.

Modification of root density and ramification varying within the soil profile

We modified the soil profile component of the Root Typ model to include changes in root density and ramification within the soil profile. We also increased the soil profile depth down to 17 m.

VIII.2.2

Main results obtained by simulations using the Root Typ model However, the improvement we made for the Root Typ model were important and more time is needed to parametrize and calibrate this model to tree root system development throughout an entire rotation. This work showed that the Root Typ model can be used to simulate tree root development over short period (up to 1-2 years) but more research is needed to simulate an entire rotation, as planned in our study. The two main issues rose in our project are listed and discussed here after.

Too much variability between seeds (simulations)

This is indeed a problem with stochastic models, when an event arriving early is very structuring for the future. In reality, compensating regulations operate, which are difficult to account for in this type of model. We should avoid in the setting up of the model, the very unlikely events that have a strong impact. For example, there must be a sufficient number of plagiotropic roots, varying their asymptotic lengths.

Exclusive pruning

All root branches have shorter root longevity than the bearing roots, therefore when branches are pruned the bearing axes become bare, which is never the case in the field. Therefore, a gap in the root length density was observed according to soil depth in the output simulations that we did not observe in field measurements within the entire soil profile.

Indeed, the fact of having a fixed lifespan for all roots belonging to the same diameter class generates unrealistic simulations. Several options could be tested in further studies, not necessarily exclusive:

• To create a root type that does not grow too fast with a wide range of length. Some will be pruned quickly and other should stay longer throughout the soil profile simulated

• To include into the code the possibility to have little branches (small branching densities) in such way that the longer roots carry some branches and therefore do not prune.

• To create a new root type of extremely fine roots that grow for longer period and branch or live longer than extremely fine roots that are pruned quickly.

• Include into the code a proximal reiteration regularly, to keep alive roots everywhere.

• Include into the code for a root lifespan different within the soil profile and for each root type.

Modeling architecture development and dynamics of deep fine roots are hindered by the limited data available in the literature yet indispensable to parametrize and evaluate the models. Root number, root diameter, root volume, and root radial distances are the main parameters of root system biomechanics (Nicoll and Ray, 1996;Danquechin Dorval et al., 2016), varying considerably with soil layers. The plasticity of root system architecture development responding to their environment is strongly influenced by soil depth. Root architectural models through a simulation in 3D space of the root system could simulate accurately spatial and temporal dynamics. But integrate into a model a vertically discretized soils is particularly important as shallow and deep roots present different spatial and temporal dynamics. Model parametrization needs to consider shallow and deeper-rooted root system behaving differently to environmental factors and soil conditions.

are considered: 1) passive solute uptake where the solute uptake rate is equal to the water uptake rate and 2) rejective or active solute uptake. Rejective uptake implies the solute to be left behind water during uptake by the root (leading to an increase of solute quantity in the root zone) and active uptake implies a preferential solute uptake by the plant root (leading to a solute depletion in the root zone). We were not able to use the outputs of the Root Typ model, so we estimated a relation between root length density, depth and time using root distributions along the soil profile measured at 1, 2, 3 and 7 years after planting. Root distributions were measured by soil coring (see Germon et al. (2018) and Christina et al. (2011) and Chapter 5 for the method). Model parameterization should be better described, particularly regarding the accuracy at which the root system and potential transpiration are simulated over time. Further studies dealing with long-term effects of rainfall regimes on soil water resources, could contribute to evaluating adaptive changes induced by drought periods in tropical Eucalyptus plantations.

plantations.

CO2 production during fine root decomposition and root respiration

Simulations should include CO2 gas emissions produced at each time step by fine roots (mortality and decomposition, root respiration, …). From these results, a comparison with the measurements of CO2 performed throughout the soil profile need to be performed to assess the main gas transport processes and sources.

CO2 production has been found to be correlated to root biomass throughout the soil profile (Chapter 6). Mechanistic biogeochemical models need to include the relationships between soil

CO2 production and soil water potential, soil temperature over time, but also fine root growth and root activity across soil layers. Indeed, incorporating the different level of processes of root

Conclusion

The modeling approach used in this thesis revealed promising efficiency in a model that couple root system architecture and functions, the Root Typ model, with reactive transport processes in soils, the Min3P model. Unfortunately, this thesis also revealed several issues that we could not overcome over the available time of 6 months at the end of the thesis. This chapter showed that additional experimental researches and model developments are required to assess the production of gas throughout the soil profiles and to infer the sensibility of gas production to environmental factors in this Eucalyptus plantation. Therefore, a specific thesis in modeling is required to reinforce and further explore the possibilities of coupling Min3P and RootTyp to gain insight into the processes governing greenhouse gases transfer at a local scale.

IX.1 Introduction

Plantations of fast-growing trees are expanding rapidly to meet the increasing demand for wood products (Keenan et al., 2015). The area covered by planted forests increased from about 168 million ha in 1990 to 278 million ha in 2015, and a large share of the new forest plantations are at sites with in highly weathered tropical soils (Keenan et al., 2015). Fast-growing Eucalyptus plantations cover about 20 million hectares throughout the world (Booth, 2013) with about 5.6 million hectares in Brazil (IBA 2016). Eucalyptus plantations provide raw material for pulp and paper, charcoal and firewood in Brazil (Battie- Laclau et al., 2014;Gonçalves et al., 2013).

While most of these eucalypt plantations are monospecific, mixed-species stands including nitrogen (N) fixing trees can help to balance the N budget, improve the N status of the eucalypts [START_REF] Forrester | Mixed-species plantations of Eucalyptus with nitrogen-fixing trees: a review[END_REF][START_REF] Paula | Evidence of short-term belowground transfer of nitrogen from Acacia mangium to Eucalyptus grandis trees in a tropical planted forest[END_REF] and, in some situations, increase the total biomass production [START_REF] Forrester | The spatial and temporal dynamics of species interactions in mixed-species forests: from pattern to process[END_REF][START_REF] Richards | The influence of mixed tree plantations on the nutrition of individual species: a review[END_REF]. Multi-purpose plantations can provide key ecosystem services [START_REF] Paquette | The role of plantations in managing the world's forests in the Anthropocene[END_REF], and positive relationships between tree diversity and soil fauna, microbial diversity, and soil carbon (C) sequestration are well documented [START_REF] Blaser | Woody encroachment reduces nutrient limitation and promotes soil carbon sequestration[END_REF][START_REF] Forrester | The spatial and temporal dynamics of species interactions in mixed-species forests: from pattern to process[END_REF][START_REF] Richards | The influence of mixed tree plantations on the nutrition of individual species: a review[END_REF]. Acacia mangium Wild is another fast-growing tree species widely planted in South-East Asia for pulpwood.

Introduction of Acacia mangium trees into commercial eucalypt plantations has been tested

recently in Brazil and Congo [START_REF] Bouillet | Eucalyptus and Acacia tree growth over entire rotation in single-and mixed-species plantations across five sites in Brazil and Congo[END_REF]Santos et al., 2016;[START_REF] Voigtlaender | Introducing Acacia mangium trees in Eucalyptus grandis plantations: consequences for soil organic matter stocks and nitrogen mineralization[END_REF]. Those studies showed that mixed A. mangium and Eucalyptus stands had higher available mineral N in the soil than monospecific eucalypt stands [START_REF] Tchichelle | Differences in nitrogen cycling and soil mineralisation between a eucalypt plantation and a mixed eucalypt and Acacia mangium plantation on a sandy tropical soil[END_REF][START_REF] Voigtlaender | Introducing Acacia mangium trees in Eucalyptus grandis plantations: consequences for soil organic matter stocks and nitrogen mineralization[END_REF] and that, in some situations, the total biomass production was higher in mixed stands than monospecific eucalypt stands at the same stocking density [START_REF] Bouillet | Eucalyptus and Acacia tree growth over entire rotation in single-and mixed-species plantations across five sites in Brazil and Congo[END_REF][START_REF] Epron | Partitioning of net primary production in Eucalyptus and Acacia stands and in mixed-species plantations: Two casestudies in contrasting tropical environments[END_REF]Santos et al., 2016). While the benefits consequences of a stratified canopy in mixed-species plantations are well documented [START_REF] Bauhus | Aboveground interactions and productivity in mixed-species plantations of Acacia mearnsii and Eucalyptus globulus[END_REF][START_REF] Binkley | Light absorption and use efficiency in forests: why patterns differ for trees and stands[END_REF][START_REF] Maire | Tree and stand light use efficiencies over a full rotation of single-and mixed-species Eucalyptus grandis and Acacia mangium plantations[END_REF][START_REF] Williams | Spatial complementarity in tree crowns explains overyielding in species mixtures[END_REF], soil partitioning between the roots of different tree species in a mixed stand has not been studied to the same extent.

Roots play a key role in forest ecosystems with their mechanical functions of tree anchorage and their physiological function of capturing and transporting the amounts of water and nutrients needed for plant growth (McCormack & Guo, 2014;[START_REF] Pregitzer | Fine root architecture of nine North American trees[END_REF]. Niche complementary among the fine roots of different species is often cited as one of the major processes that can contribute to increasing biomass production in multi-species stands compared to single-species forests (Lehmann & Schroth, 2003). Studies dealing with fine-root density in mixed-species forests are scarce and mainly limited to the upper soil layers. Deep roots, commonly defined as roots growing below 1 m, can provide access to water and nutrient pools that shallow roots cannot reach (Kell, 2012). Even though the density of roots is generally low below 1 m depth compared to the topsoil, they are important in reducing nutrient losses by deep drainage (Laclau et al., 2010) and improving trees' drought tolerance to drought (Christina et al., 2017a;McDowell et al., 2008). While the effects of environmental changes on the phenology of aboveground plant components are well documented, belowground processes remain poorly understood (Radville et al., 2016b). The lack of information on the influence of interspecific interactions on root exploration at great depth limits our ability to identify the most appropriate sites for multi-species plantations in tropical regions. Fine-root biomass in the 0-2 m soil layers was found to be 30% higher in a mixed-species plantation of E. grandis and A. mangium trees than in monospecific stands at age 5 years in Brazil (Laclau et al., 2013c).

Interaction between the two-species led to a segregation of the root systems. In mixed stands, A. mangium fine roots were partially excluded from the topsoil in mixture and over-explored the soil layers between the depths of 1 and 2 m relative to monospecific A. mangium stands (da [START_REF] Da Silva | Dynamics of fine root distribution after establishment of monospecific and mixed-species plantations of Eucalyptus grandis and Acacia mangium[END_REF]Laclau et al., 2013c). However, as far as we are aware, the effects of the interspecific interaction on fine-root densities at depths > 2 m have never been studied. Changes in fine-root traits might be a major adaptation of A. mangium and E. grandis trees to cope with inter-specific interactions in mixed stands. Strong modifications of fine-root morphology have been shown in response to competition through an increase in specific root length (SRL, fineroot length divided by fine-root dry mass) and specific root area (SRA, fine-root area divided by fine-root dry mass) to reduce the cost/benefit ratio of resource capture.

Root growth is controlled by endogenous constraints on carbon availability and environmental factors [START_REF] Freschet | Climate, soil and plant functional types as drivers of global fine-root trait variation[END_REF]McCormack et al., 2015). Fine-root production is dependent on soil water content [START_REF] Canham | Rapid root elongation by phreatophyte seedlings does not imply tolerance of water table decline[END_REF] and the high plasticity of fine roots enables them to explore resource-rich soil patches has been demonstrated (Hodge, 2004). The capacity of A.

mangium and E. grandis roots to explore soil patches might therefore vary depending on the season and the depth in the soil. Although ingrowth bags have been commonly used to estimate fine-root production in forest ecosystems (Brunner et al., 2013), the root-free soil in the ingrowth bags can be richer in nutrients and water than the surrounding soil (without water and nutrient uptake in the first weeks after installation), which can lead to overestimates of the fineroot production and length in these soil patches relative to the surrounding soil [START_REF] Bauhus | Soil exploitation strategies of fine roots in different tree species of the southern boreal forest of eastern Canada[END_REF]Jourdan et al., 2008).

Our study aimed to assess the consequences of mixing Acacia mangium and Eucalyptus grandis trees on fine-root growth down very deep profiles in highly weathered tropical soils. We hypothesized that the interaction between Acacia mangium and Eucalyptus grandis trees in mixed stands modified root growth relative to monospecific stands, resulting in i) fine-root over-yielding in all the soil layers down to the water table at a depth of 17 m, ii) modification of common fine-root traits (diameter, SRL, SRA) for the two species making it possible to increase the area of soil resource capture per gram of C invested in fine roots, and iii) a higher capacity of the tree roots to explore soil patches in the topsoil than in very deep soil layers reflecting the decrease in fine-root density with depth.

IX.2 Materials and methods

IX.2.1 Study site

The study was carried out at the Itatinga experimental station of University of São Paulo, Brazil (23°02' S., 48°38' W., 860 m a.s.l.). This region has a humid subtropical climate (Cfa according to the Köppen classification) with an average annual rainfall of 1390 mm (mean from 1990 to 2010), a mean relative humidity of 77% and a mean annual temperature of 19°C with a cold and dry season from June to September. The soils are Ferralsols (FAO classification) developed on Cretaceous sandstone with a water table at a depth of 17 m (Pradier et al., 2017). Sand content was around 85% in the topsoil and 75-80% between 1 m and 15 m depth (Maquere, 2008). Soil pHH2O was approximately 5.5 in the upper 3 m, cation exchange capacity decreased from 18 mmolc kg -1 in the 0-5 cm soil layer to 2 mmolc kg -1 in the 2-3 m layer, and exchangeable cation contents dropped below a depth of 5 cm. Full details were given in a previous study (Laclau et al., 2013c).

IX.2.2 Experimental Layout

The trial was a complete randomized block design with 7 treatments and of each species (50A50E). In the mixed stand, the two species were planted alternately in the row and offset adjacent rows (555 trees ha -1 per species). The Acacia mangium seedlings were inoculated with rhizobia strains selected by EMBRAPA (Agrobiology, Rio de Janeiro) for their N2 fixation capacities. The same amounts of P, K, Ca, Mg, and micronutrients were applied the first 18 months after planting in all the plots (no N fertilization). Destructive sampling at age 3.3 years showed that mixing the two species did not lead to higher aboveground biomass in 50A50E than the average of the two monocultures. Tree height was about 8 m higher for E.

grandis than for A. mangium (Table IX. 1). x 15 cm area at the soil surface (an operator used a tool designed to dig very deep holes, called 'cavadeira' in Brazil). Only the soil mass sampled was measured accurately, the volume of the soil samples extracted using the 'cavadeira' tool could not be measured and was estimated by multiplying the soil dry mass of the samples by the bulk density in each layer (see below).

About 15 kg and 30 kg of soil were collected at each sampling position for layers 50 cm and 100 cm thick, respectively. Fresh soil mass was measured in the field (±10 g) and all the fine roots easily visible were collected. The soil was then homogenized and a sub-sample of approximately 0.5 kg in the 0-50 cm soil layer, 1 kg in soil layers 0.5-1.0, 1.0-1.5, 1.5-2.0, 2.0-3.0, 3.0-4.0 m, and 2 kg in soil layers 4.0-5.0 and 5.0-6.0 m was taken to separate short lengths of root and small diameter fine roots in the laboratory. Each sub-sample was weighed in the laboratory and the soil water content was measured (by drying 5 g of soil at 105°C for 72 hours).

