Victoria J Burton

Sara Contu

Adriana De Palma

Samantha L L Hill

Harald Albrecht

James S Bone

Daniel Carpenter

Ronald Corstanje

Pallieter De Smedt

Mark Farrell

Helen V Ford

Lawrence N Hudson

Kelly Inward

David T Jones

Agnieszka Kosewska

Nancy F Lo-Man-Hung

Tibor Magura

Christian Mulder

Maka Murvanidze

Tim Newbold

Jo Smith

Andrew V Suarez

Sasha Suryometaram

Béla Tóthmérész

Marcio Uehara-Prado

Adam J Vanbergen

Kris Verheyen

Karen Wuyts

Jörn P W Scharlemann

Paul Eggleton

Andy Purvis

Land use and soil characteristics affect soil organisms differently from above-ground assemblages

Keywords: Land-use, Land-use intensity, Soil biota, Soil biodiversity, Organism abundance, Mixed-effects models

Background

Terrestrial biodiversity continues to decline globally in the face of increasing human impacts [START_REF] Díaz | Pervasive human-driven decline of life on Earth points to the need for transformative change[END_REF], with land-use change and intensification the biggest driver of recent biodiversity loss [START_REF] Jaureguiberry | The direct drivers of global anthropogenic biodiversity loss[END_REF]. Species extinction rates are estimated to be around 10-1000 times higher than the background rate [START_REF] Pimm | The biodiversity of species and their rates of extinction, distribution, and protection[END_REF], with 1 million plant and animal species threatened with extinction and the Living Planet Index (which reflects trends in vertebrate population size) declined by 69% between 1970 and 2022 [START_REF]Living Planet Report 2022-Building a nature-positive society[END_REF]. However, these assessments and indicators focus on data-rich taxa, especially vertebrates, and so may not reflect broader biodiversity patterns [START_REF] Norris | Biodiversity in the context of ecosystem services: the applied need for systems approaches[END_REF].

Organisms that live in the soil and leaf litter (henceforth, soil biodiversity) are particularly poorly represented in indicators and assessments of the global state of nature [START_REF] Phillips | Red list of a black box[END_REF][START_REF] Guerra | Tracking, targeting, and conserving soil biodiversity: a monitoring and indicator system can inform policy[END_REF]. This is despite the fact that they comprise 23% of described living species, support ecosystem services, such as nutrient cycling, soil formation and water quality [START_REF] Bardgett | Belowground biodiversity and ecosystem functioning[END_REF][START_REF] Fao | State of knowledge of soil biodiversity-Status, challenges and potentialities[END_REF], valued at $2.1 trillion per year worldwide [START_REF] Jónsson | Classification and valuation of soil ecosystem services[END_REF] and form the second largest carbon pool on Earth

Open Access

BMC Ecology and Evolution *Correspondence: v.burton@nhm.ac.uk 2 Natural History Museum, London, UK Full list of author information is available at the end of the article [START_REF] Bar-On | The biomass distribution on Earth[END_REF]. This poor representation partly reflects data limitations: taxonomic discovery is less complete for many groups of soil species than those above ground, their distributions are less well known, and their assemblage structure is less often quantified [START_REF] Wall | Biodiversity in the dark[END_REF][START_REF] Hortal | Seven shortfalls that beset large-scale knowledge of biodiversity[END_REF]. Additionally, because soil biodiversity samples are often not identified to the species level and because soil-dwelling species may be more taxonomically inclusive ('lumped') than aboveground species [START_REF] Bardgett | Causes and consequences of biological diversity in soil[END_REF][START_REF] Decaëns | Macroecological patterns in soil communities[END_REF], estimates of diversity may not be comparable with those for better-known taxa. Although soil and above-ground communities are linked mechanistically [START_REF] Bardgett | Belowground biodiversity and ecosystem functioning[END_REF][START_REF] Wardle | Linkages between plant litter decomposition, litter quality, and vegetation responses to herbivores[END_REF], they often show different patterns of diversity [START_REF] Cameron | Global mismatches in aboveground and belowground biodiversity[END_REF][START_REF] Provost | Contrasting responses of above-and belowground diversity to multiple components of land-use intensity[END_REF]. Soil characteristics can also affect biodiversity within both soil and above-ground assemblages. Soils are a fundamental determinant of plant communities [START_REF] Hulshof | The edaphic control of plant diversity[END_REF], with soil biota being linked to them directly through symbiosis and herbivory, and indirectly via decomposition and nutrient cycling [START_REF] Sylvain | Linking soil biodiversity and vegetation: implications for a changing planet[END_REF], but global patterns of soil fauna biomass may not follow plant biomass [START_REF] Fierer | Global patterns in belowground communities[END_REF].

We analyse biodiversity data [START_REF] Hudson | The PREDICTS database: a global database of how local terrestrial biodiversity responds to human impacts[END_REF][START_REF] Hudson | The database of the PREDICTS (Projecting Responses of Ecological Diversity In Changing Terrestrial Systems) project[END_REF] from 19,651 above-ground and 7155 soil assemblages (comprising vertebrates, invertebrates, plants, and fungi) (Table 1) in different land uses worldwide (Fig. 1 and Table 2), alongside global datasets of soil characteristics [START_REF] Hengl | SoilGrids250m: global gridded soil information based on machine learning[END_REF]. Because soil assemblage data are often less taxonomically precise than data from above-ground assemblages, the response variable we model is the summed abundance of all taxa sampled. This measure is very much less sensitive to change than more information-rich measures that incorporate species identity [START_REF] Hillebrand | Biodiversity change is uncoupled from species richness trends: consequences for conservation and monitoring[END_REF], but it has the advantage that significant differences between models cannot be artefacts of differences in taxonomic precision. The Soil Biodiversity Observation Network (SoilBON) have proposed population abundance as an Essential Biodiversity Variable [START_REF] Guerra | Tracking, targeting, and conserving soil biodiversity: a monitoring and indicator system can inform policy[END_REF].

To accommodate heterogeneity due to the wide range of sampling methods and macroecological gradients in the dataset we used mixed-effects models to test three main hypotheses (expanded on in Additional file 1: Table S1): (1) Because some land uses imply very different levels of perturbation to soil versus above-ground microenvironments, and because soil organisms are less mobile and more sensitive to microclimate change [START_REF] Collison | Macrofauna assemblage composition and soil moisture interact to affect soil ecosystem functions[END_REF], we expect differences in how assemblages from these two settings respond to land use. For example, using land to rear livestock may impact soil structure much less than aboveground habitat structure, while soil organisms may take longer than above-ground taxa to recolonise sites recovering from physical soil disturbance [START_REF] Bengtsson | Disturbance and resilience in soil animal communities[END_REF][START_REF] Adl | Slow recovery of soil biodiversity in sandy loam soils of Georgia after 25 years of no-tillage management[END_REF][START_REF] Chang | Recovery of Collembola in Pinus tabulaeformis plantations[END_REF]. [START_REF] Jaureguiberry | The direct drivers of global anthropogenic biodiversity loss[END_REF] Because physical properties of soil, such as pH and soil texture, themselves mediate the impacts of land use microenvironments, we expect these properties to influence assemblage responses to land use. For instance, moisture retention by clay-rich soils may mitigate the warming and drying effects of agriculture.

(3) Although above-ground and soil assemblages are linked mechanistically, we do not expect soil properties to shape their assemblage-level responses to land use in the same way.

To offset the different geographic biases in soil versus above-ground assemblages we ran a weighted model. Weights were calculated by dividing the number of soil sites by the number of above-ground sites within each biome. In addition to the models required to test the three hypotheses, we also constructed a set of simpler models with single or additive terms to fully characterise which terms in the full model contributed the most explanatory power. We also undertook two sensitivity analyses. Because the biome-weighting is not commonplace (despite the ubiquity of geographic biases in biodiversity databases [START_REF] Tydecks | Spatial and topical imbalances in biodiversity research[END_REF]), our first sensitivity analysis repeated the modelling without it. The second sensitivity analysis addresses the point that soil and above-ground assemblage data sets obviously have very different compositions in terms of which major taxonomic groups are well represented. While different impacts of land use on soil and above-ground assemblages would still be important even if they simply reflected such taxonomic differences, we also ran the same models using only the data for invertebrate taxa.

Results

Estimated effects of land use differed markedly between soil and above-ground biota (Table 3); relative to primary vegetation, soil assemblages had lower abundance than above-ground assemblages in secondary vegetation and (especially) plantation forest and cropland, but higher abundance in pasture (Fig. 2).

