Tjeerd J Bouma
email: t.bouma@nioo.knaw.nl

Sergej Olenin

Karsten T J Reise

Tom Ysebaert

Ysebaert

Ecosystem engineering and biodiversity in coastal sediments: posing hypotheses

Keywords: Ecosystem engineering, Biodiversity, Invasive species, Bioturbation, Endobenthos, Epibenthos, Introduced species, Soft bottom, Facilitation, Inhibition, Species interactions

Coastal sediments in sheltered temperate locations are strongly modiWed by ecosystem engineering species such as marsh plants, seagrass, and algae as well as by epibenthic and endobenthic invertebrates. These ecosystem engineers are shaping the coastal sea and landscape, control particulate and dissolved material Xuxes between the land and sea, and between the benthos and the passing water or air. Above all, habitat engineering exerts facilitating and inhibiting eVects on biodiversity. Despite a strongly growing interest in the functional role of ecosystem engineering over the recent years, compared to food web analyses, the conceptual understanding of engineering-mediated species interactions is still in its infancy. In the present paper, we provide a concise overview on current insights and propose two hypotheses on the general mechanisms by which ecosystem engineering may aVect biodiversity in coastal sediments. We hypothesise that autogenic and allogenic ecosystem engineers have inverse eVects on epibenthic and endobenthic biodiversity in coastal sediments. The primarily autogenic structures of the epibenthos achieve high diversity at the expense of endobenthos, whilst allogenic sediment reworking by infauna may facilitate other infauna and inhibits epibenthos. On a larger scale, these antagonistic processes generate patchiness and habitat diversity. Due to such interaction, anthropogenic inXuences can strongly modify the engineering community by removing autogenic ecosystem engineers through coastal engineering or bottom trawling. Another source of anthropogenic inXuences comes from introducing invasive engineers, from which the impact is often hard to predict. We hypothesise that the local biodiversity eVects of invasive ecosystem engineers will depend on the engineering strength of the invasive species, with engineering strength deWned as the number of habitats it can invade and the extent of modiWcation. At a larger scale of an entire shore, biodiversity need not be decreased by invasive engineers and may even increase. On a global scale, invasive engineers may cause shore biota to converge, especially visually due to the presence of epibenthic structures.

Introduction

Understanding biodiversity, for a long time, has been recognised as a highly important issue in ecological research which continues to receive a lot of attention 123 (e.g. >150 publications in Nature and Science over the last 3 years; ISI web of knowledge). One important aspect of these studies is aimed at unravelling the role of single species that are capable to mediate the environment for the entire biological community. Already, at the dawning of modern ecology, the term "EdiWcator" (Latin: aediWcatorconstructor, builder) was introduced to indicate a plant species which plays the crucial role in structuring the environment and providing niches for associated and dependant organisms [START_REF] Braun-Blanquet | Role of two contrasting ecosystem engineers (Zostera noltii and Cymodocea nodosa) in the food intake rate of Cerastoderma edule[END_REF]. Originating in PXanzensoziologie (phytocenology or plant ecology), this concept was widened to include also "ediWcating" animal species and in 1930s-1950s it was also applied in hydrobiological studies [START_REF] Reimers | Glossary on nature management terms[END_REF], mainly in German and Russian literature. This term is closely related to the more recently introduced concept of ecosystem engineers, which is used to describe organisms causing a biologically mediated habitat modiWcation [START_REF] Jones | Organisms as ecosystem engineers[END_REF]. In recent years, the notion of ecosystem engineers has been recognised as a highly relevant concept (with over 840 citations to date), with large consequences for neighbouring organisms and local biodiversity in a broad range of ecosystems (e.g. see [START_REF] Bruno | Inclusion of facilitation into ecological theory[END_REF][START_REF] Crooks | Characterizing ecosystem-level consequences of biological invasions: the role of ecosystem engineers[END_REF]Wright and Jones 2006;Wright et al. 2006). [START_REF] Jones | Organisms as ecosystem engineers[END_REF][START_REF] Jones | Positive and negative eVects of organisms as physical ecosystem engineers[END_REF] distinguished two types of ecosystem engineering. In autogenic engineering, the organisms change the environment via their own physical structures and are thus part of the engineered habitat (e.g. trees in a forest), whereas in allogenic engineering, organisms transform living or non-living materials from one physical state to another (e.g. dam creation by beavers).