Below a depth of 6 m, soil cores were taken every 1 m depth using a cylindrical auger with an inner diameter of 9 cm and a length of 30 cm. We used the same methodology as Christina et al. (2011a) to avoid contamination of the soil samples collected at depth by roots from the upper layers. Only soil blocks from the inner part of the auger were collected and all fragmented soil pieces likely to come from upper soil layers were systematically discarded. All the soil collected from each layer was put in plastic bag, identified and stored at 4°C until processing (within 2 months after sampling). m or 6 m depending on the depth of the bag) were placed into the holes above the ingrowth bags to make possible to retrieve of each bag from the surface using a nylon cord attached (Appendix Appendix IX. 1). A plastic bag (with a nylon cord attached) filled with about 2 kg of soil was placed between the root ingrowth bag and the bottom of the PVC tube to avoid air diffusion from inside the PVC tube to the ingrowth bags that could affect fine-root growth. The top of each PVC tube was hermetically sealed. The mesh size of 2 mm allowed fine-root growth. After a period of 3 months, the bags were carefully retrieved. We set up additional ingrowth cores at the depths of 0.1 m and 1 m in the buffer rows of our experiment to check whether fine-roots were torn out when we pulled up the ingrowth cores 3 months after their installation.

Destructive soil sampling close to the ingrowth cores showed that most of the fine roots of the two species were sheared by the stainless-steel mesh when the core was retrieved, and the biomass of fine roots not recovered inside the soil core was negligible. Two periods were studied: from July to September 2013 (winter) and October to December 2013 (spring). Just after the bags were retrieve, new bags were inserted at the same place to study the following 3month period. All the fine roots in the samples were washed free of soil with tap water using sieves and separated carefully by hand. The roots of the two species were distinguished in the 50A50E treatment as described above.

IX.2.5 Statistical analyses

Two-way analyses of variance (ANOVAs) were used to assess the effects of treatments (100A, 100E and 50A50E) and blocks on fine-root densities (FRD), specific root length (SRL), specific root area (SRA), fine-root diameter, root length index (RLI) and root area index (RAI) for individual soil layers. Individual root biomass measurements within a given soil layer were considered independent since the sampling positions were located near different trees in each plot. We used linear mixed-effects models to test the effects of soil depth, treatment, and the interaction between depth and treatment (as fixed effect) on FRD, SRL, SRA, fine-root diameter, RLI and RAI for the whole soil profile. Blocks were considered as random effects and residues were modeled by a first-order autoregressive correlation model to account for the correlations between soil depths. A Shapiro-Wilk test was performed on the data before modeling and log-transformation was used when the residuals did not follow a normal distribution or were not homoscedasticity. In addition, two-way ANOVAs were carried out for each soil layer to compare the FRD of each tree species (E. grandis or A. mangium) in the mixed stands with 50% of the FRD in the monoculture of the same species in the same block. The effects of treatments and depth on FRD in the ingrowth bags were tested using two-way ANOVAs for each 3-month period studied. Post-hoc differences were analysed using Tukey's post-hoc Honest Significant Difference (HSD) to determine which means differed significantly between treatments. All calculations and analyses were performed using the R software version 3.2.2 (R development Core Team 2013) and the level of significance was 0.05. Linear mixedeffects models used the lmerTest package [START_REF] Kuznetsova | Package 'lmerTest'. R package version 2[END_REF]. For the graphical representations, the mean values and standard errors were calculated from all the replicates (n = 9 down to a depth of 6 m and n =3 below).

IX.3 Results

IX.3.1 Fine-root over-yielding

Auger sampling down to the root front (maximum depth of root observation) showed that trees in 50A50E, 100A and 100E exhibited a similar pattern of deep rooting. Fine-roots densities dropped sharply from the 0-0.5 m layer to the 0.5-1.0 m layer and decreased gradually down to a depth of 12 m in 100A and down to the water table at a depth of 17 m in 100E and 50A50E (Figure IX. 2). Mixing E. grandis and A. mangium led to fine-root over-yielding. Fine-root biomass in 50A50E (1127 g m -2 ) was 44% higher than in 100A (780 g m -2 ) and 58% higher than in 100E (714 g m -2 ) (Table IX. 2). Fine-root densities were 20-100% higher in 50A50E than in 100E and 100A in most of the soil layers and were at least twice as high in 50A50E as The main purpose of this study was to investigate whether roots explore very deep soil layers more intensively in mixed-species stands than in monospecific stands. In agreement with our first hypothesis, mixing A. mangium and E. grandis trees led to a strong fine-root over-yielding in all soil layers down to the water table at a depth of 17 m. Although fine-root over-yielding has already been reported in the upper soil layers for mixed stands compared to monospecific stands [START_REF] Brassard | Tree species diversity increases fine root productivity through increased soil volume filling[END_REF]Laclau et al., 2013c;[START_REF] Lei | Belowground facilitation and competition in young tree species mixtures[END_REF], the opposite has also been reported [START_REF] Bolte | Interspecific competition impacts on the morphology and distribution of fine roots in European beech (Fagus sylvatica L.) and Norway spruce (Picea abies (L.) Karst.)[END_REF], and other studies have shown similar fine-root biomasses in mixed and monospecific stands [START_REF] Bauhus | Aboveground and belowground interactions in mixed plantations of Eucalyptus globulus and Acacia mearnsii[END_REF][START_REF] Meinen | Biomass and morphology of fine roots in temperate broad-leaved forests differing in tree species diversity: is there evidence of below-ground overyielding?[END_REF]. A recent global meta-analysis across forests, grasslands, croplands and pot systems showed that mixed stands had, on average 28% higher fine-root biomass and 45% higher annual production than monocultures [START_REF] Ma | Effects of species diversity on fine root productivity in diverse ecosystems: a global meta-analysis[END_REF]. The originality of our results come from the strong fine-root over-yielding observed in soil layers at depths > 2 m. Competition for water and nutrients with the neighboring trees in mixed stands may force the roots to explore and tap deep soil layers (Cardinael et al., 2015;[START_REF] Ma | Effects of species diversity on fine root productivity increase with stand development and associated mechanisms in a boreal forest[END_REF]). While most of the studies dealing with fine-root distribution in forests have been limited to the upper 2 m of soil, 35%, 45% and 50% of the total fine-root biomass was found below 2 m in 100A, 50A50E and 100E, respectively. The difficulty of sampling deep roots can lead to underestimates of root mass and belowground productivity in tropical plantations and forests (Maeght et al., 2015b;Pierret et al., 2016b).

Studies quantifying total fine-root biomass down to the root front are scarce for trees growing in very deep tropical soils. Close to our study site (on the same soil type), the proportion of fine roots below 2 m depth was 20-30% of the total fine-root biomass down to the root front in a sweet orange orchard (Adriano et al., 2017) and 30-60% of the total fine-root length, depending on tree age, in eucalypt plantations (Laclau et al., 2013b;Pinheiro et al., 2016a). As commonly reported in forest ecosystems, fine-root densities dropped rapidly within the first topsoil layers then decreased gradually with soil depth, which corresponds to the distribution of nutrients in soil profiles [START_REF] Weemstra | Fine-root trait plasticity of beech (Fagus sylvatica) and spruce (Picea abies) forests on two contrasting soils[END_REF]. Interactions between tree species greatly increase the exploration of very deep soil layers in our study, which is likely to enhance the uptake of soil resources. Establishing a deep root system can also help tropical trees withstand the prolonged droughts that are expected to increase in the future (Christina et al., 2017a;Solomon et al., 2009). A modeling approach in a nearby eucalypt stand of similar productivity showed that very low densities of fine roots at depths > 10 m can withdraw substantial amounts of water during dry periods (Christina et al., 2017a). Mixing tree species could therefore enhance the resilience of tropical planted forests to climate changes increasing the access to water and nutrients stored in very deep soil layers.

Fine-root over-yielding in 50A50E is also consistent with the higher soil respiration rates relative to 100A and 100E at the end of the previous rotation (Nouvellon et al., 2012b). Roots are a major contributor to soil respiration (Gill et al., 2002;Marsden et al., 2008) and about 25% of terrestrial net primary production is due to fine-root production and turnover (McCormack et al., 2015). The total belowground C fluxes from 4 to 6 years after planting in the previous rotation of our experiment represented 24%, 26% and 32% of the gross primary production in 100A, 100E and 50A50E, respectively (Nouvellon et al., 2012b). Large amounts of C are stored at great depths in tropical soils [START_REF] Batjes | Total carbon and nitrogen in the soils of the world[END_REF] and changes in land use increasing the supply of fresh carbon might promote the activity of microbes through a priming effect (Derrien et al., 2014b;Fontaine et al., 2007). The increase in fine-root biomass, by replacing monospecific stands by mixed-species, may have consequences on soil carbon sequestration in deep soil layers that are poorly understood. Further studies are needed to assess whether an increase in the release of fresh C in very deep soil layers resulting from the combination of tree species could contribute to mitigating climate change through a sequestration of C or, on the contrary, would promote the mineralization of ancient C and therefore increase CO2 emissions.

IX.4.2 Root strategies in response to intra-and inter-specific interactions

In agreement with our second hypothesis, the interaction mechanisms between E. grandis and A. mangium trees led to large changes in A. mangium fine-root morphology. Previous studies at the same experimental site showed that E. grandis trees dominate the competition with A.

mangium trees capturing more light per tree and taking advantage of N fixation [START_REF] Paula | Evidence of short-term belowground transfer of nitrogen from Acacia mangium to Eucalyptus grandis trees in a tropical planted forest[END_REF]. The A. mangium leaves are below the canopy of eucalypt trees in mixed stands and fine roots are partially excluded from the upper soil layer (Laclau et al., 2013c;[START_REF] Maire | Tree and stand light use efficiencies over a full rotation of single-and mixed-species Eucalyptus grandis and Acacia mangium plantations[END_REF]. A. mangium trees adopt an intensification strategy [START_REF] Bonifas | Effects of nitrogen supply on the root morphology of corn and velvetleaf[END_REF][START_REF] Lei | Belowground facilitation and competition in young tree species mixtures[END_REF]Ostonen et al., 2007a) in competition with eucalypts, making it possible to increase the capacity to take up soil resources for a relatively low investment in belowground biomass.

SRL and SRA of A. mangium fine roots in mixed stands were 2-3 times higher than in monoculture, which, in combination with a large increase in FRD, led to a much higher root length index and root area index. While some studies in forest ecosystems also showed higher SRL and SRA in mixed stands than in monospecific stands, making it possible to reduce the cost/benefit ratio for resource capture [START_REF] Beyer | Fine root morphological and functional traits in Fagus sylvatica and Fraxinus excelsior saplings as dependent on species, root order and competition[END_REF][START_REF] Lei | Belowground facilitation and competition in young tree species mixtures[END_REF][START_REF] Sun | Positive effects of tree species richness on fine-root production in a subtropical forest in SE-China[END_REF][START_REF] Weemstra | Towards a multidimensional root trait framework: a tree root review[END_REF], those root traits were similar in mixed-species plantations and monocultures of A. mearnsii and E. globulus in Australia [START_REF] Bauhus | Aboveground and belowground interactions in mixed plantations of Eucalyptus globulus and Acacia mearnsii[END_REF]. In our study, A. mangium faced competition with E. grandis by altering the root absorption capacity, much more through morphological adaptations than changing the fine-root biomass of each A. mangium tree.

C starvation affecting the fine root architecture of A. mangium trees dominated by eucalypts as well as changes in mycorrhizal status seem to be potential factors. A recent study carried out in the same experiment showed large changes in the microbiological and chemical attributes of soil between the 100A and 50A50E treatments [START_REF] Bini | Eucalyptus grandis and Acacia mangium in monoculture and intercropped plantations: Evolution of soil and litter microbial and chemical attributes during early stages of plant development[END_REF], which suggests that changes in mycorrhizal status might be contribute to explaining the effect of eucalypts on the SRL and SRA of A. mangium roots. However, the mycorrhizal status was not directly measured, and we can only speculate about this effect. Differences in nodulation might contribute to explaining this pattern. Indeed, nodule density was much higher in monospecific A. mangium stands than in mixed A. mangium and E. grandis stands in the previous rotation at this site [START_REF] Bouillet | Mixed-species plantations of Acacia mangium and Eucalyptus grandis in Brazil: 2: Nitrogen accumulation in the stands and biological N2 fixation[END_REF]. However, nodules were mainly observed in the 0-50 cm soil layer and their density was low in the scanned roots.

Our results confirm the fine-root segregation between the two species in the mixed stand observed for the previous rotation at this site [START_REF] Da Silva | Dynamics of fine root distribution after establishment of monospecific and mixed-species plantations of Eucalyptus grandis and Acacia mangium[END_REF]Laclau et al., 2013c), with a partial exclusion of A. mangium roots from the resource-rich upper soil layers in mixed stands and a higher exploration of deep soil layers. However, the methodology was less intensive than in the previous studies of this effect (only one distance to the trees was sampled here and the 0-50 cm soil layer was not divided in several layers).

Eucalyptus grandis trees respond to competition with A. mangium trees through both an extensification strategy, leading to a sharp increase in fine-root biomass relative to monospecific stands, and an intensification strategy, increasing the volume of capture of soil resources relative to the fine-root biomass. However, the changes in SRL, SRA and fine-root diameter were non-significant in most of the soil layers, which suggests that the contribution of the intensification strategy was low. SRL and SRA values in our study are in the range reported down to a depth of 12 m for four Eucalyptus genotypes in nearby plantations (Pinheiro et al., 2016a). The total biomass of E. grandis fine roots was similar in 50A50E and in 100E despite a stocking density of eucalypt trees twice as high in 100E, which shows a remarkable plasticity of eucalypt trees to explore a huge soil volume, as already shown in Laclau et al. (2013c). In boreal forests, a comparison of fine-root production in mixed and single-species stands showed that fine-root production was correlated with nitrogen concentrations in the soil layers, and suggested that an enhancement of N availability in the mixed stands contributed to increasing fine-root production [START_REF] Ma | Effects of species diversity on fine root productivity increase with stand development and associated mechanisms in a boreal forest[END_REF]). We, therefore, speculate that facilitation mechanisms for E. grandis trees planted with A. mangium resulting from an increase in soil N availability [START_REF] Tchichelle | Differences in nitrogen cycling and soil mineralisation between a eucalypt plantation and a mixed eucalypt and Acacia mangium plantation on a sandy tropical soil[END_REF][START_REF] Voigtlaender | Introducing Acacia mangium trees in Eucalyptus grandis plantations: consequences for soil organic matter stocks and nitrogen mineralization[END_REF], could be involved in the extensification strategy leading to an increase in soil exploration by E. grandis fine roots. Such pattern might be pronounced in the superficial soil layers where eucalypt trees benefit from a rapid belowground N transfer from A. mangium trees [START_REF] Paula | Evidence of short-term belowground transfer of nitrogen from Acacia mangium to Eucalyptus grandis trees in a tropical planted forest[END_REF].

While many studies show that SRL, SRA and fine-root diameter can change depending on soil depth (Bakker et al., 2009;Makita et al., 2011;Maurice et al., 2010;Prieto et al., 2015), we did not observe clear patterns down the soil profile for either species. The same type of study carried out down to the root front in other eucalypt and orange plantations in Brazil also showed a high variability of SRL, SRA and fine-root diameter between soil layers but without a clear correlation with the depth (Adriano et al., 2017;Pinheiro et al., 2016a). A study carried out in 20 plant communities sampled in tropical, Mediterranean and montane regions showed that some fine-root traits were significantly different between shallow and deep soil layers, but absolute differences were small for most of the traits measured (Prieto et al., 2015). Our results

suggest that E. grandis and A. mangium fine roots in mixed stands reflect an acquisitive resource strategy [START_REF] Freschet | Climate, soil and plant functional types as drivers of global fine-root trait variation[END_REF]McCormack et al., 2015). Further studies in eucalypt and acacia plantations should examine other important root traits (in particular tissue density, concentrations of nutrients, cellulose, lignin and carbohydrate) to gain insight into the cost to the trees of investing in fine-root production in very deep soil layers.