Soil properties, especially bulk density, affected how soil fauna abundance responds to land use (Fig. 3, Table 3). These effects were not consistent among land uses; for example, abundance correlated positively with bulk density among cropland and plantation sites but not among pasture sites (Fig. 3). Soil properties also mediated the responses of above-ground assemblages to land use, in ways that differed from how they shaped the responses of soil assemblages (Table 3). Like the soil biota, effects on above-ground biodiversity were not consistent among land uses, e.g., the positive correlation between aboveground organism abundance and organic carbon was more pronounced in cropland and pasture than in other land uses (Fig. 3).

As expected with such heterogeneous data, most of the explained variation was attributed to random effects; but interactions increased the explanatory power of the fixed effects by nearly half, from 14% to 20% (Additional file 1: Fig. S1). The unweighted model found broadly similar patterns between above-ground and soil assemblage responses to land use but had lower explanatory power Fig. 1 Locations where above-ground (green points, 19,651 sites/locations) and soil (orange points, 7155 sites/locations) biodiversity were sampled. The density plot shows the latitudinal distribution of above-ground (green) and soil (orange) sites (see Additional file 1). Compared to the pattern shown in Fig. 2, analysis of the invertebrate-only data found a bigger difference in the effects of plantations on soil versus above-ground assemblages, but a negligible difference in how cropland affected them (see Additional file 1).

Discussion

Land use-the recent main driver of biodiversity loss worldwide [START_REF] Díaz | Pervasive human-driven decline of life on Earth points to the need for transformative change[END_REF][START_REF] Jaureguiberry | The direct drivers of global anthropogenic biodiversity loss[END_REF]-affects soil assemblages differently from those above ground. As hypothesised, croplandwhere tillage, pesticides and fertilisers disturb soil biodiversity [START_REF] Tsiafouli | Intensive agriculture reduces soil biodiversity across Europe[END_REF][START_REF] Postma-Blaauw | Soil biota community structure and abundance under agricultural intensification and extensification[END_REF]-reduces abundance even more in the soil than above ground. In contrast, pasture-with relatively little physical disturbance of the soil and often increased nutrient input [START_REF] Curry | Relationships between earthworm populations and management intensity in cattle-grazed pastures in Ireland[END_REF][START_REF] Li | Management effects on soil nematode abundance differ among functional groups and land-use types at a global scale[END_REF]-shows the opposite pattern. Clear-felling and replanting with different tree species has been previously found to have the strongest negative impact on biodiversity [START_REF] Paillet | Biodiversity differences between managed and unmanaged forests: meta-analysis of species richness in Europe[END_REF], and we also find a strong negative effect of plantation on biodiversity. The much lower relative abundance in soil than above-ground assemblages (Fig. 2) may be explained by the acidified soil and recalcitrant leaf litter typical of conifer plantations [START_REF] Augusto | Impact of tree species on forest soil acidification[END_REF] (the dominant type in the soil assemblage data), together with drier soils in plantations that have a reduced under-story [START_REF] Collison | Macrofauna assemblage composition and soil moisture interact to affect soil ecosystem functions[END_REF]. Soil organism abundance has not recovered in secondary vegetation as much as aboveground abundance (Fig. 2), in keeping with our hypothesis that soil biota recovers more slowly to disturbance than above-ground biodiversity.

As well as affecting the overall abundance of soil organisms, soil properties also mediated how land use affected soil assemblages (left-hand column of Fig. 3). Perhaps more surprisingly, soil properties also affected how above-ground assemblages responded to land use, in ways that differed from their effect on the responses of soil assemblages (right-hand column of Fig. 3, Table 3). Above-ground abundance generally increased with organic carbon, which is as expected given the latter's close link with plant productivity [START_REF] Bauer | Quantification of the effect of soil organic matter content on soil productivity[END_REF]. Abundance was generally higher in more clay-rich soils, which typically have more nutrients and retain water better [START_REF] Coleman | Fundamentals of Soil Ecology[END_REF]. These effects of soil properties will include both direct, and indirect effects medicated by biotic interactions, but we were unable to separate these as few studies collected data on above-ground and soil biota concurrently.

The greater impact of cropland and plantation forestry on soil biota than above-ground assemblages shown by our models is a cause for serious concern. To feed the growing population, scenarios include the world's croplands increasing in area, being managed more intensively, or both [START_REF] Zabel | Global impacts of future cropland expansion and intensification on agricultural markets and biodiversity[END_REF]. The rapid recent expansion of plantation forests may accelerate further if they receive subsidies for carbon sequestration, despite their impacts on biodiversity [START_REF] Heilmayr | Impacts of Chilean forest subsidies on forest cover, carbon and biodiversity[END_REF]. Pathways to sustainable development must avoid the diminution of soil assemblages that would undermine the long-term provision of soil ecosystem services [START_REF] Díaz | Pervasive human-driven decline of life on Earth points to the need for transformative change[END_REF]. This highlights the likely importance of soil biodiversity for the ecological intensification of agriculture [START_REF] Kleijn | Ecological intensification: bridging the gap between science and practice[END_REF] and of considering soil biodiversity explicitly in formulating conservation policy [START_REF] Guerra | Tracking, targeting, and conserving soil biodiversity: a monitoring and indicator system can inform policy[END_REF].

Our division of assemblages into soil and above-ground was based on how they were sampled rather than on ecosystem ecology. Many organisms sampled by aboveground methods spend part of their life cycle in the soil (e.g., many flies, bees and beetles), or even have much of their biomass underground (e.g., most plants). The soil assemblages have a very different taxonomic composition from those above-ground (Table 1) and different taxonomic groups are expected to respond differently to land use and soil properties [START_REF] Decaëns | Macroecological patterns in soil communities[END_REF][START_REF] Van Capelle | Tillage-induced changes in the functional diversity of soil biota-a review with a focus on German data[END_REF][START_REF] Sünnemann | The effects of drought and nutrient addition on soil organisms vary across taxonomic groups, but are constant across seasons[END_REF]. An example of this can be seen in the invertebrate-only results (see Supplemental Information), here both above-ground and soil invertebrates are equally impacted in cropland, but above-ground invertebrate abundance is greater than soil invertebrates in plantation sites. Further work with models incorporating functional traits robust to coarse taxonomic resolution would be valuable. Better documentation of the taxonomic and functional diversity of soil fauna would also help overcome some of these limitations, so we echo calls for better soil biodiversity information systems [START_REF] Phillips | Red list of a black box[END_REF][START_REF] Ramirez | Toward a global platform for linking soil biodiversity data[END_REF]. Additionally, except for fungi, micro-organisms are unrepresented in both soil and above-ground datasets-assemblage data from metabarcoding and metagenomic approaches [START_REF] Guerra | Tracking, targeting, and conserving soil biodiversity: a monitoring and indicator system can inform policy[END_REF][START_REF] Orgiazzi | Soil biodiversity and DNA barcodes: opportunities and challenges[END_REF] will enable the use of more information-rich biodiversity measures.

Above-ground and taxa may be active and sampled at very different spatial scales, and soil property data with a spatial resolution of 250 m used here may not accurately reflect that experienced by the biota. Site-specific soil property data were available for some studies used in this analysis but were too insufficient or inconsistent to incorporate. Better standardisation of soil biodiversity surveys with a minimum level of environmental measurements collected would be a valuable contribution to the field [START_REF] Fao | State of knowledge of soil biodiversity-Status, challenges and potentialities[END_REF][START_REF] Potapov | Global monitoring of soil animal communities using a common methodology[END_REF] as would explicit tests of spatial and temporal heterogeneity [START_REF] Chust | Response of soil fauna to landscape heterogeneity: determining optimal scales for biodiversity modeling[END_REF]. Likewise, models that consider other drivers, such as climate change, alongside land use will also improve understanding. Correlative models such as ours are sufficient for developing indicators and models for monitoring and combating biodiversity loss but there is also a need for an improved understanding of the mechanisms linking land use, soil properties, and biodiversity responses [START_REF] Bardgett | Belowground biodiversity and ecosystem functioning[END_REF][START_REF] Creamer | The life of soils: integrating the who and how of multifunctionality[END_REF]. Future analysis of this dataset using structural equation models (SEMs) could be used towards this, to disentangle the direct and indirect effects of soil properties and land use on communities. However, the limitations of our data and models do not detract from the central implication that soil and above-ground assemblages respond differently to land use: inferences drawn from what lives above ground cannot safely be extended to the soil biota.