Ecosystem engineers tend to be most dominant in stressful environments [START_REF] Jones | Positive and negative eVects of organisms as physical ecosystem engineers[END_REF]) and consequently, autogenic and allogenic ecosystem engineers can have a striking presence in many coastal sediments (Fig. 1). Benthic ecosystem engineers inhabiting coastal sediments can cause a multitude of biogenic habitat transformations such as sediment stabilisation and destabilisation or bioconstructions and bioturbations [START_REF] Reise | Sediment mediated species interactions in coastal waters[END_REF][START_REF] Widdows | Impact of biotic and abiotic processes on sediment dynamics and the consequences to the structure and functioning of the intertidal zone[END_REF]. In general, benthic engineers can be divided into epibenthic and endobenthic organisms depending on whether they spend most of their lifetime above or below the sediment, respectively. Many endobenthic macroinvertebrate species modify the sedimentary habitat through their activities and can be considered allogenic ecosystem engineers. Endobenthic bottom dwelling species aVects a number of resource Xows mainly through bioturbation and bioirrigation [START_REF] Rhoads | Organism-sediment relations on the muddy sea Xoor[END_REF][START_REF] Cadée | Sediment dynamics by bioturbating organisms[END_REF][START_REF] Reise | Sediment mediated species interactions in coastal waters[END_REF]. Bioturbation is a biological mixing process that alters both the physical structure and the biogeochemical nature of the sediment, by increasing exchange Xuxes at the sedimentwater interface. Bioirrigation is the active Xushing of burrows (and its surrounding sediment) with overlying waters, thereby enhancing the exchange rates between sediment and water column. The combination of bioturbation and bioirrigation can strongly shape the environment and strongly aVect ecosystem functioning [START_REF] Meysman | Bioturbation: a fresh look at Darwin's last idea[END_REF]. Well-known examples of endobenthic ecosystem engineers are, e.g., lugworms Arenicola marina (Volkenborn et al. 2007a; Fig. 1), burrowing ghost shrimps Callianassa sp. [START_REF] Atkinson | Aspects of the physiology, biology and ecology of thalassinidean shrimps in relation to their burrow environment[END_REF] and mangrove crabs such as burrowing sesarmid (Grapsidae) and Wddler crabs (Ocypodidae) [START_REF] Kristensen | Mangrove crabs as ecosystem engineers: with emphasis on sediment processes[END_REF]. The most dominant epibenthic ecosystem engineers inhabiting temperate coastal sediments are reef building Wlter feeders or dense vegetations of seagrasses, macroalgae or salt marsh species (Fig. 1). By their epibenthic structure, these organisms aVect local hydrodynamics (e.g. for vegetations, see [START_REF] Ackerman | Reduced mixing in a marine macrophyte canopy[END_REF][START_REF] Bouma | Trade-oVs related to ecosystem-engineering: a case study on stiVness of emerging macrophytes[END_REF][START_REF] Koch | Water Xow in tide-and wave-dominated beds of the seagrass Thalassia testudinum[END_REF][START_REF] Koch | Fluid dynamics in seagrass ecology-from molecules to ecosystems[END_REF][START_REF] Peterson | Attenuation of water Xow inside seagrass canopies of diVering structure[END_REF]Peralta et al. 2008, and references therein; for reef building Wlter feeders, see [START_REF] Fréchette | Energy Xow between the pelagic and benthic zones: factors controlling particulate organic matter available to an intertidal mussel bed[END_REF][START_REF] Widdows | Use of annular Xumes to determine the inXuence of current velocity and bivalves on material Xux at the sediment-water interface[END_REF]Widdows et al. , 2002)), and thereby often aVect local sediment dynamics and particle trapping (e.g. for vegetations, see [START_REF] Koch | Beyond light: physical, geological, and geochemical parameters as possible submersed aquatic vegetation habitat requirements[END_REF][START_REF] Gacia | Sediment deposition and production in SE-Asia seagrass meadows[END_REF][START_REF] Castellanos | Nucleation and facilitation in saltmarsh succession: interactions between Spartina maritima and Arthrocnemum perenne[END_REF][START_REF] Hemminga | Biomass production in pioneer Spartina anglica patches: evidence for the importance of seston particle deposition[END_REF][START_REF] Van Hulzen | Morphological variation and habitat modiWcation are strongly correlated for the autogenic ecosystem engineer Spartina anglica (common cordgrass)[END_REF]; for reef building Wlter feeders, see [START_REF] Widdows | Use of annular Xumes to determine the inXuence of current velocity and bivalves on material Xux at the sediment-water interface[END_REF]Widdows et al. , 2002)). These epibenthic ecosystem engineers thus modify the sedimentary habitat mainly through their physical structures, and thus are true autogenic ecosystem engineers.