IX.4.3 Fine-root production

Even though the fine-root production of A. mangium and E. grandis trees exhibited a strong seasonal variability, the decrease in fine-root density with soil depth did not modify the production of fine roots in the ingrowth bags down to a depth of 6 m. This pattern is contrary to our third hypothesis and shows a huge capacity of very deep roots to explore resource-rich soil patches despite their low density in the soil. The production of fine roots in the ingrowth bags was however much higher for E. grandis trees than for A. mangium trees, which is consistent with the faster growth rates of E. grandis trees shown both aboveground and belowground [START_REF] Da Silva | Dynamics of fine root distribution after establishment of monospecific and mixed-species plantations of Eucalyptus grandis and Acacia mangium[END_REF]Nouvellon et al., 2012b). Fine-root production in the ingrowth bags confirmed the strong over-yielding in mixed-species stands relative to the monocultures suggested by the fine-root densities. However, fine roots sampled in ingrowth bags can be different from fine roots sampled in undisturbed soil and productions estimated from ingrowth bags should be interpreted with caution [START_REF] Bauhus | Soil exploitation strategies of fine roots in different tree species of the southern boreal forest of eastern Canada[END_REF]Jourdan et al., 2008). Nevertheless, the same ingrowth bags were installed at all the depths in all the treatments, making it possible to compare the capacity of fine roots to explore soil patches.

The production of A. mangium fine roots in the ingrowth bags was much more affected by the season (winter vs spring) in the topsoil than in deep soil layers, as reported for phreatophytic species (Canham et al., 2012). E. grandis trees are better adapted to the cold climate in winter at our study site than A. mangium trees, which could account for the higher fine-root production in the topsoil in E. grandis monoculture and mixed-species stands than in A. mangium monoculture. A strong influence of exogenous factors such as soil temperature and water content [START_REF] Canham | Rapid root elongation by phreatophyte seedlings does not imply tolerance of water table decline[END_REF], as well as endogenous factors such as photosynthate availability, on fine-root phenology is well documented (McCormack et al., 2015).

In conclusion, our study shows that mixing species can lead to a strong fine-root over-yielding in very deep soil layers. We demonstrate that E. grandis and A. mangium trees growing in mixed stands can explore more intensively deep soil layers than their respective monospecific stands.

Studies dealing with deep rooting are needed for other tree species, soils and climates to assess whether increasing the diversity in tropical planted forests could increase their resilience to climate change by providing access to more soil resources than monospecific stands. A better comprehension of the effects of fine-root growth and turnover in very deep soil layers on soil carbon stocks is also needed to better assess the long-term consequences of afforestation with fast-growing tree species on the global carbon cycle.

  m de profondeur. Sept tubes ont été installés dans la parcelle de référence en surface, et à 1 et 3.5 m. L'observation des racines est réalisée par acquisition d'images par un scanner circulaire (CI-600 Root Growth Monitoring System, CID, USA). Huit images (21.59 cm x 19.56 cm) par tube sont prises toutes les deux semaines depuis Mai 2015 : pendant 1 an avant la coupe des arbres et pendant 2 ans en taillis après la coupe des arbres en Juin 2016. Les images ont été analysées en utilisant le logiciel WinRHIZO tron (Régent, Canada) pour tracer les racines en marquant leur longueur et leur diamètre afin d'estimer la croissance au cours du temps. Les racines fines, d'un diamètre inférieur à 2 mm, ont été échantillonnées jusqu'à 17m de profondeur afin d'estimer la biomasse (racines vivantes) et la nécromasse sur l'ensemble du profil de sol à 1.5 an après coupe dans les traitements +W, -W et 7.5 ans après la plantation dans le traitement NH.

  la coupe des arbres sur la dynamique racinaire dans une plantation d'Eucalyptus menée en taillis. Nos résultats ont montré que le taux journalier d'élongation racinaire était fortement dépendant de la couche de sol et de la saison dans les traitements +W et -W. En effet après la coupe des arbres, la croissance des racines fines a débuté dans les couches superficielles du sol et s'est propagé de plus en plus en profondeur au fil du temps dans les deux traitements +W et -W. Ainsi, après la coupe des arbres le démarrage des cohortes racinaires s'est d'abord observé 6 mois après la coupe en superficie, 12 mois après la coupe dans la couche 3.5-4.8 m de sol et 16 mois après la coupe dans la couche 13.5-14.8 m de sol dans les deux traitements +W et -W quand la plantation est menée en taillis. Les valeurs du taux d'élongation racinaire journalier ont culminées à la fin de la saison sèche dans toutes les couches de sol à des profondeurs supérieures à 6 m, lorsque le contenu en eau du sol était à son minimum dans les couches superficielles. Ainsi, les valeurs d'élongation racinaire journalières n'étaient pas nécessairement corrélées avec les teneurs en eau du sol pour une couche de sol donnée. Nous avons observé une synchronisation entre la diminution de la quantité d'eau extractible dans la couche superficielle et les pics d'élongations racinaires après la coupe dans le traitement -W. De plus nous avons observés que la densité des racines fines chute en dessous de 20 cm de profondeur, puis diminue progressivement jusqu'à la nappe phréatique dans les trois traitements NH, +W et -W. La biomasse totale des racines fines jusqu'à 17 m de profondeur était de 1078 g m -2 dans NH, 1017 ± 301 g m -² dans +W et 1266 ± 363 g m -² dans -W. La densité des racines fines était environ 25% plus élevée dans -W que dans +W et NH dans la plupart des couches de sol. À des profondeurs supérieures à 7 m, les densités de racines fines étaient au moins deux fois plus élevées dans -W que dans + W et NH. De plus, nous nous sommes intéressés à l'effet de la réduction de pluie sur l'adaptation morphologique des racines fines sur tout le profil de sol. Dans les traitements NH, +W et -W, nous avons montrés que la profondeur avait peu d'effet sur la longueur spécifique racinaire (SRL), la surface spécifique racinaire (SRA) et le diamètre des racines fines. SRL et SRA étaient significativement plus élevés dans -W que dans + W, et des valeurs similaires ont été observées dans + W et NH. Sur tout le profil de sol jusqu'à 17 m de profondeur, les valeurs moyennes de SRL étaient de 28.8, 30.6 et 34.4 m g -1 , les valeurs moyennes de SRA de 258.8, 267.5 et 305.3 cm 2 g -1 et les diamètres moyens des racines fines de 0.31, 0.32 et 0.36 mm dans les traitements NH, +W et -W respectivement. Sur toute la période d'étude (3 ans), la longueur cumulée de racines mortes ne représentait que 6-7% de la longueur cumulée de racines produite sur tout le profil de sol jusqu'à 17 m de profondeur dans les deux traitements +W et -W. Etonnamment, la longueur des racines fines mortes n'a pas augmenté après la coupe de la plantation et n'était pas différentes entre les profondeurs de sol et entre les traitements +W et -W. Ensuite, nous nous sommes intéressés à l'impact de la coupe des arbres et d'une réduction de précipitation sur les émissions de gaz à effet de serre ainsi que sur leur production/consommation sur tout le profil de sol. Les efflux cumulés de CO2 mesurés dans les traitements +W et -W étaient respectivement de 136. 5 ± 21.8 mol m -2 et de 130.3 ± 24.8 mol m -2 an -1 la dernière année avant la coupe des arbres et de 108.0 ± 15.8 et de 119.3 ± 22.5 mol m -2 an -1 la première année après la coupe quand la plantation est menée en taillis. Nous avons observé aucunes différences significatives entre les cumuls d'émissions de CO2, CH4 et N2O entre les deux traitements +W et -W. Les efflux de CH4 ont été négatifs pendant toute la période d'étude de mars 2016 à décembre 2017, indiquant une consommation nette de CH4 atmosphérique par le sol. Aucunes différences significatives ont également été observés entre les traitements NH et +W sur les émissions de CO2, CH4 et N2O, signifiant que la coupe des arbres n'a eu aucun effet. Les efflux de CO2, de CH4 et de N2O ne différaient pas significativement entre -W et +W et ne changeaient pas après la coupe des arbres dans les peuplements menés en taillis par rapport aux peuplements non exploités. Les concentrations de CO2 et de CH4 augmentaient fortement avec la profondeur et les concentrations de N2O restaient à peu près constantes de la surface du sol jusqu'à une profondeur de 15.5 m. Les concentrations moyennes de CO2 et de N2O dans -W étaient respectivement inférieures de 20.7% et 7.6% à celles de +W et celles de CH4 dans -W de 44.4% supérieures à celles de +W sur tout le profil de sol. Un modèle de diffusivité a montré que la production et la consommation de CO2, de N2O et de CH4 se produisaient à de grandes profondeurs et étaient similaires dans les traitements +W, -W et NH. La coupe des arbres n'a pas augmenté les efflux et les productions de CO2, de CH4 et de N2O, quel que soit le régime hydrique. Les productions de CO2, CH4 et N2O entre 0.1 et 15.5 m de profondeur n'étaient pas significativement différentes entre +W et -W. Les estimations de production dans le premier mètre de sol ont montré les valeurs les plus élevées de CO2 et de N2O et les plus faibles de CH4 en raison d'un fort gradient de concentration et d'une diffusivité effective calculée particulièrement élevée pour la couche de sol superficielle. La production de CO2 et de N2O et la consommation de CH4 se sont produites principalement dans le premier mètre, mais au moins une partie de la production de CO2 et de CH4 a atteint une profondeur allant jusqu'à 15.5 m.

Figure I. 1 :

 1 Figure I. 1: Eucalyptus plantation located in the southeastern region of Brazil, in São Paulo state. .......................................................................................................................................... 56 Figure I. 2: Average forecasts of changes in global rainfall distribution. Rainfall variations are expressed as a percentage change in precipitation per degree of warming. Predictions are made for decadal precipitation variations from 1900-1950 as the reference period (Solomon et al., 2009). ........................................................................................................................................ 57 Figure I. 3: Schematic representation of belowground production, consumption and transport processes for Eucalyptus plantations. ....................................................................................... 63

  Figure V. 4: Cumulated root length production (CLP) on minirhizotron tubes (m m -2 of minirhizotron area) measured every 14 days from May 2015 to July 2018 in soil layers 0-1.3 m, 1-2.3 m, 3.5-4.8 m, 5.5-6.8 m, 11.5-12.8 m, 13.5-14.8 m and 15.5-16.8 m in the undisturbed rainfall plot (+W, A), in the plot with 37% of throughfall excluded by plastic sheets (-W, B) and in the non-harvested plot (NH, C). Standard errors are shown (shaded area). The clear-cut

  Figure V. 5: Daily living root elongation rate (DRER) on minirhizotron tubes (cm m-2 of minirhizotron area day-1) estimated every 14 days from May 2015 to July 2018 in soil layers 0-1.3 m, 1-2.3 m, 3.5-4.8 m, 5.5-6.8 m, 11.5-12.8 m, 13.5-14.8 m and 15.5-16.8 m in the undisturbed rainfall plot (+W, A), in the plot with 37% of throughfall excluded by plastic sheets (-W, B) and in the non-harvested plot (NH, C). Standard errors are shown (shaded area). The clear-cut date is indicated by a vertical line. The stands were coppice-managed after clearcutting in +W and -W. The monitoring of DRER started in May 2015 in the +W and -W plots, and in March 2016 in the NH stand, where only the first three layers (0-1.3 m, 1-2.3 m and 3.5-4.5 m) were sampled. ............................................................................................................. 125 Figure V. 6: A) Time course of soil extractable water (mm) in soil layers 0-1 m and 1-2 m, in the -W (37% of throughfall excluded by plastic sheets) coppice of block 1, from March 2017 (10 months after the clear-cut) to December 2017.The mean daily values of soil extractable water were estimated from semi-hourly SWC measurements. B) Daily living root length production on the surface of minirhizotron tubes (cm m -2 of minirhizotron area day -1 ) estimated over the same period and same plot as a), at two-week intervals, in soil layers 0-1.3 m, 1-2.3 m,3.5-4.8 m, 5.5-6.8 m, 11.5-12.8 m, 13.5-14.8 m and 15.5-16.8 m. Standard errors are shown (shaded area). ......................................................................................................................... 127

  Figure V. 6: A) Time course of soil extractable water (mm) in soil layers 0-1 m and 1-2 m, in the -W (37% of throughfall excluded by plastic sheets) coppice of block 1, from March 2017 (10 months after the clear-cut) to December 2017. The mean daily values of soil extractable water were estimated from semi-hourly SWC measurements. B) Daily living root length production on the surface of minirhizotron tubes (cm m -2 of minirhizotron area day -1 ) estimated over the same period and same plot as a), at two-week intervals, in soil layers 0-1.3 m, 1-2.3 m,3.5-4.8 m, 5.5-6.8 m, 11.5-12.8 m, 13.5-14.8 m and 15.5-16.8 m. Standard errors are shown (shaded area). ......................................................................................................................... 127 Figure V. 7: Mean fine root densities down to the root front in the undisturbed rainfall plots (+W, blue), in the plots with 37% of throughfall excluded by plastic sheets (-W, orange) and in the non-harvested plot (NH, gray). Standard deviations between blocks (n = 3) for -W and +W and between pseudo replicates in a single block for NH are shown. ..................................... 128 Figure V. 8: Root area index (m 2 m -2 ) in the 0-1 m, 1-2 m, 2-5 m, 5-10 m and 10-17 m deep soil layers in the undisturbed rainfall plots (+W), in the plots with 37% of throughfall excluded by plastic sheets (-W) and in the non-harvested plot (NH). Different upper-case letters indicate significant differences between treatments for the cumulative indices and different lower-case letters indicate significant differences between treatments within each individual soil layer (p < 0.05). NH was not included in the ANOVA because the three soil coring replicates were located in the same plot. ..................................................................................................................... 130

  Figure VII. 1: Conceptual representation of the influence of A) throughfall exclusion and B) clear-cutting on mean specific root area (yellow), total root biomass (orange), mean diameter (green), mean root area index (purple), total root necromass (black) and mean specific root length (blue) across deep soil profiles. The size of the circles is not at scale, the idea is only to visualize trends between soil layers 0-1 m, 2-6 m and 10-16 m, and between treatments +W, -W and NH. Ref in A) and B) are the reference values. .......................................................... 200 Figure VII. 2: Conceptual representation of the influence of A) throughfall exclusion and B) clear-cutting on mean CO2 (blue), N2O (green) and CH4 (red) concentrations across deep soil profiles. The size of the circles is not at scale, the idea is only to visualize trends between soil layers 0-1 m, 2-6 m and 10-16 m, and between treatments +W, -W and NH. Ref in A) and B) are the reference values. The arrows at soil surface indicate whether the net gas efflux from soil to atmosphere is positive or negative. .................................................................................... 201

  (2008) (mean value of nine trenches). ............................................... 70 Table III. 2: Main results obtained in the experimental set up on the effects of drought, Na deficit and K deficit on soil parameters, tree biomass and anatomy, on the traits involved in the capture of light resources and/or controlling CO2 assimilation and traits controlling the transport of water into the plant and transpiration. indicates a positive effect, indicates a negative trend and indicates predominantly no effect. ...................................................................... 77 Table IV. 1: Root traits at depth compared to the top soil. indicates a predominantly positive trend, indicates a predominantly negative trend and indicates predominantly no effect. Categories of root traits and individual root traits are adapted from Brunner et al. 2015, Brunner et al. 2009, McCormack et al. 2012, Prieto et al. 2015. ........................................................... 93

  ......................................................................................................... 129 Table V. 3: Main results obtained in the experimental set up on root traits categories in deep soil layers, subjected to drought and in response of clear-cutting and coppice management. indicates a positive effect, indicates a negative trend and indicates predominantly no effect. ...................................................................................................................................... 147 Table VI. 1: Main results obtained in the experimental set up on water filled pore space, CO2, CH4 and N2O in deep soil layers, subjected to drought and in response of clear-cutting and coppice management. indicates a positive effect, indicates a negative trend and indicates predominantly no effect. ......................................................................................... 191 Table VIII. 1: Comparison of the key flow and transport features of reactive transport models (adapted from Steefel et al. (2015)). ...................................................................................... 218

Figure I. 1 :

 1 Figure I. 1: Eucalyptus plantation located in the southeastern region of Brazil, in São Paulo state.

Figure I. 2 :

 2 Figure I. 2: Average forecasts of changes in global rainfall distribution. Rainfall variations are expressed as a percentage change in precipitation per degree of warming. Predictions are made for decadal precipitation variations from 1900-1950 as the reference period(Solomon et al., 2009).