Conclusions

We show that soil biodiversity does not respond the same way to land use and soil properties as aboveground assemblages. The most widely used indicators of biodiversity, e.g. the Red List Index [START_REF]IUCN Red List 2017-2020 Report[END_REF] and the Living Planet Index [START_REF] Mcrae | The diversity-weighted living planet index: controlling for taxonomic bias in a global biodiversity indicator[END_REF], include few or no soil taxa [START_REF] Phillips | Red list of a black box[END_REF]. This means that current indicators, models, and frameworks for monitoring and combating biodiversity loss may be insufficient to safeguard the soil biodiversity needed to underpin ecosystem function.

Methods

Biodiversity data

In the absence of a well-developed catalogue of global soil biodiversity [START_REF] Ramirez | Toward a global platform for linking soil biodiversity data[END_REF], we initially searched within the PRE-DICTS database [START_REF] Hudson | The PREDICTS database: a global database of how local terrestrial biodiversity responds to human impacts[END_REF][START_REF] Hudson | The database of the PREDICTS (Projecting Responses of Ecological Diversity In Changing Terrestrial Systems) project[END_REF] for soil assemblage data, defining soil assemblages as those sampled within the soil; at the soil surface, or in the leaf litter. The database is a global compilation of studies that have each compared non-cultivated species assemblages at multiple sites facing different landuse and related pressures [START_REF] Hudson | The PREDICTS database: a global database of how local terrestrial biodiversity responds to human impacts[END_REF]. To the 59 studies (from 38 source publications with 1356 sites and 1570 taxa) of soil assemblage data previously in the PREDICTS database, we added 46 further studies (from 25 sources with 2726 sites and 3857 taxa (Tables 1 and2 ). Above-ground assemblage data came from the other 509 studies (from 422 source publications, with 20,634 sites and 22,721 taxa) in the PRE-DICTS database at that time (October 2016).

The fraction of taxa resolved to species level was over twice as high in the above-ground assemblages as in the soil assemblages (58% versus 28%). Given this, plus the likelihood that species-level taxa are more inclusive in soil than above-ground organisms (i.e., the latter tend to be subdivided more finely when species are demarcated [START_REF] Decaëns | Macroecological patterns in soil communities[END_REF]), measures that use compositional information (such as diversity indices, or even numbers of species) cannot be compared between soil and above-ground assemblages. We therefore used the summed abundance across all sampled taxa-which is unaffected by taxonomic precision-as the site-level response variable. Whenever sampling effort varied among sites within a study, any abundance data sensitive to it (i.e., metrics not already reported as numbers per unit time, distance, area, or volume) were divided by sampling effort. Finally, abundance values were rescaled within each study to have a maximum value of 1, reducing among-study heterogeneity and thereby aid model convergence.

Explanatory variables

Using the information in the original papers, each site was classified into one of six categories of land use-primary vegetation, secondary vegetation, plantation forest, cropland, pasture or urban-and either low, medium, or high use intensity (see Additional file 1 and [START_REF] Hudson | The PREDICTS database: a global database of how local terrestrial biodiversity responds to human impacts[END_REF] for full definitions). Most combinations of land use and use intensity (henceforth, LUI) had large enough sample sizes in both the above-ground and soil subsets, but even after targeted literature searching to augment the database's holdings of urban data, there were insufficient sites for robust comparison of above-and below-ground in urban land use sites. The above-ground subset comprised primarily arthropods, plants, and vertebrates whereas the soil biodiversity subset was mostly arthropods (Table 1).

Nine soil properties widely reported to influence soil biodiversity (Additional file 1: Table S1) were obtained from the SoilGrids250m database [START_REF] Hengl | SoilGrids250m: global gridded soil information based on machine learning[END_REF] using ESRI Arc-GIS 10.3 [51]. Values were not available for 49 sites, which were therefore removed from the analysis. We averaged the values from depths 0, 5, 15 and 30 cm as no biodiversity data sources sampled at depths greater than 30 cm. The soil properties were expected to be collinear so, before model construction began, generalised variance inflation factors (GVIFs) were calculated [START_REF] Zuur | Mixed effects models and extension in ecology with R[END_REF]. Among the soil texture properties, the percentage of clay had the lowest GVIF so was chosen in preference to percentages of silt or sand. Successively dropping the variable with the highest GVIF until all remaining GVIFs were low enough to suggest collinearity was not a major issue (all GVIF < 1.5), led to all soil moisture properties being dropped, while pH, bulk density, organic carbon, and clay percentage were retained.

Biome weighting

To offset the geographic bias in soil versus above-ground assemblages (Fig. 1), we applied weights in the models. Weights were calculated by dividing the number of soil sites by the number of above-ground sites within each biome (Additional file 1: Table S2). Weights were calculated separately for the invertebrate-only subset (not shown).

Statistical analysis

All analyses were carried out in R 3.5.1 [START_REF] Core | R: a language and environment for statistical computing[END_REF]. Because total abundance contained non-integers even before rescaling, it was log(x + 1) transformed before modelling with Gaussian errors. The studies in the dataset vary widely in many aspects of sampling. We therefore fitted mixedeffects models (as implemented in lme4 version 1.1.18.1 [START_REF] Bates | Fitting linear mixed-effects models using lme4[END_REF] with bobyqa numerical optimisation) to reduce heterogeneity caused by among-study differences in sampling methodology and macroecological gradients such as latitude.

Our previously listed hypotheses were tested by comparing a maximally complex model with three simpler models (see Additional file 1 for model structures) that lacked the hypothesised effects. The full model included six main fixed effects-land-use type and intensity (LUI), above-ground or soil assemblage (habitat layer), and the four soil properties (rescaled to the range 0-1 to aid fitting)-plus each soil property's interaction with land-use type and habitat layer, the interaction between land-use type and habitat layer, and the three-way interactions of each soil property with land-use type and habitat layer. The random-effects structure was chosen by comparing the Akaike's Information Criterion (AIC) of models having the full set of fixed effects plus, as random intercepts, (a) spatial block nested within study identity, (b) spatial block identity, or (c) study identity [START_REF] Zuur | Mixed effects models and extension in ecology with R[END_REF]; models with random slopes did not converge. The optimal randomeffects structure was then retained for all models. To ascertain the influence of use intensity on the full model was compared to one with only land use. To test whether above-ground and soil assemblages respond differently to land use, the full model was compared to one in which habitat layer could not interact with other explanatory variables. The importance of soil properties in shaping assemblage responses to land use was tested by comparing the full model to one in which soil properties were included as main effects but could not interact with LUI. Whether effects of soil properties differ for above-ground and soil assemblages was tested by comparing the full model to one in which neither the soil properties nor their interactions with land use could interact with habitat layer.

In addition to the models required to test the three hypotheses, we also constructed a set of simpler models with single or additive terms to fully characterise which terms in the full model contributed most explanatory power. The variance explained by fixed effects alone (marginal R 2 glmm ) and fixed and random effects combined (conditional R 2 glmm ) were calculated using the MuMIn package [START_REF] Nakagawa | A general and simple method for obtaining R2 from generalized linear mixed-effects models[END_REF] as measures of explanatory power. The random effects and spatial blocks intended to accommodate the heterogeneity among studies are expected to explain much more of the variance than the fixed effects. Consequently, when comparing models in terms of the explanatory power of their fixed effects, we compare their marginal R 2 glmm / (1 -conditional R 2 glmm ). We repeated the analyses without the weighting procedure used to compensate for the different geographic biases of above-ground and soil assemblage data (results in Additional file 1).