Understanding the biodiversity eVects of the multitude of biogenic habitat transformations by ecosystem engineers inhabiting coastal sediments is rather complex. Within the European network of excellence MarBEF, we have tried to enhance our general understanding of the biodiversity eVect of ecosystem engineers in soft-sediment coastal ecosystems by establishing collaboration between related research groups. During our meetings, we have formulated two conceptual hypotheses which are presented here and may stimulate further discussions and testing.

Habitat creation by ecosystem engineers: eVects of thresholds and positive feedback loops

Other than trophic relations where intraspeciWc competition for space, nutrients or prey constitutes a negative feedback mechanism on population density, habitat modiWcations by ecosystem engineers tend to constitute a positive feedback on conspeciWcs [START_REF] Cuddington | Invasive engineers[END_REF]. These positive feedbacks generally require a minimal threshold to be surpassed before becoming eVective (e.g. [START_REF] Bouma | Density-dependent linkage of scaledependent feedbacks: a Xume study on the intertidal macrophyte Spartina anglica[END_REF][START_REF] Van Der | Positive feedbacks in seagrass ecosystems-theoretical and management implications[END_REF]). As a result, at sediment shores, isolated individuals of autogenic engineers often come and go. However, once several individuals managed to establish, they synergistically succeed in modifying the environment to their own advantage, and patches of marsh plants, meadows of seagrass or beds of suspension feeders are known to persist over long periods of time (e.g. [START_REF] Van Wesenbeeck | Potential for sudden shifts in transient systems: distinguishing between local and landscape-scale processes[END_REF]. The same kind of positive feedback mechanisms and thresholds appear to apply to allogenic ecosystem engineers. For example, for lugworms, it has been suggested that their bioturbating activities contribute to the maintenance of their sandy habitat by preventing a succession towards muddy bottoms (Volkenborn et al. 2007a). However, again thresholds apply as juvenile lugworms Wrst have to settle outside the areas that are strongly bioturbated by the adults and only later in life Wll in gaps among the adults [START_REF] Reise | Density-dependent recruitment after winter disturbance on tidal Xats by the lugworm Arenicola marina[END_REF]. In stressful environments, such as the seashore, the combination of thresholds and positive feedback dynamics may induce alternative stable state dynamics (e.g. [START_REF] Van Der | Positive feedbacks in seagrass ecosystems-theoretical and management implications[END_REF]). This typically results in large characteristic stands dominated by a principal autogenic or allogenic ecosystem engineer, which generates a modiWed environment that can provide habitat for other species.

In case of autogenic ecosystem engineers, these stands that are dominated by a single ecosystem engineer can provide habitat to an often diverse assemblage of smaller organisms. These may be sessile as is the autogenic engineer itself and tend to constitute a burden, such as fouling algae on seagrass blades or barnacles on mussels. On the other hand, there are mobile organisms which keep the aforementioned fouling organisms in check, i.e. grazing eVects of snails on epigrowth of algae and barnacles rather than feeding on the principal ecosystem engineer. Stands that are dominated by allogenic infaunal ecosystem engineers such as, e.g., lugworms may by their joint irrigation facilitate other infauna [START_REF] Volkenborn | Lugworm exclusion experiment: responses by deposit feeding worms to biogenic habitat transformations[END_REF] and also may accommodate inmates in their burrows [START_REF] Reise | Sediment mediated species interactions in coastal waters[END_REF]. In general, highly diverse benthic assemblages are expected to arise in stands dominated by a principal autogenic or allogenic ecosystem engineer which creates a complex habitat. Understanding the interplay of facilitating and inhibiting eVects in a mechanistic way remains however a challenging area of research (see below).