Figure I. 3 :

 3 Figure I. 3: Schematic representation of belowground production, consumption and transport processes for Eucalyptus plantations.

  The results obtained in this thesis are presented as three scientific articles and the organization of the different parts are summarized in Figure II. 1: ➢ Chapter 4: « Deep fine root dynamics in forest ecosystems ». This review will be submitted to the Journal Forest Ecology and Management, after co-authors revision. ➢ Chapter 5: « Consequences of clear-cutting and drought on fine root dynamics down to 17 m in coppice-managed eucalypt plantations ». This article has been published in the journal Forest Ecology and Management. ➢ Chapter 6: « Consequences of clear-cutting and drought on CO2, CH4 and N2O productions throughout deep soil profiles in coppice-managed eucalypt plantations ».This article will be submitted to the journal Global Biochemical Cycles.

Figure

  Figure II. 1: Conceptual diagram of the organization of the different parts of the thesis.

Forest

  Science Experimental Station owned by the Agricultural Superior School of Luiz de Quieroz (ESALQ) of São Paulo State University (USP). This experimental station, of an area of 2120 hectares, is located on the western plateau of São Paulo (23°02'S 48°38'W) at 300 km from the sea. This experimental site was heavily instrumented to quantify the dynamics of C, water and nutrient fluxes and to model the functioning of highly productive eucalypt plantations.

III. 2

 2 Experimental LayoutChanging water availabilities is an important issue in a context of global change as the continuing rise in atmospheric CO2 levels may come along increased variability in rainfall distribution in many regions. A split-plot experimental design was set up in June 2010 with a Eucalyptus grandis clone used in commercial plantation by the Suzano Company (São Paulo, Brazil), to evaluate the impact of rainfall reduction and contrasting fertilizations on the productivity and adaptability of Eucalyptus plantations. The experimental layout contained six treatments (three types of nutrient supply x two water regimes) replicated in three blocks. The whole-plot factor was the water supply regime (''exclusion" plots, -W, vs ''non-exclusion" plots, +W) and the split-plot factor was the fertilization regime(Figure III. 1). In this thesis, we studied two treatments out of all those available in the experimental design: one treatment with undisturbed rainfall (+W) and one treatment with throughfall exclusion (-W). Treatments -W and +W were used to determine the water deficit effect (Figure III. 1).The individual plots area was about 864 m 2 . Trees were planted in June 2010 at a spacing of 3 m x 2 m with a stocking density of 1666 trees per hectare, e.g. 144 trees per plot totalizing 432 trees per treatment per 3 blocks. All the plots were fertilized at planting with 3.3 g P m -2 , 200 g m -2 of dolomitic lime and trace elements, and at 3 months of age 12 g N m -2 and 0.45 mol K m - 2 were applied as KCl. Field trials at the study site and in nearby areas on the same type of soil

Figure

  Figure III. 1: Throughfall exclusion experiment located in the southeastern region of Brazil, at the Itatinga Forest Science Experimental Station in São Paulo state.In +W and -W, the eucalypt stands were harvested six years after planting, in June 2016, and the plantation was coppice-managed thereafter. Several new shoots were regenerated from the stumps after the clear-cut and 1 or 2 shoots per stump were selected to maintain the same

Figure III. 2 :

 2 Figure III. 2: Deep permanent pit down to a depth of 17 m in throughfall exclusion experiment at the Itatinga Forest Science Experimental Station in São Paulo state. Root dynamics were studied using minirhizotron over 1 year before clear-cutting, then over 2 years in coppice, as well as in the non-harvested plot (NH) serving as a control, and fine roots (i.e. diameter < 2 mm) were sampled down to 17 m in +W, -W and NH. More complete descriptions of the methods used as well as the results obtained are presented in Chapter 5 « Consequences of clear-cutting and drought on fine root dynamics down to 17 m in coppicemanaged eucalypt plantations »

Figure III. 3 :

 3 Figure III. 3: Chronology of the experiment

  photosynthate and nutrient availability[START_REF] Tierney | Fine root turnover in a northern hardwood forest: a direct comparison of the radiocarbon and minirhizotron methods[END_REF][START_REF] Sloan | Contrasting synchrony in root and leaf phenology across multiple sub-Arctic plant communities[END_REF], which may be considerably heterogeneous along the soil profile (Figure IV. 1). However, deep fine root dynamics, functional significance and contribution to the water cycles and biogeochemistry processes at plant and ecosystem scale, are still poorly known. The objective of this study is to provide an up-to-date literature review on deep fine roots through their root traits, morphology and phenology, and through the biotic and abiotic interactions with the soil environment. Previous studies on deep fine root production, mortality and longevity, belowground C sequestration, symbiosis with mycorrhizae, and nutrient uptake will be reviewed more specifically.

Figure

  Figure IV. 1: Conceptual model illustrating the relative magnitude of different controls on fineroot dynamics (according to Coleman et al. 2018). The width of the pyramid and shading reflects the relative magnitude of each factor. As the width narrows and shading decreases, the magnitude of the response decreases.

  , but the trends are still not clear. Indeed,Pinheiro et al. (2016) found a slight increase in SRL and SRA with soil depth down to 13.5 m for 4 different genotypes of Eucalyptus in Brazil.Maurice et al. (2010) also found that SRL increased down to a depth of 3 m in Eucalyptus plantations of different ages.Adriano et al. (2017) found no significant changes in SRL with soil depth down to 8 m in Citrus sinensis plantations, but they observed a tendency toward an increase in mean fine root diameters.[START_REF] Gwenzi | Spatial analysis of fine root distribution on a recently constructed ecosystem in a water-limited environment[END_REF] found that roots tended to be thicker down to a depth of 1.4 m in Acacia rostellifera and Melaleuca nesophila plantations in Western Australia.Prieto et al. (2015) measured root functional traits in 20 plant communities in 3 climatic zones: tropical climate, montane climate, and sub-humid Mediterranean climate. They found that fine roots were thicker in deep soil layer down to a depth of 1.6 m compared to the shallow layers. On the contrary,[START_REF] Sochacki | Accuracy of tree root biomass sampling methodologies for carbon mitigation projects[END_REF] observed that root diameter decreased systematically with depth down to 6 m in Eucalyptus globulus plantations in southwest Australia, andBakker et al. (2009) found that SRL decreased with depth down to 1.2 m in Pinus pinaster plantations in the southwest of France. Fast-growing

  acquisition and transport. Indeed,[START_REF] Mcelrone | Variation in xylem structure and function in stems and roots of trees to 20 m depth[END_REF] found that deep roots of Juniperus ashei, Bumelia lanuginosa, Quercus fusiformis and Quercus sinuate had higher vessel diameter and larger tracheid than shallow roots in deep soil layers down to 18-20 m (Figure IV. 2). They also found that deep roots had a greater hydraulic conductivity. In line with those results,[START_REF] Pate | Hydraulic architecture and xylem structure of the dimorphic root systems of South-West Australian species of Proteaceae[END_REF] reported that roots at a depth of 2 m had larger xylem conduits, higher length, specific area, and hydraulic conductivities, up to 15 times higher than roots in shallow layers for Australian species. Physiological and anatomical adjustment of fine roots in deep soil seems to be developed by plants to maximize hydraulic efficiency. Despite those results, studies on fine root morphology and anatomy at great depth are still scarce.

Figure IV. 2 :

 2 Figure IV. 2: Scanning electron micrographs of stems (top row), shallow roots (middle row) and deep roots (bottom row, 18-20 m) for Quercus fusiformis, Juniperus ashei Buchh., Quercus sinuata (Torr.) C.H. Mull and Bumelia lanuginosa tree species from the Edward's Plateau region of central Texas (According to McElrone et al. 2004).

  [START_REF] Stone | Changes in extracellular enzyme activity and microbial community structure with soil depth at the Luquillo Critical Zone Observatory[END_REF] studied microbial community characteristics down to a depth of 1.4 m in a tropical soil of northeastern Puerto Rico. They unexpectedly found that extracellular microbial activity decreased in deep soil layers but C acquiring enzymes activities increased with depth. Recently,Robin et al. (2019) observed ectomycorrhizal roots down to a depth of 4 meters in a deeply weathered soil under Eucalyptus trees in Brazil. Deep root symbiosis with microorganism could potentially impact nutrient acquisition in deep soil layers and may enhance the exploitation of nutrient stock throughout the entire soil profile. Indeed, some studies highlighted that deep root

  observed that root of Haloxyolon ammodendron C.A. Mey penetrated down to a depth of 10 m in a sandy soil, while it only reached 3 m in a heavy soil. Roots had a higher root surface area in the sandy soil compared to roots growing in the heavy soil. Freycon et al. (2015) also compared root distribution down to 6 m for Entandrophragma cylindricum Sprague (Meliaceae) grown in two different soil types: Arenosols and Ferralsols in an African semi-deciduous rainforest. They

  , varying considerably with soil layers. Soil depth strongly influences the root system architecture due to the heterogeneity of its environment. Root architectural models could simulate accurately spatial and temporal dynamics through a simulation of the root system in 3D. Integrating a vertically discretized soil into a model is particularly important as shallow and deep roots present different spatial and temporal dynamics. Model parametrization needs to consider shallow and deeper-rooted systems behaving differently according to the environmental factors and soil conditions. Indeed, these models are parametrized according to the definition of root types (e.g. RootTyp fromPagès et al. (2004) or DigR from[START_REF] Barczi | DigR: a generic model and its open source simulation software to mimic three-dimensional root-system architecture diversity[END_REF]) or by branching order (e.g. OpenSimRoot fromPostma et al. (2017)) or through parametric L-system modeling(Leitner et al., 2010) which also might vary with soil layer. Such a model without discretized processes by soil layers is not capable to simulate accurately the impact of environmental conditions and soil resources on root development. Models devoted to simulating water and nutrient uptake dynamics need to integrate the functional specialization of deep roots and root growth plasticity in response to environmental conditions, in particular in deep soil layers.

  Deep root systems are complex components of ecosystems. Deep roots display different functional specialization, anatomy and morphology and are mainly oriented toward water acquisition and transport (TableIV. 1). Climatic factors affect differently root phenology along with the soil profile as there are more buffered in deep soil layers. Research devoted to deep fine root dynamics linking anatomical, architectural and functional characteristics along very deep soil profiles to site characteristics, species and soil conditions should be carried out to gain insight into their impact on C, water and nutrient cycles. Deep fine root display plasticity by responding to changing soil conditions and have an important role for ecosystem functioning.It is then crucial to focus the research efforts on the understanding of deep root dynamics and associated functions which could have a significant influence on climate change mitigation.

  supply regimes. This chapter presents the results of 3 years of root dynamics monitoring and was published in the journal Forest Ecology and Management as scientific article with the title: "Consequences of clear-cutting and drought on fine root dynamics down to 17 m in coppice-managed eucalypt plantations". Co-authors associated with this project are Christophe Jourdan, Bruno Bordron, Agnès Robin, Yann Nouvellon, Lydie Chapuis-Lardy, José Leonardo de Moraes Gonçalves, Céline Pradier, Iraê Amaral Guerrini and Jean-Paul Laclau. Germon, A., Jourdan, C., Bordron, B., Robin, A., Nouvellon, Y., Chapuis-Lardy, L., Gonçalves, JLM., Pradier, C., Guerrini, IA., Laclau, JP. Consequences of clear-cutting and drought on fine root dynamics down to 17 m in coppice-managed eucalypt plantations. Forest Ecology andManagement, v. 445, p. 48-59, 2019.

A

  Figure V. 1: Layout of the position of the pit in the +W treatment of block 1 and distribution of minirhizotron tubes at the soil surface (n=3) and in the permanent pit from 1 m (n=2) down 17 m (n=1 per m in depth). The same set-up was used for the -W treatment.

Figure V. 2 :

 2 Figure V. 2: Vertical growth (m) over the first 2.5 years after harvesting of the previous stands for the replanting (June 2010-June 2016) and the coppice (from June 2016) in the undisturbed rainfall plots (+W, blue) and in the plots with 37% of throughfall excluded by plastic sheets (-W, orange). Standard errors are shown (shaded area).

Figure V. 3 :

 3 Figure V. 3: Daily rainfall (A) and soil water content (SWC, %) within the soil profiles down to a depth of 16 m in the undisturbed rainfall plots (+W, B) and in the plots with 37% of throughfall excluded by plastic sheets (-W, C) from May 2015 to January 2018. SWC graphical representation is a contour line interpolation obtained with a marching square algorithm. R software version 3.4.4 and the "plotly" package version 4.8.0 were used. The clear-cut date is indicated by a vertical line. The stand was coppice-managed after the clear-cut.

Figure V. 4 :

 4 Figure V. 4: Cumulated root length production (CLP) on minirhizotron tubes (m m -2 of minirhizotron area) measured every 14 days from May 2015 to July 2018 in soil layers 0-1.3 m, 1-2.3 m, 3.5-4.8 m, 5.5-6.8 m, 11.5-12.8 m, 13.5-14.8 m and 15.5-16.8 m in the undisturbed rainfall plot (+W, A), in the plot with 37% of throughfall excluded by plastic sheets (-W, B) and in the non-harvested plot (NH, C). Standard errors are shown (shaded area). The clear-cut date is indicated by a vertical line. The stands were coppice-managed after clear-cutting in +W and -W. The monitoring of CLP started in May 2015 in the +W and -W plots, and in March 2016 in the NH stand, where only the first three layers (0-1.3 m, 1-2.3 m and 3.5-4.5 m) were sampled.

  Figure V. 3, Figure V. 5).