Fig. 2

 2 Fig.2Response of above-ground (circles) and soil (triangles) organismal abundance to land-use type and intensity (from left to right within each land use: minimal, light, and intense use) compared to abundance in primary vegetation (baseline). Responses have been back-transformed. For this plot, other fixed effects are set at their median values. Error bars show 95% confidence intervals

Fig. 3

 3 Fig.3The (back-transformed) response of abundance to soil properties for five land uses for soil biodiversity (left) and above-ground biodiversity (right), with median values for other fixed effects. Shading spans ± 0.5 standard errors, and rugs along the x axes show the values of the explanatory variables represented in the data set used for modelling

Table 1

 1 Summary of soil biodiversity and above-ground biodiversity data included in this analysis

		Above-ground	Soil
	Sources	412	101
	Studies	498	122
	Sites	20,178	7515
	Countries	88	37
	Biomes	14	13
	Total taxa	55,443	13,056
	Vascular plants	19,166	0
	Bryophytes	1454	0
	Fungi and Mycetozoa	1464	479
	Vertebrates	9704	3
	Annelids	5	401
	Arthropods	23,194	11,606
	Other invertebrates	5	6
	Molluscs	451	34
	Nematodes	0	527
	Sources typically represent a single paper with each source containing one or
	more Studies, defined as data collected using the same sampling method. Sites
	are individual sampling points

Table 2

 2 Sites by land use and use intensity for soil biodiversity and above-ground biodiversity based on the description of the Source authors

	Land Use	Above-ground biodiversity		Soil biodiversity
		Minimal	Light	Intense	Minimal	Light	Intense
	Primary vegetation	4326	2153	491	826	395	121
	Secondary vegetation	2512	1364	502	655	341	236
	Plantation forest	552	1238	357	153	198	152
	Cropland	567	1081	1121	143	288	331
	Pasture	873	1185	327	726	1085	1146
	For more details on curation see Additional file 1: Tables S3, S4 and Hudson et al. [22]

Table 3

 3 Model comparison table for the three models used for hypothesis testing compared with the full model, for all taxa and invertebrate only subset

			All taxa			Invertebrates only
	Model	d.f.	AIC	log lik.	χ 2	AIC	log lik.	χ 2
	Full model Full model minus UI Full model minus LUI × habitat layer interaction (hypothesis 1) Full model minus soil property × land use interactions (hypothesis 2) 32 73 53 30 Full model minus soil property × land use × habitat layer interactions (hypothesis 3) 20	-12949.60 -13244 -13284.10 -13121.93 -13262.79	6547.80 6675.3 6685.05 6601.96 6684.40	145.35 125.78 291.96 127.10	-9616.36 -9615.97 -9896.90 -9841.82 -9931.08	4881.18 4860.99 4991.45 4961.91 5018.54	171.06 139.49 198.58 85.31
	All results were significant at p < 0.001

Acknowledgements

This is a contribution from the Imperial College Grand Challenges in Ecosystems and the Environment Initiative. We thank the following who either contributed or collated data: Dr Andrew D. Barnes, Dr David Bogyó, Professor Céline Boutin, Joanna Zawadzka, Ilona Leighton-Goodall, Keiron Brown and the Earthworm Society of Britain. This study is part of the PREDICTS project, which is endorsed by the GEO BON.

Funding This work was supported by Natural Environment Research Council (Grants NE/L002515/1 and NE/M014533/1) and through Excalibur which received funding through the European Union's Horizon 2020 research and innovation programme under Grant agreement No 817946.

Supplementary Information

The online version contains supplementary material available at https:// doi. org/ 10. 1186/ s12862-022-02089-4.

Additional file 1. Contains Tables S1-S4 and

Availability of data and materials

The datasets generated and/or analysed during the current study are available in The Natural History Museum Data Portal, https://doi.org/10.5519/zall06xc.

Declarations

Ethics approval and consent to participate Not applicable.

Consent for publication

Not applicable.

Competing interests

The authors declare that they have no competing interests.

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.


C-T Soulard

Mousselin G 12

Napoleone C 13

J C Paoli

Peri-urban Agroecosystems in the Mediterranean: diversity, dynamics and drivers

Keywords:

To address sustainability challenges of agro-ecosystems located in Mediterranean urban regions, this paper focuses on the multidisciplinary subject of urban agricultural systems. To better understand the diversity and dynamics of peri-urban agro-ecosystems and the main drivers of their sustainability, we compare six case-studies located in Southern Europe (Montpellier, France; Pisa, Italy; Lisbon, Portugal; Athens, Greece) and the Maghreb (Constantine, Algeria; Meknes, Morocco). The research is based on fieldwork in each urban region (qualitative analysis) and literature analysis aimed to position each case study in its national and Mediterranean contexts. The comparison between local contexts indicates large discrepancies in the integration of environmental focus among the respective urban planning objectives. Generally, urbanization tends to accentuate agricultural diversity. The different forms of peri-urban agriculture evolve despite their persistent decline, and they also show a capacity to resist, and even new growth in response to urban demand.

Introduction

The Mediterranean region is one of the areas in the world most exposed to the combined effects of urban growth and climate change. The Mediterranean region covers roughly 854 million ha, but only 118 million (14 per cent) are suitable for agricultural production (Zdruli 2012). The population is expected to continue increasing (from 446 million in 2000 to 570 million in 2025) and remain concentrated in cities and on coastlines. The peri-urban agro-ecosystems face major global issues. In order to address these threats over the long term, three challenges must be met: the conservation of ecosystem diversity, the scarcity of water resources, and food security.

Challenges for the peri-urban agro-ecosystems

The first challenge is the richness and vulnerability of Mediterranean ecosystems. According to [START_REF] Underwood | Threats and biodiversity in the mediterranean biome[END_REF], the Mediterranean biome is richer in terms of biodiversity than Africa and tropical Asia combined. However, this biodiversity is at risk. Urbanization threatens biodiversity, first through the 'artificialization' of land, and also through patches of urban development mixed with wildlands that fragment habitats and increase the risk of fire (Spyratos et al. 2006). A second challenge is the scarcity of water resources. According to Garcia-Ruiz et al. (2011), the overexploitation of water in plains and valleys comes as a result of (1) urbanization (including tourism and industry) and (2) intense agriculture through irrigation. These factors act in concert with the reduced water storage capacity of rural areas, plateaus and highlands, resulting from agricultural abandonment (erosion, landslides) and climatic change (reduced rainfall and snowmelt consecutive to warming). The third challenge is food security. Agricultural areas of the Mediterranean have always needed to engage in trade for food. According to [START_REF] Turmo | Chapter 5. The Mediterranean Diet: consumption, cuisine and food habits[END_REF], the Mediterranean diet derives from trade among agricultural areas of the basin. However, population growth has increased food dependency. According to [START_REF] Agrimonde | Urban Agriculture. Social inclusion and Sustainable City. Case Study of two municipal gardens in Northern Greece[END_REF], the Mediterranean is and will be the region that is most dependent on imports for food. Therefore, the issue of food security arises at the level of trade between Europe and the Southern Mediterranean shore, but also between the Mediterranean and other exporting countries [START_REF] Hervieu | Les dynamiques agricoles en Méditerranée[END_REF]. Local and regional exchanges will play a key role as interfaces of social and environmental sustainability.

Agriculture represents divergent interests in the analysis of environmental and food issues: providing ecosystem services and food, yet generating threats to resources. The apparent contradictions in these issues suggest the need to adopt a systemic approach. Conserving natural resources during production, ensuring food security, allowing the supply and marketing of agricultural products, and elaborating strategies for developing rural and urban territories, are all objectives that should be part of the search for sustainable solutions (MediTerra 2008). In this Mediterranean context, urban and peri-urban agriculture can be viewed as one means for agricultural development to make more efficient use of land. The scarcity of arable land, water, and the fragility of cultivated ecosystems hinder the development of agriculture in the Mediterranean (Ben [START_REF] Ali | Politiques urbaines, terres agricoles et marché foncier : quel avenir pour l'agriculture périurbaine à Constantine (Algérie) ?[END_REF]Nasr et Padilla 2004). This explains the focus of the literature on one hand on agricultural lands facing urbanization (Jarrige et al. 2003;Elloumi et al. 2011;[START_REF] Perrin | Un littoral sans nature ? L'avenir de la Méditerranée face à l'urbanisation[END_REF], and on the other hand on the internal contradictions of Mediterranean agricultures, where both productivist and non-productivist intertwined trends (Ortiz-Miranda et al. 2013). In contrast, research works on the diversity of peri-urban agro-ecosystems and their development in the Mediterranean remain sporadic.

The Mediterranean agro-ecosystems in the urban and peri-urban areas

Urban agriculture still exists. Nasr and Padilla (2004) have shown that its presence in Mediterranean cities is historical. It has appeared in various forms that remain an integral part of society: gardens, huertas, oases. However, it has declined sharply with agricultural modernization and urban development. At the cities' periphery, urban expansion absorbs agricultural and natural terrains. The peri-urban agricultural that was once rural and primarily oriented towards national markets and exportation is now found within the jurisdiction of urban policies.