Mechanisms by which ecosystem engineers may aVect biodiversity

Due to their functional characteristics, ecosystem engineers can exert a strong inXuence on ecosystem properties that exceeds what may be expected based on their relative abundance alone [START_REF] Hooper | EVects of biodiversity on ecosystem functioning: a consensus of current knowledge[END_REF]. Although conceptually this may be easily understood (Fig. 2), understanding the underlying mechanism by which these biodiversity eVects occur is complex, and may involve a mix of diVerent ecosystem characteristics: productivity, disturbance intensity, and habitat complexity.

It has been long time recognised that both productivity and stress (physical, disturbance or predation) can have a strong eVect on biodiversity, for which, we summarise a simpliWed schematic general concept (Fig. 3). Biodiversity is the lowest in situations where productivity is maximal or where stress in the form of physical conditions, disturbance or predation is high. In areas with high productivity, the diversity is determined by competition processes. Hence, if ecosystem engineers modify the productivity, this may also explain their eVect on biodiversity. A meta-analysis on this hypothesis by [START_REF] Wright | Predicting eVects of ecosystem engineers on patch-scale species richness from primary productivity[END_REF] indicated that this approach requires further testing in order to obtain a clear Fig. 1 Visual example of the major habitat modifying impact that can be exerted by a bioturbating endobenthic allogenic ecosystem engineer (a) and a sediment stabilising epibenthic autogenic ecosystem engineer (b). The smooth sediment surface on the mudXat was formed upon the exclusion of bioturbating lugworms (Arenicola marina) by burying a net in the sediment (a; picture courtesy of Nils Volkernborn). The presence of the cordgrass Spartina anglica causes the formation of a dome shaped tussock (b) answer. The hydrodynamic transport of particles may make aquatic systems a suitable system to work on this type of questions [START_REF] Braun-Blanquet | Role of two contrasting ecosystem engineers (Zostera noltii and Cymodocea nodosa) in the food intake rate of Cerastoderma edule[END_REF].

In areas with high physical or disturbance stress, the diversity is kept low by the adaptations required for stress survival mechanisms. Sedimentary shores are typically governed by stress gradients related to inundation period, hydrodynamic forces and Xuctuations in temperature and salinity (Fig. 4). The signiWcance of ecosystem engineering tends to increase in stressful environments [START_REF] Jones | Positive and negative eVects of organisms as physical ecosystem engineers[END_REF], and the decrease of biodiversity of aquatic organisms in up shore direction and that of terrestrial organisms in down shore direction may be mitigated by ecosystem engineering at sediment shores [START_REF] Bertness | Atlantic shorelines: natural history and ecology[END_REF]. There has been a growing recognition of the importance of facilitative interactions for understanding community structure and thereby the local biodiversity in stressful environments, with facilitation generally being due to ecosystem engineering species [START_REF] Bruno | Inclusion of facilitation into ecological theory[END_REF]. Whilst [START_REF] Hacker | Some implications of direct positive interactions for community species diversity[END_REF] emphasised the positive eVect that facilitation by ecosystem engineers can have on community diversity in stressful environments, more recent studies indicate that ecosystem engineers can also cause direct negative species interactions via their modiWcation of the environment (Ecosystem Engineering-exclusion or 'biomechanical warfare ';[START_REF] Van Wesenbeeck | Biomechanical warfare in ecology; negative interactions between species by habitat modiWcation[END_REF]. The relative balance between the role of facilitation versus EE-exclusion (i.e. space between dashed lines, Fig. 3) needs further study.