  Figure V. 6: A) Time course of soil extractable water (mm) in soil layers 0-1 m and 1-2 m, in the -W (37% of throughfall excluded by plastic sheets) coppice of block 1, from March 2017 (10 months after the clear-cut) to December 2017. The mean daily values of soil extractable water were estimated from semi-hourly SWC measurements. B) Daily living root length production on the surface of minirhizotron tubes (cm m -2 of minirhizotron area day -1 ) estimated over the same period and same plot as a), at two-week intervals, in soil layers 0-1.3 m, 1-2.3 m, 3.5-4.8 m, 5.5-6.8 m, 11.5-12.8 m, 13.5-14.8 m and 15.5-16.8 m. Standard errors are shown (shaded area). V.3.5 Fine root distributions

Figure V. 7 :

 7 Figure V. 7: Mean fine root densities down to the root front in the undisturbed rainfall plots (+W, blue), in the plots with 37% of throughfall excluded by plastic sheets (-W, orange) and in the non-harvested plot (NH, gray). Standard deviations between blocks (n = 3) for -W and +W and between pseudo replicates in a single block for NH are shown.

  Figure V. 8). Similar RAI values in the NH stand (26.8 m 2 m -2 ) and in the +W coppice suggested that the effect of clear-cutting on fine root dynamics was low, in agreement with elongation and mortality rates observed in the upper 4 m on minirhizotron tubes. RAI in the 0-1 m surface soil layer accounted for only one third of the total RAI down to the water table in NH, +W and -W (about 11 m 2 m -2 on average). Significant differences between +W and -W were found at depths > 5 m (Figure V. 8). In the 5-10 m soil layers, RAI was 5.0 m 2 m -2 in -W and 2.8 m 2 m -2 in +W. At depths > 10 m, RAI was 3.2 m 2 m -2 in -W and only 0.4 m 2 m -2 in +W.

Figure V. 8 :

 8 Figure V. 8: Root area index (m 2 m -2 ) in the 0-1 m, 1-2 m, 2-5 m, 5-10 m and 10-17 m deep soil layers in the undisturbed rainfall plots (+W), in the plots with 37% of throughfall excluded by plastic sheets (-W) and in the non-harvested plot (NH). Different upper-case letters indicate significant differences between treatments for the cumulative indices and different lower-case letters indicate significant differences between treatments within each individual soil layer (p < 0.05). NH was not included in the ANOVA because the three soil coring replicates were located in the same plot.

3 .Table V. 3 :

 33 Main results obtained in the experimental set up on root traits categories in deep soil layers, subjected to drought and in response of clear-cutting and coppice management. indicates a positive effect, indicates a negative trend and indicates predominantly no effect.

  N2O fluxes throughout very deep tropical soils in coppice-managed Eucalyptus grandis (Hill ex. Maid) stands after clear-cutting. We put forward three hypotheses: (H1) throughfall exclusion lower soil water contents, which increases gas diffusivity and modify greenhouse gases production and consumption, (H2) throughfall exclusion increases the partition of C to deep roots, which increases the production of CO2 in deep soil layers, and (H3) fine root mortality and slash decomposition after harvesting Eucalyptus grandis trees managed in coppice increase substrate availability for microbes throughout the soil profile, which increases CO2, CH4 and N2O effluxes at soil surface. carried out at the research station owned by the Luiz de Quieroz College of Agriculture (ESALQ) near Itatinga (São Paulo state, Brazil, 23°02′S 48°38′W), at an altitude of 850 m. The relief is typical of the São Paulo Western Plateau, with a topography varying from flat to hilly (slopes < 3%). The soils are very deep Ferralsols according to the ISS Working Group WRB (2015) developed on Cretaceous sandstone. Clay contents range from 160 mg g -1

  surface from March 2016 to December 2017: over 3 months before clear-cutting and 19 months after the clear-cut in the coppice-managed +W and -W treatments and over 22 months in the NH treatment.

Figure

  Figure VI. 1: A) Layout of the position of the pit in the +W treatment of block 1 and distribution of the PVC collars for closed-path Li8100 Licor system (n=9) and anchors for closed-chamber method (n=4). B) Layout of the position of the syringes for soil-gas sampling from the soil surface at 0.1, 0.5 and 1 m (n=3 per depth) and in the permanent pit at the depths of3.5, 7.5, 11.5 and 15.5 m (n=3 per depth). The same set-up was used in the -W treatment. The photographs show a view from the bottom of each pit, the top of one pit and the tube used to sample soil gas.

  .3.1 Water filled pore space (WFPS) WFPS values throughout the soil profiles were strongly influenced by throughfall exclusion and reflected the distribution of rainfall events (Figure VI. 2). Mean WFPS from March 2016

Figure VI. 2 :

 2 Figure VI. 2: Daily rainfall (A) and water filled pore space (WFPS, %) within the soil profiles down to a depth of 16 m in the undisturbed rainfall plots (+W, B) and in the plots with 37% of throughfall excluded by plastic sheets (-W, C) from March 2016 to December 2017. Water filled pore space graphical representation is a contour line interpolation obtained with marching square algorithm. R software version 3.4.4 and the "plotly" package version 4.8.0 were used. The clear-cut is indicated by a vertical line and the stand was coppice-managed after the clear-cut.

Figure VI. 3 :

 3 Figure VI. 3:A) Time course of soil CO2 efflux (µmol m -2 s -1 ) measured using the Li-8100 device in the undisturbed rainfall treatment (+W, blue) and in the treatment with 37% of throughfall excluded by plastic sheets (-W, orange) measured every 14 days from December 2014 to December 2017. Standard errors are shown (shaded area). The vertical line indicates the date of the clear-cut. B) Boxplots of soil CO2 effluxes in treatments +W (blue) and -W (orange) from December 2014 to December 2017. Overlapping notches between boxplots suggest that the medians did not significantly differ. C) Cumulative soil CO2 effluxes (mol m -2 year -1 ) at yearly time scale in treatments +W (blue) and -W (orange), the last year before the clear-cut (between 5 and 6 years after planting) and the first year after the clear-cut in coppice-managed stands.

Figure VI. 4 :

 4 Figure VI. 4: Time course of soil CO2 (µmol m -2 s -1 , A), CH4 (nmol m -2 s -1 , C) and N2O (nmol m -2 s -1 , E) effluxes in the undisturbed rainfall treatment (+W, blue) and in the treatment with 37% of throughfall excluded by plastic sheets (-W, orange) measured every 14 days from March 2016 to October 2017. The vertical line indicates the date of the clear-cut. Standard errors are shown (shaded area). Boxplots of soil CO2 (B), CH4 (D) and N2O (F) effluxes from March 2016 to October 2017 in treatments +W and -W are shown. Overlapping notches between boxplots suggest that the medians did not significantly differ.

Figure VI. 5 :

 5 Figure VI. 5: Time course of CO2 concentrations (ppm) within the soil profile down to a depth of 16 m (A) in the undisturbed rainfall treatment (+W) and (B) in the treatment with 37% of throughfall excluded by plastic sheets (-W), from March 2016 to December 2017. Time course of N2O concentrations (ppb) within the soil profile down to a depth of 16 m in treatment +W (C) and in treatment -W (D). Time course of CH4 concentrations (ppm) within the soil profile down to a depth of 16 m in treatment +W (E) and in treatment -W (F). Graphical representations are contour line interpolations using a marching square algorithm (R software version 3.4.4 and the "plotly" package version 4.8.0). The clear-cut date is indicated by a vertical line and the stand was coppice-managed after the clear-cut.

(

  FigureVI. 6: Time course of CO2 production (µmol m -2 s -1 ) calculated with the diffusivity model within the soil profile down to a depth of 16 m (A) in the undisturbed rainfall treatment (+W) and (B) in the treatment with 37% of throughfall excluded by plastic sheets (-W), from March 2016 to December 2017. Time course of N2O production (nmol m -2 s -1 ) within the soil profile down to a depth of 16 m in treatment +W (C) and in treatment -W (D). Time course of CH4 production (nmol m -2 s -1 ) within the soil profile down to a depth of 16 m in treatment +W (E) and in treatment -W (F). Graphical representations are contour line interpolations using a marching square algorithm (R software version 3.4.4 and the "plotly" package version 4.8.0). The clear-cut date is indicated by a vertical line and the stand was coppice-managed after the clear-cut.

Figure

  Figure VI. 7: A) Cumulative CO2 fluxes (mol m -2 year -1 ), B) cumulative CH4 fluxes (mol m -2 year -1 ), and C) cumulative N2O fluxes (mmol m -2year -1 ) the first year after the clear-cut in coppice-managed stands in the undisturbed rainfall treatment (+W, blue) and in the treatment with 37% of throughfall excluded by plastic sheets (-W, orange). Cumulative fluxes of CO2, CH4 and N2O were not significantly different (P < 0.05) between treatments +W and -W, whatever the soil layer.

Figure VI. 8 :

 8 Figure VI. 8: Relationship between water filled pore space (WFPS) and CO2 (A), CH4 (B) and N2O (C) production obtained using the diffusivity model for each soil layer 0.1-0.5 m, 0.5-1 m, 1-3.5 m, 3.5-7.5 m and 7.5-11.5 m in the undisturbed rainfall treatment +W.

  of climate change on forest plantations: Let's look deeper! Understanding the effects of climate changes, predicting its potential impacts and anticipating adaptation is mandatory for the sustainability of fiber and food production in a context of increasing human population. If greenhouse gas emissions maintain their current increase, climate change may increase the vulnerability of agricultural and forestry systems and reduce

Figure VII. 1 :

 1 Figure VII. 1: Conceptual representation of the influence of A) throughfall exclusion and B) clear-cutting on mean specific root area (yellow), total root biomass (orange), mean diameter (green), mean root area index (purple), total root necromass (black) and mean specific root length (blue) across deep soil profiles. The size of the circles is not at scale, the idea is only to visualize trends between soil layers 0-1 m, 2-6 m and 10-16 m, and between treatments +W, -W and NH. Ref in A) and B) are the reference values.

Figure VII. 2 :

 2 Figure VII. 2: Conceptual representation of the influence of A) throughfall exclusion and B) clear-cutting on mean CO2 (blue), N2O (green) and CH4 (red) concentrations across deep soil profiles. The size of the circles is not at scale, the idea is only to visualize trends between soil layers 0-1 m, 2-6 m and 10-16 m, and between treatments +W, -W and NH. Ref in A) and B) are the reference values. The arrows at soil surface indicate whether the net gas efflux from soil to atmosphere is positive or negative.

  concentrations in a deep tropical soil explored by roots in eucalypt plantations? -What is the contribution of fine roots in CO2 effluxes at the soil surface? -What are the consequences of drought periods on CO2 production and efflux in eucalypt plantations established in deep Ferralsols? -What are the consequences of future climatic scenarios on CO2 production in deep soil layers and the effluxes at the soil surface? Process-based models are needed to gain insight into the biogeochemical processes driving the concentrations of greenhouse gases measured at a few dates in soil profiles. Modeling root architecture development is important to simulate temporal and spatial dynamics of the root system architecture. Root architectural models are also useful to estimate global root variables like biomass or surface over depth and time. They are parameterized by root type (e.g. RootTyp, Pagès et al. (2004); ArchiSimple, Pagès et al. (2014); DigR, Barczi et al. (2018)) or by branching order (e.g. OpenSimRoot; Postma et al. (2017); parametric L-system modeling; Leitner et al. (2010)). The number of parameters needed to simulate root architecture vary

  below (Figure VIII. 1).

Figure

  Figure VIII. 1: Schematic representation of Eucalyptus root system in vertical view, with the different root types and their characteristics.

•

  Duration before emergence • Growth parameters: maximum, average and standard deviation of growth rate • Inter-branch distance along the root • Indicator of tropism type and tropism intensity • Sensibility to mechanical constraint • Apical diameter • Necrosis duration • Dates of reiterations and probability for reiteration at the reiteration dates • Minimal and maximal number of reiterated roots • Age from which transition may happen and daily probability of transition • Proportions of type among the branches A literature review made it possible to estimate all the parameters needed for the simulations.We mainly used data obtained in Eucalyptus plantations in Brazil and Congo. Most of the data dealing with root architecture came from the PhD thesis "Study of the root system of Eucalyptus in tropical plantation: architectural analysis, growth and respiration" of Armel Thongo M'Bou in Congo[START_REF] Thongo | Etude du système racinaire de l'Eucalyptus en plantation tropicale: analyse architecturale, croissance et respiration[END_REF]. The next step was to include for each root type a coefficient for diameter increases throughout tree growth. Then we included into the code the possibility of choosing the seed to start the simulation. Those changes were important to represent accurately Eucalyptus root systems and to validate the output simulations made.

  We succeeded in simulating realistic root systems throughout the development of Eucalyptus trees (Figure VIII. 2, Figure VIII. 3, Figure VIII. 5).

Figure VIII. 2 :

 2 Figure VIII. 2: Simulated Eucalyptus root system using the Root Typ model at age 6 months, in a XZ orientation and representation within the soil profile (left) and traced viewing from above the soil surface (XY) orientation (right).

Figure VIII. 3 :

 3 Figure VIII. 3: Simulated Eucalyptus root system using the Root Typ model at age 1 year (A), 2 years (B) and 3 years (C), in a XZ orientation representation within the soil profile (left) and traced viewing from above the soil surface (XY).

Figure VIII. 4 :

 4 Figure VIII. 4: Fine root length (m m -2 ) per soil layer simulated using the Root Typ model (blue) and measured (collected in the field) for Eucalyptus plantations of age 3 years Total root length obtained with the simulations using Root Typ Model were consistent with the measured data (observed in the field) for Eucalyptus plantations of 3 years of age, but the distribution throughout the different soil layers were not accurately simulated (Figure VIII. 4).

Figure

  Figure VIII. 5: Simulated Eucalyptus root system using the Root Typ model at age 6 years, in a XZ orientation and representation within the soil profile (left) and traced viewing from above the soil surface (XY) (right).

  The first key step was to calibrate and parameterize the water transport. The simulations of water dynamics were validated using measurements of: (i) actual transpiration fluxes and (ii) volumetric soil water content monitored over the whole study period. The climatic variables (potential and actual transpiration fluxes, precipitation) determined at the experimental site were used either to constrain the model or to validate it.

Figure

  Figure VIII. 6: Graphical representation of the close link between water transport and CO2 production, transport and effluxes.

  Figure VIII. 7: Soil water contents (Theta_a %) within the soil profile down to a depth of 18 m simulated with the Min3P model (Cmvs 2, top) and simulated with the MAESPA model (Maespa, bottom) every day from June 1st, 2010 to May 31, 2016, which was the entire rotation for this Eucalyptus grandis plantation in the undisturbed rainfall plot. Soil water content graphical representation is a contour line interpolation using marching square algorithm. R software version 3.4.4 and the package plotly version 4.8.0 were used.

  respiration and microbial decomposition over depths should provide more accurate estimations and could reduce uncertainty in model simulations.Prediction of CO2 production in deep soil profiles under climate changeSimulations to explore the effects of future climate scenarios on CO2 production and transfer in deep tropical soils could be performed including the current measurements as initial boundary conditions, and by comparing climatic series representing future climatic scenarios at the experimental field location. The predictions could be useful to assess qualitatively the consequences of climate change on CO2 production in tropical eucalypt plantations growing on deep Ferralsols.