Some local experiments on the conservation of threatened urban agriculture have been studied: the Huerta of Valencia and the agrarian park Baix Llobregat in Barcelona [START_REF] Paül | Peri-urban farmland conservation and development of alternative food networks: Insights from a case-study area in metropolitan Barcelona (Catalonia, Spain)[END_REF], the peri-urban agricultural parks in Italy and Spain [START_REF] Giacché | vers un outil de projet et de ricoles en Italie et en Espagne L'expérience des parcs ag gouvernance de l'agriculture en zone périurbaine 30[END_REF], the plain of Mitidja and the Setif region in Algeria [START_REF] Imache | La Mitidja 20 ans après : réalités agricoles aux portes d'Alger. Alpha, Alger Jarrige F, Jouve AM Napoleone C[END_REF][START_REF] Boudjenouia | L'agriculture périurbaine à Sétif (Algérie) : quel avenir face à la croissance urbaine ?[END_REF], the Soukra plain in Tunis [START_REF] Bouraoui | Quelles perspectives pour les espaces agricoles dans les projets de valorisation touristique du littoral tunisien? Le cas de la plaine de Soukra dans le Grand Tunis. In Perrin C (ed) Un littoral sans nature ? L'avenir de la Méditerranée face à l'urbanisation[END_REF], the urban agriculture in Casablanca [START_REF] Kasper | Urban Agriculture Casablanca[END_REF]. These works investigate local initiatives that seek to enhance the economic, social, and environmental value of urban and peri-urban agro-ecosystems. The studies tend to be focused on symbolic locations, and have little relationship with each other. Some recent publications have compiled summaries of the agricultural dynamics in urban regions, showing the key role of urban agriculture in the food security of southern Mediterranean cities [START_REF] De Bon | Sustainable urban agriculture in developing countries. A review[END_REF][START_REF] Hamilton | Give peas of chance. Urban agriculture in developing countries: a review Agron[END_REF], or analysing agriculture's positive and negative contributions to the self-sufficiency of cities in developed countries [START_REF] Mok | Strawberry fields forever? Urban agriculture in developed countries: a review[END_REF]. However, recent comparative work on the Mediterranean region is almost non-existent, even though the region offers a particularly interesting perspective with its amalgamation of Northern and Southern countries with contrasting socio-economic profiles but quite similar problems of urban expansion, agriculture and the environment.

The object of our paper is to compare the relationships between urban systems and agricultural systems in some cities of the Mediterranean: Are there contrasts between Northern and Southern cities? Do we confirm the differences reported in the literature between developed and developing countries? Are the differences between local contexts stronger? Are there some specific issues due to the Mediterranean context? In order to give some responses to these questions, we will compare six peri-urban agro-ecosystems in the Mediterranean region, and analyse their diversity and evolutionary dynamics, through an agricultural-urban systemic approach.

Method

The methodological challenge of our work is to better understand the relationships between urban systems and agricultural systems by looking beyond the 'rural-urban divide' separating urban perspectives from agricultural perspectives, and examining the interactions between these systems. We used this systemic approach in the comparison of six urban regions on the northern and southern banks of the Mediterranean [START_REF] Valette | Sustainable cities vs sustainable agricultures. A scientific project on agricultural-urban systems in the Mediterranean[END_REF]. In each case study, we described agricultural-urban dynamics at three levels: farms, local community projects, urban region. Sustainability was assessed at each level through global and local challenges, drivers, and actors that foster (or not) the links between cities and agriculture. To do this, we analysed urban sprawl, peri-urban farmland use, adaptation of farming systems, natural resources management, public policies, actors' strategies and territorial governance. This comparative approach [START_REF] Perrin | Pour une approche constructiviste de la comparaison internationale. L'expérience d'un projet de recherche interdisciplinaire sur l'agriculture urbaine en Méditerranée[END_REF] shows how local issues of urban and peri-urban agroecosystems reflect the ways in which global trends (on land, climate or political issues) impact specific agroecosystems throughout the Mediterranean region. It also highlights how local initiatives and policies actually deal with these global trends.

We compare six case studies. In each, we use two elements to characterize the urban agricultural system: the diversity in agro-ecosystems and the dynamics of evolution in the city-agriculture relationship. The case studies were conducted in six countries from the northern and southern Mediterranean regions, located in the west and centre of the basin (Table 1). The cities involved have all been subject to sustained population growth and the dynamics of urban spread, both compact as in the Maghreb and more diffused as in Southern Europe. Although the case studies cannot pretend to represent the totality of Mediterranean contexts, they do present different types of relationships between cities and agriculture: (1) separation and competition dominate the these relationships in Maghreb, in Constantine (Algeria) and Meknes (Morocco); (2) the relationships in the two biggest cities, Athens (Greece) and Lisbon (Portugal), are equally scarce but demonstrate a resurgence following the economic crisis experienced by the countries of southern Europe; (3) Montpellier, (France) and Pisa (Italy), which are middle size cities, are characterized by a city-agriculture relationship at the heart of public policies promoting sustainable development.

Constantine, Algeria

Constantine is marked with a long history of specialization in cereal production, political upheavals creating insecurity in access to land for farmers, and national urban policies dominated by housing and construction objectives. The economic viability of local agricultural systems depends on markets found outside of the city, in Algeria or internationally.

Periurban agriculture is dominated by cereal production

There is limited diversity among the agro-ecosystems surrounding Constantine (Fig. 1,a). The land, flat and fed by winter rains, is well adapted to cereal cultivation. To the north of the city, a huerta was developed on an upwelling of water at Hamma Bouziane, the historic garden of Constantine. There are also extensive forest zones of Aleppo pine, eucalyptus, oak, and cork oak. Traditional agriculture was historically characterized by social inequality and a system of tenant farming on the land. But after the country's independence in the 1970s, the government's socialist policies led to large collective farms on nationalized lands of European colonists and Algerian land-holders, or on public lands. By the end of the 1980s and during the 1990s, the failure of socialist policies lead to the restitution of land to the original Algerian owners or the reorganization of socialist farms into a different style of collective (Exploitations Agricoles en Commun) or individual activity (Exploitations Agricoles Individuelles). The irrigated land of small traditional peri-urban agriculture of Constantine (market farms and fruit trees) has been largely overtaken by development, and today, the cultivation of cereal alternated with fallowing is the predominant system of agriculture. Any diversification towards fruit trees and market farming is limited to irrigated areas around the ancient Hama Bouziane gardens. The province of Constantine holds 5,941 farms of which only 492 (8%) are irrigated. Beyond the uncertainty of available land generated by urban growth, the agricultural sector is weakened by the naturally poor soil, adverse weather conditions, and a lack of water resources.

The agricultural terrains remain a reserve for planned urban expansion

As seen throughout Algeria, the focus is on clearing constructible land to absorb the considerable urban growth that has occurred for the last 40 years. Urban planning is conceived as identifying land to reserve for habitation, commercial development and infrastructure. Agriculture is not part of the formula for peri-urban space. As a result, farmers in the area are constantly concerned about the vulnerable access to land. Beyond the typical coexisting property markets with different price structures (agricultural versus urban) that favour urban development on agricultural land, the national housing policy prescribes low prices for the transfer of State lands (usually agricultural) with the specific intent of supporting construction efforts. This policy has increased development pressure on public land and resulted in the integration of large tracts of agricultural land into the urban perimeter. In the most recent urban plan, 1,676 ha of land previously designated as agricultural (part of a grouping of 2,099 ha of public and private land in the area of Constantine) were designated for urban development.

Few projects integrate rural and urban systems

There are, however, some farms geared towards diversification: arboriculture and market gardening in the irrigated zones (ancient Hamma Bouziane gardens), dry arboriculture, legumes (in crop rotation rather than fallowing), and a few instances of poultry and dairy farming. This diversification is not significantly linked to the city itself and suffers from the uncertain access to land and a lack of capital investment. Our research (Bendjaballah et al. 2013) shows that diversification appears to be more prevalent among the larger farms in the areas of Hamma Bouziane and Aïn Smara. Small producers are interested in diversifying but generally don't have the capital to make the investments necessary. Any attempts at diversification are even more difficult when the farmer does not own the land.

Meknes, Morocco

The province of Meknes is located in the centre of the Saïs plain, one of the most fertile areas in Morocco, and Meknes owes its reputation to the prosperous, surrounding agriculture. In 2011, there were approximately 36,285 ha of agricultural land in the urban and peri-urban area of Meknes and its adjacent municipalities [START_REF] Valette | Urbanisation en périphérie de Meknès (Maroc) et devenir des terres agricoles : l'exemple de la coopérative agraire Naïji[END_REF], including around 1,800 ha within the urban perimeter. In 2004, the total surface was estimated at 31,900 ha, of which 10% was irrigated.

There is a gap between urban and peri-urban agriculture

Intra-urban agriculture occupies three valleys (non-constructible) holding very small farms (between 75 a and 3 ha) with limited production in market gardening and arboriculture, and a few head of cattle or sheep (Fig. 1,a). The farms are irrigated with water from the wadi and with city waste water (which affects the sanitary quality of the products). By contrast, the peri-urban zone encompasses vast, mechanised and well irrigated farms. These farms are primarily producers of winter cereals (77% of all cultivation), market farming (13.2%), and arboriculture (27,7%), intensified with irrigation and inputs, including a growing presence of olive production. These peri-urban examples of highly productive agriculture are the target of the Moroccan national plan supporting agriculture (Plan Maroc Vert) which aims to transform Moroccan agriculture into mechanised production for export.

Public action threatens agriculture

In spite of national programs, the major threat to the sustainability of urban and peri-urban agriculture is urbanization. In Meknes, there is a sharp contrast between (1) national agricultural policies addressing food security and water management issues at a national level, and (2) urban policies focusing on social housing and economic development. A remote sensing analysis of land changes in the Meknes region showed that 2.4% of the agricultural areas existing in 2001 became urbanized by 2011 and 6.1% was transformed into bare soil, which can be considered as a first step towards urbanization. Despite a history of compact urban growth, land speculation is extending the perimeter of the city of Meknes faster than required by the increase in population. This urbanization and its impact on farmland is directly influenced by local and national public policies. In the early 1990s a trend emerged in Morocco advocating the privatization of state, collective, and guich (religious orders) landholdings, as one of the best incentives to encourage farmers to initiate improvements. This perspective leads to the main levée, a law endorsed in 2005 that allows a cooperative's beneficiaries to become private owners of their agricultural land. However, most farmers refused to invest and either sold their land at very attractive prices or modified their farming practices (annual crops, fallowing) in a strategy of land speculation. Prior to privatization, there were 32 cooperatives in the Meknes region covering a total surface of approximately 15,000 ha with a UAA (used agricultural area) of 14,000 ha. Since being distributed among 1,119 assignees, at least 3 of the cooperatives located closest to the city fringe have almost completely disappeared (as of 2014), and approximately 60% of the remaining cooperative land has been sold [START_REF] Valette | Urbanisation en périphérie de Meknès (Maroc) et devenir des terres agricoles : l'exemple de la coopérative agraire Naïji[END_REF].

The few agricultural urban projects are likely not to be implemented

The hard truth remains that very few projects have been well designed to develop the synergy between agriculture and the city. Two emblematic examples stress the divergent issues of agriculture and urbanization that we have observed in this case study. First, the landscape plan for the Oued Boufekrane valley, designed by the local urban agency in 2008 attempts to integrate agriculture into the urban system as one of the structural elements enhancing multifunctionality (conserving urban green space, and food production). This plan sets aside 25% of the project's surface for market gardening, but it doesn't specify the source of farmers or the mechanism for supporting them. In the real world application, there appears to be very little political will to see this project succeed, even now, seven years after it was conceived. A more informal project introduced as intra-urban CSA (Community supported agriculture) currently led by a local association claims to promote and support synergies between intra-urban agriculture and the urban population. A closer examination suggests that rather than developing a genuine agricultural-urban initiative, the project's main objective is to establish roads, a water supply and electrical service in the valley in order to make it attractive to investors and more suited to welcome urban activities such as restaurants and playgrounds.

In the Messoghia plain, urban sprawl continues

In the late 1990s, these phenomena were more exacerbated in East Attiki, and especially the Messoghia plain (38.900 ha belonging to 11 Municipalities). The construction of mega-projects in relation to the 2004 Olympic Games in Athens (including the new airport and peripheral highways) triggered counter-urbanisation phenomena causing a population shift from the inner city to peri-urban spaces, and encouraged the transformation of littoral residences from seasonal to permanent, further shrinking farmland and degrading the natural environment (Nikolaidou 2011). Between 1996 and 2006 the population on the plain of Messoghia increased by 42% and the surface of agricultural land was reduced by 36%. In particular the emblematic vineyard (the famous "Retsina wine of Attiki"-traditional appellation) decreased by 52%, especially in the expanded new airport area (land expropriation to establish major infrastructures).

The economic crisis showed that another paradigm based on localised agri-food systems is possible

The outbreak of the public debt crisis ( 2009) and collapse of the real estate market has dampened the frenzied urban development in the peri-urban region of Athens. The economic crises also led to a broader questioning of the urban consumerist pattern and living conditions. However, the public debt crisis contributed to the relaxation of the national urban development plan (including legislation on specific building conditions on coastal, protected natural areas, agricultural land) in an effort to attract international investors through privatization or concession of public land. The self-managed urban farm of "Agros in Ellinikon" is an emblematic grassroots movement conceived in metropolitan Athens (2011) to combat the large scale fast track privatisation of public land (620 ha, former international airport). The farm (2,600 m2, organic, traditional seeds, vegetables and olive grove) which focuses on food production for educational and social purposes (Anthopoulou 2013), was originally planned to become a high green Metropolitan Park. Municipal allotment gardens are the most widespread and popular form of urban agriculture in Greece. They first emerged in 2011 as a spontaneous initiative of municipalities developing social policy schemes to tackle the poverty and depression of urban dwellers affected by the economic crisis and severe austerity measures. There are approximately 25 small-scale gardens in the metropolitan Athens area. They are primarily oriented towards vulnerable social groups with the intention of easing family food expenses and enhancing social solidarity in neighbourhoods (Anthopoulou 2013). All of these civic and institutional initiatives confirm the social need for food re-localisation and reconnecting with agricultural land. The economic crisis highlighted problems in the post-war urban development model in Greece and the absence of an agricultural-urban perspective in spatial planning. It showed that another paradigm based on localised agri-food systems in peri-urban areas is possible.

Lisbon, Portugal

In the Lisbon Metropolitan Region (LMR), one of the most fertile regions of the country, a highly professionalised agriculture co-exists with small-scale subsistence agriculture, giving the landscape a somewhat rural quality through the juxtaposition of agricultural and urban spaces, be it within city limits, in its outskirts or in peri-urban spaces. Urban expansion and sprawl have not been pervasive enough for this type of traditional agriculture to disappear [START_REF] Abrantes | Lezíria do Tejo : agriculture et étalement urbain aux marges métropolitaines de Lisbonne[END_REF]. In fact the rural exodus during the 1960s and later in the 1980s, the return of Portuguese nationals from the former African colonies, as well as the economic crisis since 2009 were key elements keeping and boosting agricultural practices and the tradition of farming within the city and it surroundings [START_REF] Luiz | Hortas urbanas cultivadas por populações caboverdianas na área metropolitana de lisboa: entre a produção de alimentos e as sociabilidades no espaço urbano não legal[END_REF].

The crisis has given rise to new types of small-scale subsistence agriculture

During interviews made throughout the LMR, we identified three types of subsistence agriculture related to the type of farmer and the land tenure: (1) Traditional subsistence agriculture that is practiced on farms or on private plots waiting for construction. This is practiced by farmers and by landowners as a complement to employment or income (Fig. 1,b). According to INE data ( 2009), this type of agriculture within the LMR accounts for 7% of the national utilised agricultural area dedicated to family farming. (2) Subsistence agriculture called "unplanned" [START_REF] Luiz | Hortas urbanas cultivadas por populações caboverdianas na área metropolitana de lisboa: entre a produção de alimentos e as sociabilidades no espaço urbano não legal[END_REF], is carried out on utility and restricted areas (e.g. near roads, transportation routes) and on vacant parcels, many of those areas without the knowledge of the property owner. This type of agriculture is usually associated with an elderly or unemployed population and can be found throughout the region but mostly in suburban municipalities. The municipality of Almada (a suburban area on the southern bank of the Tagus river) has 537 ha of agricultural terrain, 60 ha of which are dedicated to "unplanned" agriculture. (3) An agriculture that we have called "planned" (hortas urbanas), is practiced in community gardens, most of them were originally unplanned gardens that have been developed by the municipalities and replicated both in urban and peri-urban contexts. These municipal agricultural-urban projects keep expanding both in offer and demand. The population has diverse social-economical backgrounds, ranging from retirees and former agricultural or industrial workers to younger employees in the services sector. In the case of all three types, the production accounts for 80% to 100% of the food source of each family (3 to 5 family members on average); and in some cases surplus products are either exchanged or sold out.