Fine

  roots (diameter < 2 mm) were sampled down to a depth of 17 m in the three treatments (100A, 100E and 50A50E; Figure IX. 1) within the three blocks. Three replicates of soil samples were collected at mid distance between 4 adjacent trees (Figure IX. 1) in each plot down to a depth of 6 m and one replicate per plot between the depths of 6 m and 17 m (total of 9 samples per treatment in each soil layer down to 6 m depth and 3 samples between the depths of 6 m and 17 m). At each sampling position, soil layers 0were collected by digging a square hole of approximately 15 cm

Figure IX. 1 :

 1 Figure IX. 1: Layout of the three treatments studied: Acacia mangium and Eucalyptus grandis monospecific stands (100A and 100E, respectively) and a mixed stand with 50% of each species (50A50E). A. mangium trees are represented by grey circles and E. grandis trees by black triangles. Each inner plot (excluding two buffer rows) is delimited by a grey square. Three replicates samples (position indicated by a red cross) of soil cores were collected at mid distance between 4 adjacent trees in each plot down to a depth of 6 m and one sample per plot between the depths of 6 m and 17 m. Only one block is presented. A complete scheme of the trial is presented on Fig. 1 in Le Maire et al. (2013).

  in 100A in soil layers 1.5 -2 m, 2 -3 m, 3 -4 m, and at depths > 8 m. Low fine-root densities at depths > 8 m in 100A were consistent with higher soil water contents in 100A than in 100E and 50A50E (Figure IX. 2).

Figure IX. 2 :

 2 Figure IX. 2: Mean fine-root densities (a) and gravimetric water content (b) down to the root front in treatments 100E (filled black bars), 100A (open bars) and 50A50E (filled grey bars). Standard errors between blocks are given down to a depth of 6 m (n=3). Different letters indicate significant differences between treatments within each individual soil layer down to 6 m depth (p < 0.05, only significant in the upper soil layer).

Figure IX. 3 :

 3 Figure IX. 3: Percentages of fine-root biomass in each soil layer in 50A50E relative to the fineroot biomass in the single-species stands. The dotted line indicates the 50% reference for Acacia mangium roots (open bars with standard errors) and Eucalyptus grandis roots (solid bars with standard errors), if root development was similar to the monoculture, for a 50% tree stocking density for each species. Standard error bars are shown. Asterisks * denotes a significant difference (p<0.05) between the root biomass of a particular species in 50A50E and 50 % of the biomass in the monoculture of the same species.

Figure IX. 4 :

 4 Figure IX. 4:Specific root length (a), specific root area (b) and mean fine-root diameter (c) in each soil layer for Acacia mangium (left) and Eucalyptus grandis (right) in monospecific stands and in 50A50E. Standard errors between blocks are indicated (n=3). Asterisks * denotes a significant difference (p<0.05) between 50A:50E and the monoculture.

Figure IX. 5 :

 5 Figure IX. 5:Root length index (km m -2 ) a) and root area index (m 2 m -2 ) b) in the 0-1 m, 1-2 m, 2-4 m, 4-6 m, 6-9 m and 9-17 m soil layers for Acacia mangium monospecific stands (100A), Eucalyptus grandis monospecific stands (100E) and the mixed stands (50A50E). Different upper-case letters indicate significant differences between treatments for the cumulative indices and different lower-case letters indicate significant differences between treatments within each individual soil layer (p < 0.05).

Figure IX. 6 :

 6 Figure IX. 6: Fine root production (g dm -3 month -1 ) in ingrowth bags down to a depth of 6.35 m in 100E (filled black bars), 100A (open bars) and 50A50E (filled grey bars) (a) and percentages of fine-root production in 50A50E relative to the production in each soil layer for the single-species stands (b) in winter (dry season; Trimester 1, left) and in spring (Trimester 2, right). Significant differences between treatments in the same soil layer are indicated by different letters (p<0.05). The dotted lines indicate the 50% reference for Acacia mangium roots (open bars with standard errors) and Eucalyptus grandis roots (solid bars with standard errors) if root development was similar to the monoculture, for a 50% stocking density for each species. Standard error bars are shown (n=3). Asterisks * denotes a significant difference (P<0.05) between the root biomass of a particular species in 50A50E and 50 % of the biomass at the same positions in the pure stands of the same species. F and P values of linear mixed models for fine-root production (g dm -3 month -1 ) as a function of soil depth and treatment are shown.

Table 1 :

 1 Summary of the root parameters used in this study, how we obtained them and how we can interpret them. .............................................................................................................. 51 Table III. 1: Chemical attributes of the soil of the experimental area down to a depth of 6 meters determined by Maquere

257 LIST OF ABBREVIATIONS AND ACRONYMS

  . ..................... 248 Table IX. 2: Total fine-root biomass down to a depth of 17 m and mean specific root length (SRL), mean specific root area (SRA) and mean fine-root diameter down to a depth of 6 m in 100A, 100E and 50A50E at 4 years of age. Different uppercase letters indicate significant differences between treatments, and different lowercase letters indicate significant differences between the monospecific stands and the mixed stands for each species (p < 0.05). ............ 253 Table IX. 3: P values of linear mixed models for specific root length (SRL), specific root area (SRA) and root diameter applied to the whole soil profile between 100A and 50A50E for A. mangium roots and between 100E and 50A50E E. grandis roots as a function of treatment, soil depth and the interactions between factors. ........................................................................... 256 Table IX. 4: Fine-root biomass (g m -2 ) in 100A, 100E and 50A50E. The percentage of root mass in each soil layer relative to the total root mass is in parentheses. Different letters indicate significant differences between treatments in each soil layer (p < 0.05). ..............................

	UNESP	Universidade Estadual Paulista Júlio de Mesquita Filho
	FCA	Faculdade de Ciências Agronômicas
	ESALQ	Escola Superior de Agricultura Luiz de Quieroz
	USP	São Paulo State University
	CIRAD	Centre de coopération internationale en recherche agronomique pour le
		développement
	-W	Throughfall exclusion treatment
	+W	Treatment with undisturbed rainfall
	WFPS	Water filled pore space
	GDP	Gross domestic product
	GHG	Greenhouse gases
	SWC	Soil water content
	LP	Length production
	CLP	Cumulative length production
	RER	Root elongation rate
	Mean RER Mean of root elongation rate
	Max RER	Maximum root elongation rate
	DRER	Daily root elongation rate
	SRL A. Germon 2019 Specific root length	51
	SRA	Specific root area
	FRD	Fine root density
	FRB	Fine root biomass
	RAI	Root area index
	RLI	Root length index
	HSD	Tuckey's post-hoc Honest Significant Difference
	Min3P	The Reactive Transport Code MIN3P: Multicomponent reactive transport
		modeling in variably saturated porous media

Table 1 :

 1 Summary of the root parameters used in this study, how we obtained them and how we can interpret them.

	How to measure		Root parameter	Unit	All roots / Individual roots	Description	Interpretation
	Minirhizotron	LP	Length production	cm m -2	Individual root	Individual root length per observed soil area	Root length observed
		CLP	cumulative length production	cm m -2	Ʃ roots	Sum of LP	Total root length observed
						Root increment
		RER	root elongation rate	cm day -1	Individual root	between two sessions	Individual root growth
						over time
		Max RER	Maximum root elongation rate	cm day -1	Comparing all roots	Higher value	Maximum root growth observed
		Mean RER	Mean Root elongation rate	cm day -1	Taking into account all roots	Mean root elongation period rate over the study	Mean root growth
		DRER	Daily root elongation rate	cm m -2 day -1	Ʃ roots	Sum of root elongation rate per session	Total root increment per day => indicator of phenology
	Root sampling	FRB	Fine root biomass	g kg -1	All roots	g of roots per kg of soil	Indicator of root distribution in soil
		FRD	Fine root density	g dm -3	All roots	g of roots per dm -3 of soil sampled	Indicator of root distribution in soil
		SRL	Specific root length	m g -1	All roots	Length of roots per g of root	Indicator of root exploration and nutrient uptake
		SRA	Specific root area	m 2 g -1	All roots	Area of root per g of root	Indicator of root exploration and nutrient uptake
		RLI	Root length index	m m -2	All roots	Length of root per soil area	Indicator of root investment
		RAI	Root area index	m 2 m -2	All roots	Area of root per soil area	Indicator of root investment

CHAPTER 1: INTRODUCTION

Many studies have been carried out other the last decades to help facing future dramatic climatic and demographic changes

Table III .

 III 1: Chemical attributes of the soil of the experimental area down to a depth of 6 meters determined byMaquere (2008) (mean value of nine trenches).

	Depth	ph	K	Ca	Mg	Na	H+Al SB	CTC V
	m	water KCl			mmolc kg -1			%
	0-0.05	4.6	4.0 0.1246 0.2180 0.3115 0.0000 23.54 1.4 24.94 5
	0.05-0.15	5.3	4.4 0.0467 0.0081 0.1303 0.0000 11.66 0.30 11.95 2
	0.15-0.5	5.5	4.7 0.0286 0.0052 0.0316 0.0000 8.80 0.09 8.89	1
	0.5-1.0	5.5	4.6 0.0161 0.0000 0.0124 0.0000 6.49 0.04 6.53	1
	1.0-2.0	5.7	5.2 0.0305 0.0153 0.0153 0.0034 3.94 0.12 4.06	3
	2.0-3.0	6.0	5.3 0.0133 0.0007 0.0103 0.0159 0.80 0.08 0.87 18
	3.0-4.0	5.7	5.3 0.0393 0.0363 0.0375 0.0042 0.28 0.16 0.44 36
	4.0-5.0	5.9	5.5 0.0298 0.0261 0.0253 0.0000 0.04 0.16 0.20 79
	5.0-6.0	5.8	5.6 0.0287 0.0095 0.0164 0.0072 0.13 0.11 0.24 56

Table III . 2 :

 III2 Main results obtained in the experimental set up on the effects of drought, Na deficit and K deficit on soil parameters, tree biomass and anatomy, on the traits involved in the capture of light resources and/or controlling CO2 assimilation and traits controlling the transport of water into the plant and transpiration. indicates a positive effect, indicates a negative trend and indicates predominantly no effect.

	Na deficit	K deficit	Water deficit	References
	Soil parameters
	Soil water content			Battie-Laclau et al. 2014;
				Christina et al. 2015;
				Christina et al. 2018
	Amount of water stored in ground			Christina et al. 2018
	Deep seepage			Christina et al. 2018
	H3O + rhizo/ H3O + bulk			Pradier 2016
	Kech rhizo / Kech bulk			Pradier 2016
	C rhizo/ C bulk			Pradier 2016
	H + Al 3+ rhizo			Pradier 2016
	Biomass and Anatomy
	Tree height			Christina et al. 2015;
				Epron et al. 2015
	Trunk circumference at breast height			Christina et al. 2015
	Aboveground biomass			Battie-Laclau et al. 2016;
				Battie-Laclau et al. 2014
	Stem wood biomass			Battie-Laclau et al. 2016
	Wood production			Battie-Laclau et al. 2016
	Wood density			Poyet 2017
	Leaf area			Battie-Laclau et al. 2013;
				Battie-Laclau et al. 2014;
				Epron et al. 2015
	Leaf thickness			Battie-Laclau et al. 2014
	Leaf biomass			Epron et al. 2015
	Chlorophyll content			Battie-Laclau et al. 2014
	Leaves palisade			Battie-Laclau et al. 2014
	Leaves spongy			Battie-Laclau et al. 2014
	Leaves intercellular space			Battie-Laclau et al. 2014
	Leaves paracytic stomata			Battie-Laclau et al. 2014

Traits involved in the capture of light resources and/or controlling CO2 assimilation

	Na deficit	K deficit	Water deficit	References
	LAI: Leaf area index			Battie-Laclau et al. 2014
	Leaf water potential at predown			Battie-Laclau et al. 2014;
				Epron et al. 2015
	Leaf water potential at midday			Battie-Laclau et al. 2014;
				Epron et al. 2015
	Leaf gas exchange			Battie-Laclau et al. 2014
	Leaf net primary production			Battie-Laclau et al. 2016
	Aboveground net primary production			Battie-Laclau et al. 2016
	Stomatal conductance			Battie-Laclau et al. 2016
	Canopy conductance
	Crown CO2 uptake			Epron et al. 2015

Soil parameters Traits involved in the capture of light resources and/or controlling CO2 assimilation

	Maximum rate of photosynthetic electron	Christina et al. 2015
	transport at 25°C
	Maximum rate of rubisco carboxylase	Christina et al. 2015
	activity at 25°C
	GPP: Gross primary production	Christina et al. 2015
	LUE: Light use efficiency	Christina et al. 2015
	aPar: absorbed photosynthetically active	Christina et al. 2015
	radiation
	WUE: Water use efficiency	Battie-Laclau et al. 2016

Traits controlling the transport of water into the plant and transpiration

	CHAPTER 4:
	Sapwood cross section area		Epron et al. 2015
	Xylem sap flux		Epron et al. 2015
	Cambial activity		Poyet 2017
	Canopy transpiration		Christina et al. 2018
	Soil water stress index		Christina et al. 2018
	Vessel diameter		Poyet 2017
	Hydraulic conductivity		Poyet 2017
	Traits involved in the capture of water and nutrient resources
	SRL	?	This thesis
	SRA	?	This thesis
	Root diameter	?	This thesis
	Root biomass	?	This thesis
	Root necromass	?	This thesis
	Greenhouse gases (CO2, N2O and CH4)
	Effluxes at soil surface	?	This thesis
	Concentration in the soil	?	This thesis
	Production within the soil profile	?	This thesis

DEEP FINE ROOT DYNAMICS IN FOREST ECOSYSTEMS: WHY DIGGING DEEPER? Abstract Deep

  fine roots have been recently defined as fine roots encountered below a depth of 1 m and represent a large part of tree root system. While knowledge on deep root dynamics is constantly expending, our understanding of the phenology, morphology, anatomy and role of deep fine roots is still largely incomplete. In this review, the current knowledge about fine root production, mortality and longevity in deep soil layers, and the magnitude of the impacts and significance of deep fine root on carbon and nutrient cycling were discussed and highlighted.Roots are plant's underground organs responsible for anchorage in the soil and absorption of water and nutrients needed for plant development. The anchorage function is provided by the largest roots and mainly involves physical interactions between roots and the soil. The absorptive function is more complex as it involves biogeochemical, biochemical and biological interactions between fine roots, soil, but also soil microorganism. Roots develop often symbiosis with soil bacteria and fungi. Fine roots have the ability to adapt to different environments to facilitate the development of the plant. Fine roots link plant metabolism to soil nutrient cycles, they are ephemeral and frequently replaced. They can modify the physical,

Deep fine roots are highly plastic in response to environmental conditions and soil resources.

They present contrasting functional traits and functional specializations compared to shallow roots and are mainly oriented toward water acquisition and transport. Deep roots have a large impact on plant development and biogeochemical cycles through water and nutrient uptake, carbon allocation and sequestration in the soil. Therefore, modeling processes need to consider deep root functioning and dynamics accurately to better estimate net ecosystem productivity and nutrients, carbon and water cycles.

Key words: fine root growth, root traits, root longevity, root production, root mortality, carbon sequestration, tree plantations IV.1 Introduction chemical and biotic soil properties by their activities which can have repercussions not only at the plant scale but also at the ecosystem level

(McCormack et al., 2015)

. Indeed, fine roots play a major role in the global carbon (C) cycle, representing significant C input into the soil by the incorporation of exudates and root necromass, and generating a return of C to the atmosphere through respiration and decomposition processes

  reviewed that roots under different vegetation systems extend in deep horizons down to 9.5±2.4 m in deserts, 7.3±2.8 m in tropical evergreen forest and 15.0±5.4 m in tropical grassland and savannah, with maximum rooting depths of 68 m for Eucalyptus trees.

  table.[START_REF] Li | Optimal root system strategies for desert phreatophytic seedlings in the search for groundwater[END_REF] found a higher root growth rate when the water table was artificially deeper for Alhagi sparsifolia Shap. (Leguminosae). They found a root front growth of 0.66 cm d -1 when the water table was at a depth of 0.8 m and 1.5 cm d -1 when the water table was at a depth of 2.2 m.Canham et al.