Small-scale subsistence agriculture is progressively integrated into municipal master plans

The expansion of the hortas urbanas and its progressive integration into urban planning through instruments like the Municipal Ecological Structure (e.g. Lisbon and Almada masters plans) or the Metropolitan Ecological Network become a factor of permanence of these areas. These types of agricultural practices benefit from the sustainability dimensions that they can provide, their contribution to environmental issues such as the capability to create, regenerate and/or maintain green corridors, and their impact on socioeconomic issues such as income generation for the families. The uncertainty and fragility of traditional subsistence agriculture and the unplanned agriculture is related to their dependence on the variations of the real estate market on one side, and socialeconomic conditions on the other. However, the current trend of acquisition by the municipalities increases the chance that these unplanned agriculture spaces will be transformed into community gardens (e.g. 51 ha of the 60 ha of unplanned gardens will be integrated into the Almada community garden municipal network, thus representing almost 10% of the total farming area in the municipality). The current orientation of National public policies towards self-sufficiency and local food supply indicates a promising future for the sustainability of subsistence agriculture and for the strengthening of the relationship between city and agriculture at the scale of these urban regions.

Montpellier, France

The viticulture crisis leaves space for other agricultural dynamics

The Montpellier region has a long history of a wine grape monocrop, but there has been a recent trend in diversification of peri-urban agro-ecosystems. Vineyards still occupy the majority of peri-ubran agricultural terrains, however, the surface in grape production has decreased significantly since 1960, challenged by a succession of crises in wine production. More than half of the vineyards in the Hérault department were torn out between 1974 and 2010. This crisis is linked to a drop in the demand for table wines, but it has also been affected by the rapid expansion of the residential and service sectors of Montpellier. The population of the metropolitan region tripled in fifty years, from 145,000 inhabitants in 1960 to 432,000 in 2012. This demographic growth created a striking urban spread around the city of Montpellier and the surrounding villages. During the same period, declines in the wine industry left land available for other farming systems: horse farms and forage cultivation, market gardening and cereal crops. The spread of these agro-ecosystems in the context of intense pressure from urban expansion is based largely on spatial mobility: they use the land temporarily until urban expansion overtakes them.

Agricultural spaces and natural spaces enter the realm of urban planning

The relationship between the city and agriculture were also evolving during this period [START_REF] Perrin | L'espace et le temps des liens ville-agriculture : une présentation systémique du cas de Montpellier[END_REF]. Until 1960, the growth of Montpellier was linked to the expansion of the vineyard and wine economy. Then between 1960 and 2000, relations between the city and farming grew apart. But since then, the relationship between the two has been on the rise, and the city of Montpellier has come to tie high quality wines to its image. A list of community support for the industry bears witness to this relationship: a trail of wine and heritage, an annual festival of vineyards and wine, the promotion of wine and direct sales, the addition of a 'Grès de Montpellier' wine at official events. In 2006, the city adopted a metropolitan Master Plan which includes specific planning tools for farmland conservation and urban containment. In a complete about face, agricultural and natural spaces have become recognized as a framework of urbanization at the scale of the metropolitan region. These strict regulations have been incorporated into local urban planning of the peri-urban municipalities and have slowed the rate of urban expansion on agricultural terrains. Nevertheless, not even the strictest regulations favour the sustainability of an agricultural presence in the absence of existing agricultural projects.

Agriculture, nature and food favored the emergence of multiple urban agriculture initiatives

In recent years, many agricultural-urban initiatives have emerged. From a top down perspective, the city fosters new multifunctional farming systems in order to address two major issues: (1) environmental issues, such as natural hazards related to floods and fires, and (2) local food supply through short chains. Such issues are key drivers of the reconnection between cities and agricultural sustainability. These intentions are manifested by several agripark projects on agricultural terrains acquired by the city or the metropolitan region, with the objective of combining agricultural production, forest and environmental services (protection against natural risks) and recreation spaces for residents. The quality of life and the environment as well as food sources (farmers' market) is making peri-urban agriculture an issue in the small peri-urban municipalities. Livestock has been introduced to defend forest land from fire risks, and maintain grasses along river banks or in fields designated to hold flood waters. From a bottom up perspective, the demands of city residents for access to nature and gardening has resulted in a program initiated by the city in 2004 to create collective and shared gardens in the heart of urban space. The sustainability of this amateur urban agriculture rests on its occupation of the interstitial spaces between habitations and its social functions. The governance of these interactions between the city and agriculture is still under construction. An agricultural and food production policy was developed in 2014 which represents the first effort to link the different metropolitan services and the peri-urban municipalities to encourage a return to cultivation on fallow agricultural terrains, and promote agricultural production to supply the local restaurant industry and school catering.

Pisa, Italy

Urbanization has had a profound effect on peri-urban agriculture and on the competitiveness of Italian small-scale farming.

The number of periurban farms are diminishing, the remaining survive by diversifying

The urban region of Pisa (Tuscany, Italy) is composed of a coastal plain with cereal and industrial crops, livestock and vegetables, and hills exclusively planted in olive trees. The plain and the hills are connected by a complex hydrological system composed of two sub-systems: a reclaimed area and a bench terraced-based drainage area. [START_REF] Marraccini | Durabilité de l'agriculture dans les territoires périurbains méditerranéens: enjeux et projets agriurbains dans la région de Pise (Toscane, Italie)[END_REF] analyse a combination of stakeholder interviews and policy documents to identify issues for peri-urban agriculture in the region of Pisa. The most frequently encountered issues were the quantity and quality of water resources, food production and the protection of farmland against urbanization. Farmland protection is integrated into several institutional and planning documents, e.g. urban planning at the municipality and county levels [START_REF] Marraccini | Durabilité de l'agriculture dans les territoires périurbains méditerranéens: enjeux et projets agriurbains dans la région de Pise (Toscane, Italie)[END_REF], and has also been the object of regional legislation on the establishment of a land bank for the management of abandoned or unexploited agricultural areas. Despite the importance that policies accord to peri-urban agricultural land, the last agricultural census highlighted a steady decrease in the Usable Agricultural Area (UAA) (16% less) and the number of farms (71% less) in the urban region since the 1980s. This decrease affects more small and non-diversified farms, whereas larger and diversified farms are more adapted to the urban context (Fig. 1,c).

The hydrological network links plain, mountains and the city of Pisa

Water issues are quite complex and heterogeneous in the area. They are both localized (e.g. nutrient leaching within a lake basin, underground water salinization) and diffuse (e.g. flooding). Although these water issues are the most recognized issues related to peri-urban agriculture in the area, they are poorly integrated into territorial projects and when they are included, they relate exclusively to sectoral water policies (reclaimed area and protection against natural hazards) or European Union water regulation implementation (water plans and vulnerable area action plans) [START_REF] Marraccini | Durabilité de l'agriculture dans les territoires périurbains méditerranéens: enjeux et projets agriurbains dans la région de Pise (Toscane, Italie)[END_REF]. However, farmers and other land managers need to use different practices, at the individual and collective level. For example, to mitigate flooding risks farmers in the plain have specific tillage practices and manage drainage channels to let water flow, whereas olive growers in the hills need to conserve bench terraces and their drainage system. A land reclamation consortium is charged with ensuring proper water drainage within the whole system and requires farmers to maintain these practices locally.

Food issue links agriculture and the city

Food production for the city has been the subject of several territorial projects joining institutional and local stakeholders (e.g. road of the oil, local farmers markets, and local meat labels). These initiatives were unified under the umbrella of a provincial food plan [START_REF] Iacovo | La stratégie urbaine : il piano del cibo[END_REF] to provide local food and sustain local farms. In this context, we investigated the ability of peri-urban farms to feed the local population. [START_REF] Filippini | Assessing food production capacity of farms in peri-urban areas[END_REF] highlighted that the potential food capacity depends not only on the effective size and number of farms but also on the collective actions targeting a product. The analysis of the beef and lamb production from peri-urban farms and sold in the local food supply chain showed that most local beef production was sold locally under a local label, whereas most of the locally produced lamb, which is not labelled, was marketed through conventional food chains.

The relationships between agriculture and the city (agricultural-urban system) are defined by different issues (water, food production, and farmland protection in the case of the urban region of Pisa) which in turn are managed at different levels (farming systems and local policies) and target different elements of the agro-ecosystems.