	(2012) found a seasonal distribution of fine root biomass in deep soil layers following the
	fluctuations of the depth of the water table. A deeper water table level might induce a higher
	root elongation downwards

  Eucalyptus grandis monospecific stands, 52% in Acacia mangium monospecific stands and 37% in a mixture stands with 50% of both species in the 0-1 m soil layers.Furthermore, the proportion of roots at great depth increase with stand age:[START_REF] Ma | Effects of drip irrigation on deep root distribution, rooting depth, and soil water profile of jujube in a semiarid region[END_REF] found that fine roots below 1 m represented 10.54 %, 29.62% and 42.42% of the total roots in 2 years, 4 years and 12 years of Ziziphus jujube Mill. CV. Lizao plantation in China, and Laclau

[START_REF] Falkiner | Root distribution of Eucalyptus grandis and Corymbia maculata in degraded saline soils of south-eastern Australia[END_REF]

observed that Eucalyptus grandis root proliferation resulted in equal root length densities between 0-0.5 m and 2.4-2.8 m soil layers in another agroforestry system in southeastern Australia.

Germon et al. (2018)

observed fine root biomass represented 31% of total biomass in

Table V .

 V 2: Total living fine root biomass (g m-2

  , to gain insight into the processes governing CO2 transfer at a local scale. To consider the distribution of eucalypt fine roots within the entire root profile, including the deep soil horizons, we first tried to calibrate the Root-Typ model (Part 1) with eucalypt root data measured at Itatinga, then we tried to include fine root dynamics in Min3P (Part 2). To simulate tree root systems, additional parameters are needed to simulate reiteration, senescence and late emission processes. All the parameters of Root Typ model are indexed to the apical diameter of all roots without distinction of root typology, which is impossible to assume in order to simulate growth and distribution of all types of roots of Eucalyptus trees within the soil profile. The issue was thus to adapt the Root Typ model to

	VIII.2	Part 1: The Root Typ model
	VIII.2.1	Calibration and parameterization of the Root Typ model
	Description and parameterization of the Root Typ model
	The Root Typ model (Pagès et al., 2004) simulates root growth processes at a daily time step:
	emission of new roots, elongation, branching and radial growth of various plant species by
	computing at each time step the root segments and the corresponding root length densities on a
	Cartesian grid. The model implements several developmental processes including root
	emission, axial and radial growth, sequential branching, reiteration, transition, decay and
	abscission. Eucalyptus trees.

  4 blocks set up in May 2003 in a site which had been a Eucalyptus grandis plantation from 1998 to 2002 and previously a Eucalyptus saligna Sm. coppice from 1940 to 1998. The experimental layout was described in detail by Laclau et al. (2008) and Le Maire et al. (2013). There were plots with A. mangium May 2009) and only the harvested boles were removed from the plots. Harvest residues were spread uniformly over each plot and A. mangium and E. grandis seedlings were re-planted in November 2009 in the same planting rows of the same plots, at 50 cm from the stumps of the

	previous rotation.
	Our study was carried out 4 years after replanting in 3 treatments within 3 blocks: A. mangium
	and E. grandis monospecific stands (100A and 100E, respectively) and mixed stands with 50%

monoculture, E. grandis monoculture and mixed plantations of A. mangium and E. grandis within each block. Each plot was 30 m x 30 m with two buffer rows. The seedlings were planted at a density of 1111 trees ha -1 (3 m x 3 m spacing). The trees were harvested at age 6 years (in

Table IX .

 IX 1: Main characteristics of the stands at 39 months (mean and standard deviation between blocks, n=3). Different uppercase letters indicate significant differences between treatments, and different lowercase letters indicate significant differences between the monospecific stands and the mixed stands for each species (p < 0.05). The methods used to estimate the aboveground biomass are described inNouvellon et al. (2012b).

	IX.2.3 Root sampling
		100A	100E		50A:50E
		A. mangium	E. grandis	A. mangium	E. grandis	Total
	Stocking density (trees ha -1 )	988 ± 18	1111 ± 0	535 ± 21	556 ± 0	1091 ± 15
	Stand basal area (m 2 ha -1 )	15.3 ± 0.4 B a	16.6 ± 0.4 A a	7.1 ± 0.8 b	9.3 ± 0.6 b	16.4 ± 0.2 A
	Tree height (m)	9.3 ± 0.2 C a	17.8 ± 0.2 A a	9.5 ± 0.3 a	16.8 ± 0.1 b 13.1 ± 0.2 B
	Biomass (kg m -2 ):
	Leaves	0.66 ± 0.02 A a	0.58 ± 0.02 B a	0.22 ± 0.03 b 0.46 ± 0.03 b 0.67 ± 0.01 A
	Branches	0.83 ± 0.02 A a	0.81 ± 0.02 A a	0.31 ± 0.04 b 0.57 ± 0.07 b 0.88 ± 0.03 A
	Bark	0.53 ± 0.01 C a	0.67 ± 0.02 A a	0.18 ± 0.02 b 0.43 ± 0.02 b 0.62 ± 0.00 B
	Wood	1.99 ± 0.05 C a	4.96 ± 0.13 A a	0.80 ± 0.09 b 2.29 ± 0.12 b 3.09 ± 0.03 B
	Aboveground biomass	4.01 ± 0.09 C a	7.03 ± 0.19 A a	1.51 ± 0.17 b 3.75 ± 0.24 b 5.26 ± 0.07 B

Table IX .

 IX 2: Total fine-root biomass down to a depth of 17 m and mean specific root length (SRL), mean specific root area (SRA) and mean fine-root diameter down to a depth of 6 m in 100A, 100E and 50A50E at 4 years of age. Different uppercase letters indicate significant differences between treatments, and different lowercase letters indicate significant differences between the monospecific stands and the mixed stands for each species (p < 0.05).

		100A	100E		50A50E
		A. mangium E. grandis A. mangium E. grandis	Total
	Fine-root biomass (g m -2 )	779.68 B	714.19 B	421.94	696.93	1127.01 A
	Specific root length (m g -1 )	17.98 b	20.53 b	45.63 a	28.11 a
	Specific root area (cm 2 g -1 )	268.36 b	253.57 b	584.11 a	338.55 a
	Diameter (mm)	0.53 b	0.47 a	0.48 a	0.47 a

IRD, UMR Eco&Sols, LMI IESOL, BP 1386, CP 18524 Dakar, Senegal * Corresponding author, E-mail address: amandine.germon@gmail.com

Améliorer notre compréhension de la dynamique spatio-temporelle des racines fines et des gaz à effet de serre dans les couches profondes du sol est un élément clé pour identifier des pratiques sylvicoles plus durables pour les forêts plantées dans un contexte de changement climatique et pour améliorer les modèles biogéochimiques actuels. Notre étude visait à évaluer l'effet de la coupe des arbres et de la sécheresse sur la production de racines fines et les émissions et production de CO2, N2O et CH4 sur un profil de sol profond jusqu'à la nappe phréatique, dans des plantations d'Eucalyptus menées en taillis au Brésil. Les racines fines, d'un diamètre inférieur à 2 millimètres, ont été échantillonnées jusqu'à une profondeur de 17 m sur un dispositif d'exclusion de pluie comparant des peuplements soumis à une exclusion de 37% des pluviolessivats (-W) et des peuplements sans exclusion (+ W). La dynamique des racines a été étudiée à l'aide de minirhizotrons installés dans deux fosses permanentes d'une profondeur de 17 m dans les traitement -W et + W, pendant un an avant la coupe des arbres, puis pendant deux ans en taillis, et jusqu'à 4 m de profondeur dans un peuplement non récolté (NH) servant de témoin. Les flux de CO2, de CH4 et de N2O à la surface du sol ont été mesurés durant trois ans en utilisant la méthode des chambres manuelles dans les traitements -W, + W et NH. Les concentrations de CO2, de CH4 et de N2O dans le sol ont été mesurées à partir des fosses jusqu'à une profondeur de 15.5 m dans les traitements -W, + W et NH durant 3 mois avant la coupe des arbres et 1.5 ans après, en taillis. Après la coupe, nous avons observé une croissance spectaculaire des racines fines en grande profondeur (> 13 m) chez les arbres menés en taillis et, étonnamment, une mortalité extrêmement faible des racines quelle que soit la profondeur et le traitement. La biomasse totale des racines fines jusqu'à 17 m de profondeur dans les traitements menés en taillis était de 1266 et 1017 g m -2 dans + W et -W, respectivement, 1.5 an après la coupe des arbres et de 1078 g m -2 dans le traitement NH, 7.5 ans après la plantation. La longueur spécifique et la surface spécifique des racines étaient environ 15% plus élevées dans -W que dans + W. Les flux de CO2, de CH4 et de N2O ne différaient pas significativement entre -W et + W et ne changeaient pas après la coupe des arbres dans les peuplements menés en taillis par rapport aux peuplements non exploités. Les concentrations de CO2 et de CH4 augmentaient fortement avec la profondeur et les concentrations de N2O restaient à peu près constantes de la surface du sol jusqu'à une profondeur de 15.5 m. Les concentrations moyennes de CO2 et de N2O dans -W étaient respectivement inférieures de 20.7% et 7.6% à celles de + W et celles de CH4 dans -W de 44.4% supérieures à celles de + W sur tout le profil de sol. Un modèle de diffusivité a montré que la production et la consommation de CO2, de N2O et de CH4 se produisaient à de grandes profondeurs et étaient similaires dans les traitements + W, -W et NH. La coupe des arbres n'a pas augmenté les flux et les productions de CO2, de CH4 et de N2O, quel que soit le régime hydrique. La mise en place de systèmes racinaires profonds dans les forêts tropicales plantées pourrait permettre aux arbres de résister aux périodes de sécheresse attendues dans un contexte de changement climatique. Notre étude réalisée dans des peuplements d'eucalyptus gérés en taillis, représentatifs de vastes zones tropicales, suggère que les émissions de gaz à effet de serre pourraient être peu influencées par les modifications de régimes de précipitations dus au changement climatique. Mots clés : Brésil, Eucalyptus grandis, croissance racinaire en profondeur, gaz à effet de serre, exclusion de pluie, sol tropical très profond, taillis

ACKNOWLEDGEMENTS

Une thèse est un marathon en sprint. Et moi qui n'aime pas courir… La thèse, c'est beaucoup de petites taches, qui mises bout à bout, forment un plus grand projet. Ces tâches, mine de rien, ont représenté : 24048 images prises dans les minirhizotrons et analysées ; 3828 seringues collectés et analysés soit 684 heures passées au « labo de la mort » ; 2022 échantillons de sols collectés et 1820 analyses de N minéral au laboratoire ; 307 m de sol collecté soit 578 échantillons de sols lavés pour séparer les racines ; Plus de 400 descentes dans les fosses soit bien plus de 400 heures passées sous terre ; Et surtout un nombre infini de personnes sans qui tout cela n'aurait été possible et je souhaite donc, ici, les en remercier ! Acknowledgements ............................................................................................................ A. Germon 2019 Acknowledgments The study was funded by São Paulo Research Foundation (FAPESP, Project 2015/24911-8), Centre de cooperation Internationale en Recherche Agronomique pour le Développement (CIRAD) and São Paulo University. This study belongs to SOERE F-ORE-T, which is supported annually by Ecofor, Allenvi and the French National Research Infrastructure ANAEE-F (http://www.anaee-france.fr/fr/). We are grateful to the staff at the Itatinga Research Station (ESALQ/USP), Floragro Apoio for their technical support, in particular Eder Araujo da Silva (http://www.floragroapoio.com.br) and our CIRAD colleague Maxime Duthoit. We are grateful to Peter Biggins for correcting the English language. Acknowledgements The study was funded by São Paulo Research Foundation (FAPESP, Project 2015/24911-8 and Project 2017/13572-3), Centre de cooperation Internationale en Recherche Agronomique pour le Développement (CIRAD) and São Paulo University. This study belongs to SOERE F-ORE-T, which is supported annually by Ecofor, Allenvi and the French National Research Infrastructure ANAEE-F (http://www.anaee-france.fr/fr/). We are grateful to the staff at the Itatinga Research Station (ESALQ/USP), Floragro Apoio for their technical support, in particular Eder Araujo da Silva (http://www.floragroapoio.com.br), Dorrival Pires de Arruda and Tiara Moraes Guimarães from the Department of "produção e melhoramento vegetal" and Natália Rodrigues Ferreira Eloy from the Department of "solos e recursos ambientais", São Paulo State University.

Acknowledgements

We are truly grateful to Daise Silva Ferreira for the huge work carried out in the field and in the laboratory. We would like to thank Agence national de la recherche (Intens&fix Project ANR-2010-STRA-004-03) and São Paulo Research foundation (FAFESP, projects 2015/24911-8 and 2011/20510-8) for their financial support. The study belongs to the SOERE F-ORE-T, which is supported annually by Ecofor, Allenvi and the French National Research

Je remercie la Fundação de Amparo à Pesquisa do Estado de São Paulo (FAPESP) pour l'aide financière (Processos nº 2015/24911-8; nº 2017/13572-3). Je remercie le CIRAD pour avoir financé une partie de

LIST OF APPENDIXES

Appendix VI. 1: Time course of soil CO2 efflux (µmol m -2 s -1 ) in the undisturbed rainfall treatment (+W, blue) and in the treatment with 37% of throughfall excluded by plastic sheets (-W, orange) measured every 14 days from October 2016 to October 2017 A) using the Li-8100 closed-path system and B) the closed-chamber method. Standard errors are shown (shaded area). Relationship between soil CO2 efflux (µmol m -2 s -1 ) measured using the Li-8100 closedpath system and the closed-chamber method in exclusion and undisturbed rainfall treatments Appendix VI. 2: Relationship between fine root biomass (diameter < 2mm) and CO2 production cumulated over 1 month (October 2017) in soil layers 0.1-0.5 m, 0.5-1 m, 1-3.5 m, 3.5-7.5 m and 7.5-11.5 m in the undisturbed rainfall treatment (+W, blue) and in the treatment with 37% of throughfall excluded by plastic sheets (-W, orange)

Root traits categories Root trait At depth References

Growth Root biomass Markesteijn and Poorter 2009;Jackson et al. 1996;[START_REF] Gwenzi | Spatial analysis of fine root distribution on a recently constructed ecosystem in a water-limited environment[END_REF][START_REF] Ma | Effects of drip irrigation on deep root distribution, rooting depth, and soil water profile of jujube in a semiarid region[END_REF] Root density Freycon et al. 2015;[START_REF] Gwenzi | Spatial analysis of fine root distribution on a recently constructed ecosystem in a water-limited environment[END_REF][START_REF] Ma | Effects of drip irrigation on deep root distribution, rooting depth, and soil water profile of jujube in a semiarid region[END_REF] Lifespan

Consequences of clear-cutting and drought on fine root dynamics down to 17 m in coppice-managed eucalypt plantations

Amandine Germon 1,2 *, Christophe Jourdan 2,3 , Bruno Bordron 4 , Agnès Robin 2,3,5 , Yann Nouvellon 2,3,4 , Lydie Chapuis-Lardy 2,6 , José Leonardo de Moraes Gonçalves 4 , Céline Pradier 2,3 , Iraê Amaral Guerrini 1 , Jean-Paul Laclau 1,2,3,4