Conclusion

Agro-ecosystems differ depending on the urban region. Around Athens, Montpellier and Constantine, the farming systems remaining are the ones which are the more adapted to the constraints in water and soil (grapes, olives, winter cereals). The urban regions endowed with better agronomic resources allow more diversification as found in Meknes (the Saïss plain), Lisbon (the Tejo valley) and Pisa (the Arno valley). But pressures from urban growth are evident in all these regions: the city encroaches on agricultural land, engendering changes in land use well beyond the limits of urban development. But the retreat of agriculture in face of this expansion is not the only phenomenon that characterises the dynamics of peri-urban agro-ecosystems.

Urbanization accentuates the diversity of agro-ecosystems.

Our observations indicate that urbanization heightens agricultural diversity. The disruptions and opportunities created by the pressures of urban growth encourage the development of hybrid agro-ecosystems that adapt to the specific urban conditions or conserve more classical forms. These conditions also support the evolution of multiple agricultural systems, some of which may be declining and others which show a capacity to resist or even expand in response to urban demands. These dynamics are perceptible in all six city regions, though in different proportions. In some cases we can identify the effects of agro-tourism or the promotion of regional products due to the urban proximity. These positive effects co-exist with the challenges to agro-ecosystems that struggle with varying success, or evolve towards more viable production strategies. Other 'alternative' agricultural systems have appeared along with production efforts taken up by urban and periurban farmers to serve the urban market. The transformations in Mediterranean agro-ecosystems are complex and merit further analyses, not only from the perspective of productivity and land use, but also in view of the advantages of developing the relationship of exchange between urban and agricultural systems.

Our comparison calls attention to the importance of the national contexts for three large types of regional agricultural-urban system. Firstly the urban regions of Constantine and Meknes exhibit a divide between the city and agriculture, leading to segregated sectoral policies and urban policies which ignore the problems of remaining urban agriculture and treat peri-urban farmlands as a reserve of land for urban expansion. Without local support, the peri-urban agro-ecosystems are weakened by urbanization. Secondly by contrast, the urban regions of Southern Europe have witnessed a renewal of the links between urban development and agriculture. The urban regions surrounding Athens and Lisbon have experienced this renewal in response to the economic crisis. The fall in property values slowed construction and the growing poverty encouraged the development of subsistence forms of agriculture and food initiatives. Thirdly, the mobilization of urban actors has influenced the regions around Montpellier and Pisa, regions less affected by the urban economic crisis, but benefitting from local projects established to address agricultural, food, and environmental issues. These urban demands stimulate the development of diverse agro-ecosystems: urban or rural, professional or amateur, oriented towards food or social issues. The 'rural-urban divide', the resurgence of urban agriculture in times of crisis, and new projects linking agriculture, food and environment, all provide research avenues that should be further explored to reinforce the typology of these contexts and identify Mediterranean specificities.

Global and local drivers: What are the peri-urban agro-ecosystems of tomorrow?

The future of peri-urban agro-ecosystems depends on evolving factors, both globally and locally.

On a global scale, the divergent or convergent trajectories of agricultural policies and urban policies are powerful levers controlling the evolution (or disruption) of peri-urban agro-ecosystems. Neither the support structure of the organisation for national industry and export in the Maghreb, nor the Common Agricultural Policy (CAP) in Europe, offer particular support for peri-urban agro-ecosystems: the agricultural dynamics vary as much whether a function of production networks or that of urbanisation dynamics. But the development priorities of urban policies in the Maghreb are very different than those in Europe, where they promote (recently) the value of agricultural and natural spaces in urban regions. Finally, the question of climate change is one that is just beginning to be addressed in the support directives of local policies (e.g. the recent local climate and energy plans in France). The future research on the ability of Mediterranean farming systems to adapt to climate change (Inglesias et al. 2013) should be applied to peri-urban agro-ecosystems.

On the local scale, the comparison allows us to identify other factors controlling the evolution of urban agroecosystems. First, environmental issues are major factors in the fate of urban and peri-urban agro-ecosystems. Water stands out as an important object at the interface between the city and agriculture, whether it is a question of managing the quality of the water resource or the quantity of that resource. This question includes the likelihood of increasing periods of drought as well as those of flooding and the related human and material losses (landslides). Fire risk is also an issue at this interface, justifying the preservation of open space around habitations, or the reintroduction of pasturing livestock. The issue of biodiversity can also be a source of local mobilisation, much as seen in the Metropolitan Ecological Network of Lisbon where the project came about as a response to the explosion in demand for gardens, and will serve as support for an urban agriculture strategy. Second, the social movements act as another factor promoting evolution. In Southern Europe, they emerge as new forms of community driven agriculture, and involve a diverse public: the urban poor, the affluent, investors in rural land, etc. Even in the Maghreb, the possibilities for such an evolution are plausible, given recent urban agriculture initiatives developed in Casablanca, Rabat and elsewhere. Finally, local policies represent a third factor influencing the evolution. When policies are developed on a city-region scale as in Pisa or Montpellier, the recognition of agro-ecosystem specificities allows these policies to simultaneously address urban issues (food security), agriculture issues (opportunities for local farmers) and environmental issues (risk management). Placing these issues at the heart of integrated policies emerges as a challenge.

In conclusion, ten years after a beginning overview of peri-urban agriculture in the Mediterranean (Nasr & Padilla 2004), the resurgence of these peri-urban agro-ecosystems is driven by a transition towards urban policies which include agriculture and food issues. This transition must take place on large scales of space and time. As underlined by [START_REF] Braudel | La Méditerranée, les hommes et l'héritage[END_REF], Mediterranean cities were built on constant exchanges with their rural hinterlands, and trade with the countries of Europe and Africa. Being able to renew and reinvent these exchanges in the current context of competing resources and threats of climate change is a challenge for the future.

Fig. 1

 1 Fig. 1 Periurban agroecosystems in Meknès/Constantine (a), Lisbonne (b), Pisa (c)

Table 1

 1 Six case studies

	Case study	Constantine	Meknès	Athens	Lisbon	Montpellier	Pisa
		(Algeria)	(Marocco)	(Greece)	(Portugal)	(France)	(Italy)
	Study area
	Area	City region	Urban	Metropolitan	Lisbon	Montpellier	Urban region
	(local name)	(wilaya)	development	Athens area	Metropolitan	metropolitan	(Unione dei Comuni
			plan (SDAU)		region (RML)	(MMM)	Area Pisana)
			boundaries
	Population	938 400	599 555	3 737 750	3 436 948	434 100	200 000
		(wilaya)		(2011)	(INE, 2011)
	Surface, km2	2297	633	42	9 497	423	500
	(density, inhab/km2)	(408)	(947)	(8700)	(362)	(356)	(400)
	Growth (10 last years)	2,2%	21,3%	1,3%	5,35%	13,8%	3.5%
	Ecosystems
	Geography	Plateaus,	Plateau	Coastal plain	Alluvial plain,	Coastal plain	Alluvial plain, Hills
		hills and			coastal plain, hills
		plains
	Water resource	Low	Irrigation and	Limited irrigation	River, aquifers,	River, irrigation	River, reclaimed area,
			rain		irrigation		coastal lake
	Biodiversity interest	Shrubland,	Olive trees!	coastal wetlands-	Forest (and	Mattoral, Wetlands	Coastal Forest,
		Aleppo pine		Natura 2000	corktrees),		Wetlands, 3 Natura
				coniferous forests	Wetlands		2000 areas, a Regional
				shrublands			Natural Park
				natural pastures
	Natural hazards	Flooding,	Drought,	Fire	Flooding, Fire,	Flooding, Fire	Flooding, Landslide
		erosion, high	flooding, fire		erosion, streams
		temperature			and aquifers
					pollution
	Agricultures
	Main periurban	Cereals	Vegetables	Vine	Rice, Vine, Fruits	Vine	Cereals
	productions		Cereals	Olive trees	and Vegetables,	Cereals	Industrial crops
			Orchards	Shrublands	Cork, Olive trees	Shrublands,	Livestock (cattle, sheep)
	Types of farms	Specialized	Small and	Small scale farms	Specialized	Specialized farms	Small and large scale
	(average farm size)	farms (dry	large scale	(vine), Part-time	farms, small scale	(vine)	farming, Pluriactivity (14
		farming)	farms	farmers	farms		ha)

Acknowledgments

The authors acknowledge the French National Research Agency (ANR) funding via the DAUME project n°ANR-2010-STRA-007. They thank all the members of the DAUME project, Ben Boswell for English language revision and the reviewers for their valuable advices.