Abstract

Improving our understanding of the spatiotemporal dynamics of fine roots in deep soil layers is of utter importance to manage tropical planted forests in a context of climate change. Our study aimed to assess the effect of clear-cutting and drought on fine-root dynamics down to the water table in Brazilian ferralsol under eucalypt plantations conducted in coppice. Fine roots (i.e. diameter < 2 mm) were sampled down to 17 m deep in a throughfall exclusion experiment comparing stands with 37% of throughfall excluded by plastic sheets (-W) and stands without rain exclusion (+W). Root dynamics were studied using minirhizotron in two permanent pits down to 17 m deep, over 1 year before clear-cutting, then over 2 years in coppice, as well as down to 4 m deep in a non-harvested plot (NH) serving as a control. After harvesting, a spectacular fine root growth of trees conducted in coppice occurred in very deep soil layers (> 13 m) and, surprisingly, root mortality remained extremely low whatever the depth and the treatment. Total fine-root biomass in coppice down to 17 m depth was 1266 and 1017 g m -2 in +W and -W, respectively, at 1.5 year after the clear-cut and was 1078 g m -2 in NH 7.5 years after planting. Specific root length and specific root area were about 15% higher in -W than in +W. Proliferation of fine roots at great depths could be an adaptive mechanism for tree survival, enhancing the access to water stored in the subsoil. The root system established before clearcutting provides access to water stored in very deep layers that probably contribute to mitigate the risk of tree mortality during prolonged drought periods when the eucalypt plantations is conducted in coppice after the clear-cut. Amandine Germon 1,2* ,3 ,Yann Nouvellon 2,4,5 ,Christophe Jourdan 2,4 ,Agnes Robin 2,4,6 ,Joannès Guillemot 2, 4,5 , Ciro Antonio Rosolem 1 , José Leonardo de Moraes Gonçalves 5 , Irae Amaral Guerrini 1 , Jean-Paul Laclau 1,2,4,5

Consequences of clear-cutting and drought on CO2, CH4 and N2O productions throughout deep soil profiles in coppice-managed eucalypt plantations

Abstract

The major factors driving greenhouse gas exchanges in forest soils (substrate supply, temperature, water content) can vary considerably with depth. Our study aimed to assess the effects of clear-cutting and drought on the temporal variability of CO2, CH4 and N2O fluxes throughout very deep soil profiles in Brazilian coppice-managed eucalypt plantations. CO2, CH4 and N2O surface effluxes at soil surface were measured over three years using the closedchamber method in a throughfall exclusion experiment comparing stands with 37% of throughfall exclusion (-W) and stands without rain exclusion (+W). CO2, CH4 and N2O concentrations in the soil were measured from two permanent pits down to a depth of 15.5 m in -W and +W, as well as down to a depth of 4 m in a non-harvested control plot (NH).

Measurements were carried out every 2 weeks over 3 months before clear-cutting, then over 19 months in coppice. CO2, CH4 and N2O effluxes were not significantly different between -W and +W and did not change after clear-cutting in the coppice-managed stands compared to nonharvested stand. CO2 and CH4 concentrations greatly increased with depth and N2O concentrations remained roughly constant from the soil surface down to a depth of 15.5 m.

Mean CO2 and N2O concentrations in -W were 20.7% and 7.6% lower than in +W, respectively, and CH4 concentrations in -W where 44.4% higher than in +W throughout the soil profiles. A diffusivity model showed that CO2, N2O and CH4 production and consumption occurred at great depths and were similar in +W, -W and NH plots. Clear-cutting did not increase CO2, CH4 and N2O effluxes and productions, whatever the water supply regime. Our study suggests that the consequences of changes in rainfall regimes and silvicultural practices on greenhouse gas emissions could be minor in tropical eucalypt plantations.

Appendix

Appendix VI. 1: Time course of soil CO2 efflux (µmol m -2 s -1 ) in the undisturbed rainfall treatment (+W, blue) and in the treatment with 37% of throughfall excluded by plastic sheets (-W, orange) measured every 14 days from October 2016 to October 2017 A) using the Li-8100 closed-path system and B) the closed-chamber method. Standard errors are shown (shaded area). Relationship between soil CO2 efflux (µmol m -2 s -1 ) measured using the Li-8100 closedpath system and the closed-chamber method in exclusion and undisturbed rainfall treatments (C).

Appendix VI. 2: Relationship between fine root biomass (diameter < 2mm) and CO2 production cumulated over 1 month (October 2017) in soil layers 0.1-0.5 m, 0.5-1 m, 1-3.5 m, 3.5-7.5 m and 7.5-11.5 m in the undisturbed rainfall treatment (+W, blue) and in the treatment with 37% of throughfall excluded by plastic sheets (-W, orange). Fine roots were sampled in October 2017.

What to remember from Chapter 6?

The main results of this chapter are summarized in the following Table VI Eucalyptus grandis trees in a throughfall exclusion experiment, comparing plots with 37% of throughfall excluded by plastic sheets (-W), and plots without rain exclusion (+W). The main results obtained over 3 months before clear-cutting, then over 18 months in coppice, showed that CO2 concentrations increased on average from 4475 ± 2180 ppm at a soil depth of 10 cm to 15885 ± 3538 ppm at a depth of 15.5 m across the two water supply regimes. CO2

concentrations measured in treatment -W were on average 20.7% lower than in treatment +W, across the sampling depths.

We intended to go beyond the current measurements of gas concentrations at different depths in the soil profile through a mechanistic modeling approach making it possible to assess the production of gas throughout the soil profiles and to infer the sensibility of gas production to environmental factors. To better understand the dynamics of organic matter in deep tropical soils and to improve the modeling of element flows, it is necessary to quantify in situ the carbon (CO2 as well as dissolved inorganic and organic C) concentrations throughout entire soil profiles (down to the root front), and to characterize the carbon stabilization/destabilization processes, as well as the main regulatory factors. A modeling approach was required to (i) quantify the production of CO2 in different soil horizons from soil properties, root growth and gas concentration measurements throughout the profile, and (ii) to improve our understanding of transfer processes and the contribution of CO2 deep production mechanisms to soil surface emissions [START_REF] Maier | Using the gradient method to determine soil gas flux: A review[END_REF].

Reactive transport models derived from Darcy's law allows a dynamic description of transient water flow in soils but also chemical processes controlling soil solution chemical composition [START_REF] Feyen | Modelling water flow and solute transport in heterogeneous soils: A review of recent approaches[END_REF][START_REF] Simunek | The HYDRUS software package for simulating the two-and three-dimensional movement of water, heat, and multiple solutes in variably-saturated media[END_REF][START_REF] Samouëlian | Upscaling hydraulic conductivity based on the topology of the sub-scale structure[END_REF][START_REF] Steefel | Reactive transport codes for subsurface environmental simulation[END_REF]. Reactive transport models require a vast number of input parameters and careful calibration procedures. Min3P is particularly suitable for the current study thanks to its implementation of the uptake of water and solute by plants [START_REF] Gérard | Preferential flow revealed by hydrologic modeling based on predicted hydraulic properties[END_REF][START_REF] Gérard | Modelling the biogeochemical cycle of silicon in soils: application to a temperate forest ecosystem[END_REF]. Indeed, gas transfer in the soil is highly dependent on soil water content and modeling soil water fluxes is therefore compulsory (Figure VIII. 6). Separate sink terms have been implemented in the Richard's equation to account for physical evaporation and transpiration (components of the root water uptake) in Min3P. For each control volume of the grid, the physical evaporation is depending on the local water saturation and is considered as a one-dimensional process in vertical direction along a soil column. To model the biological plant transpiration process, the evaporative budget must be estimated and is determined with the soil moisture, allowing the consideration of the negative effects of water stress on plant transpiration. Finally, the solute uptake has been implemented by an additional sink term in the mass balance equation. Then, two uptake regimes

Soil parameterization and root profiles

Three layers of 33.3 cm thickness were defined to account for the variability of soil and root characteristics in the upper meter. Layers of 50 cm were defined from a depth of 1m to a depth of 18 m. Soil retention curves and hydraulic conductivity were estimated at the same site using Van Genuchten equations. In each soil layer, the soil water potential was linked to the soil water content by the relation of [START_REF] Van Genuchten | A closed-form equation for predicting the hydraulic conductivity of unsaturated soils 1[END_REF].

Supplementary Article

In addition to the studies presented in this thesis, during my thesis, I had the opportunity to study the consequences of mixing Acacia mangium and Eucalyptus grandis trees on soil exploration by roots down to the water table at 17 m depth in a tropical planted forest.

Eucalyptus plantation mixed with nitrogen fixing trees can be considered as a form of ecological intensification through the increase of forest plantations production and nutrient availability in the soil (Bouillet et al. 2012, Forrester et al., 2005;Kelty, 2006). Multi-purpose plantations can provide key ecosystem services [START_REF] Paquette | The role of plantations in managing the world's forests in the Anthropocene[END_REF], in some situations, increase the total biomass production [START_REF] Forrester | The spatial and temporal dynamics of species interactions in mixed-species forests: from pattern to process[END_REF][START_REF] Richards | The influence of mixed tree plantations on the nutrition of individual species: a review[END_REF] and positive relationships between tree diversity and soil fauna, microbial diversity, and soil carbon (C) sequestration are well documented [START_REF] Blaser | Woody encroachment reduces nutrient limitation and promotes soil carbon sequestration[END_REF][START_REF] Forrester | The spatial and temporal dynamics of species interactions in mixed-species forests: from pattern to process[END_REF][START_REF] Richards | The influence of mixed tree plantations on the nutrition of individual species: a review[END_REF]. But the consequences of mixing trees on root growth and fine-root morphology in very deep soil layers is poorly know.

In this study, root sampling was realized down to 17 m in A. mangium and E. grandis monospecific stands and a mixture with 50% of each species using the method described in chapter 5. In this study, I did not contribute to the acquisition of the data, but I contributed to the data analysis as well as the statistical analyses and the writing of the paper.

This article is intitled "Consequences of mixing Acacia mangium and Eucalyptus grandis trees on soil exploration by fine-roots down to a depth of 17 m". Co-authors associated with this project are Iraê Amaral Guerrini, Bruno Bordron, Jean-Pierre Bouillet, Yann Nouvellon, José Leonardo de Moraes Gonçalves, Christophe Jourdan, Ranieri Ribeiro Paula and Jean-Paul Laclau.

This article was published in the journal Plant and Soil.

Consequences of mixing Acacia mangium and Eucalyptus grandis trees on soil exploration by fine-roots down to a depth of 17 m

Amandine Germon 1,2 , Iraê Amaral Guerrini 1 , Bruno Bordron 3 , Jean-Pierre Bouillet 2,3,4 , Yann Nouvellon 2,3,4 , José Leonardo de Moraes Gonçalves 3 , Christophe Jourdan 2,4 , Ranieri Ribeiro Paula

Abstract:

Background and Aims Fine-root functioning is a major driver of plant growth and strongly influences the global carbon cycle. While fine-root over-yielding has been shown in the upper soil layers of mixed-species forests relative to monospecific stands, the consequences of tree diversity on fine-root growth in very deep soil layers is still unknown. Our study aimed to assess the consequences of mixing Acacia mangium and Eucalyptus grandis trees on soil exploration by roots down to the water table at 17 m depth in a tropical planted forest.

Method Fine roots (diameter < 2 mm) were sampled in a randomized block design with three treatments: monospecific stands of Acacia mangium (100A), Eucalyptus grandis (100E), and mixed stands with 50% of each species (50A50E). Root ingrowth bags were installed at 4 depths (from 0.1 m to 6 m) in the three treatments within three different blocks, to study the fine-root production over 2 periods of 3 months.

Results Down to 17 m depth, total fine-root biomass was 1127 g m -2 in 50A50E, 780 g m -2 in 100A and 714 g m -2 in 100E. Specific root length and specific root area were 110-150% higher in 50A50E than in 100A for Acacia mangium trees and 34% higher in 50A50E than in 100E

for Eucalyptus grandis trees. Ingrowth bags showed that the capacity of fine roots to explore soil patches did not decrease down to a depth of 6 m for the two species.

Conclusions Belowground interactions between Acacia mangium and Eucalyptus grandis trees greatly increased the exploration of very deep soil layers by fine roots, which is likely to enhance the uptake of soil resources. Mixing tree species might therefore increase the resilience of tropical planted forests through a better exploration of deep soils. Improving our understanding of the spatiotemporal dynamics of fine roots and greenhouse gases in deep soil layers is a key component to identify more sustainable silvicultural practices for planted forests in a context of climate change and to improve the current biogeochemical models. Our study aimed to assess the effect of clear-cutting and drought on fine-root production, soil CO2, CH4 and N2O effluxes and production throughout deep soil profiles down to the water table in Brazilian coppicemanaged Eucalyptus plantations. Fine roots (i.e. diameter < 2 mm) were sampled down to a depth of 17 m in a throughfall exclusion experiment comparing stands with 37% of throughfall excluded by plastic sheets (-W) and stands without rain exclusion (+W). Root dynamics were studied using minirhizotron in two permanent pits down to a depth of 17 m in treatments -W and +W, over 1 year before clear-cutting, then over 2 years in coppice, as well as down to a depth of 4 m in a non-harvested plot (NH) serving as a control. CO2, CH4 and N2O surface effluxes were measured over three years using the closed-chamber method in treatments -W, +W and NH. CO2, CH4 and N2O concentrations in the soil were measured from the pits down to a depth of 15.5 m in treatments -W, +W and NH over 3 months before the clear-cut and 1.5 years after in coppice. After harvesting, spectacular fine root growth of trees conducted in coppice occurred in very deep soil layers (> 13 m) and, surprisingly, root mortality remained extremely low whatever the depth and the treatment. Total fine-root biomass in coppice down to a depth of 17 m was 1266 and 1017 g m -2 in treatments +W and -W, respectively, at 1.5 years after the clear-cut and was 1078 g m -2 in NH 7.5 years after planting. Specific root length and specific root area were about 15% higher in -W than in +W. CO2, CH4, and N2O effluxes were not significantly different between treatments -W and +W and did not change after clear-cutting in the coppice-managed stands compared to non-harvested stand. CO2 and CH4 concentrations greatly increased with depth and N2O concentrations remained roughly constant from the soil surface down to a depth of 15.5 m. Mean CO2 and N2O concentrations in -W were 20.7% and 7.6% lower than in +W, respectively, and CH4 concentrations in -W were 44.4% higher than in +W throughout the soil profiles. A diffusivity model showed that CO2, N2O and CH4 production and consumption occurred at great depths and were similar in treatments +W, -W and NH. Clear-cutting did not increase CO2, CH4 and N2O effluxes and productions, whatever the water supply regime. Establishing deep root systems in tropical planted forests could help trees withstand the long drought periods expected under climate change in many tropical regions. Our study suggested that coppice management might be an interesting option in tropical Eucalyptus plantations, both to improve tree tolerance to drought and store carbon at great depth in the soil. Keywords: Brazil, Eucalyptus grandis, deep root growth, greenhouse gases, throughfall exclusion, very deep tropical soil, coppice Conséquence de la coupe rase sur la production de racines fines, CO2, CH4 et N2O jusqu'à la nappe phréatique dans une plantation d'Eucalyptus grandis menée en taillis sur un dispositif d'exclusion de pluie.