The eVect of habitat complexity also Wts within the concept summarised in Fig. 3, as increased habitat complexity may reduce predation stress. Autogenic ecosystem engineers often increase habitat complexity and thereby enhance biotic densities and/or diversity [START_REF] Crooks | Characterizing ecosystem-level consequences of biological invasions: the role of ecosystem engineers[END_REF]. A clear example of increased habitat complexity due to autogenic ecosystem engineering is the enhanced macrofaunal biodiversity in seagrass meadows (e.g. see [START_REF] Attrill | Are macroinvertebrate communities inXuenced by seagrass structural complexity?[END_REF][START_REF] Bartholomew | Faunal colonization of artiWcial seagrass plots: the importance of surface area versus space size relative to body size[END_REF]Bologna andHeck 1999, 2002;Edgar 1999a, b;[START_REF] Hovel | Habitat fragmentation in a seagrass landscape: patch size and complexity control blue crab survival[END_REF][START_REF] Hovel | EVects of seagrass landscape structure, structural complexity and hydrodynamic regime on macrofaunal densities in North Carolina seagrass beds[END_REF]. The eVect of allogenic engineers on habitat complexity is less clear: on the one hand, disturbance generation by bioturbating allogenic engineers may destroy above-ground structures and thereby decrease habitat complexity but on the other hand the formation of burrows generates habitat complexity that may increase biodiversity. It is also noted that increased habitat complexity does not necessarily always lead to enhanced biodiversity (e.g. [START_REF] Castel | InXuence of seagrass beds and oyster parks on the abundance and biomass patterns of meiobenthos and macrobenthos in tidal Xats[END_REF]), indicating that there may be other factors involved in explaining biodiversity eVects of ecosystem engineers.

In addition to accounting for diVerent mechanisms (i.e. altering productivity, physical disturbance or predation stress), understanding the eVect of ecosystem engineering on biodiversity may also require accounting for scale-, species-and system-speciWc eVects as exempliWed below. (1) Ecosystem engineers can have opposite eVects on diVerent groups of organisms on diVerent spatial scales within and directly around an engineered habitat. This has been illustrated for the mytilid mussel Musculista senhousia that forms structurally complex byssal mats on the surface of intertidal and subtidal soft sediments [START_REF] Crooks | Habitat alteration and community-level eVects of an exotic mussel, Musculista senhousia[END_REF][START_REF] Crooks | Assessing invader eVects within changing ecosystems: historical and experimental perspective on the role of the exotic mussel in an urban lagoon[END_REF][START_REF] Crooks | Architectural vs. biological eVects of a habitat-altering, exotic mussel, Musculista senhousia[END_REF][START_REF] Reusch | Variable responses of native eelgrass Zostera marina to a non-indigenous bivalve Musculista senhousia[END_REF]. On the landscape scale, ecosystem engineering often cause the replacement of one habitat type at the expense of another.

The net biodiversity eVect will then of course strongly depend on the scale of analysis: within habitats or between habitats or the scale of the whole estuary (also see section on eVects of alien engineers). ( 2) Related ecosystem engineers that share a comparable (autogenic) ecosystem engineering mechanism can diVer greatly in the extent that they modify the local habitat, either due to diVerences in speciWc organism traits (e.g. shoot stiVness of vegetations; [START_REF] Bouma | Trade-oVs related to ecosystem-engineering: a case study on stiVness of emerging macrophytes[END_REF][START_REF] Peralta | Consequences of shoot density and stiVness for ecosystem engineering by benthic macrophytes in Xow dominated areas: a hydrodynamic Xume study[END_REF] or due to diVerences in the local environmental conditions [START_REF] Norkko | Conditional outcomes of facilitation by a habitat-modifying subtidal bivalve[END_REF]Volkenborn et al. 2007a;[START_REF] Buschbaum | Mytilid mussels: global habitat engineers in coastal sediments[END_REF].

The variety in underlying mechanisms and additional interfering factors that all may play a role in the eVect that ecosystem engineers can have on biodiversity, makes it clear why it is diYcult to identify generalities on the eVects of ecosystem engineering on biodiversity. Focusing on a single type of ecosystem may facilitate the identiWcation of such generalities. Hence, we postulate two testable generalising hypotheses to enhance current understanding of the biodiversity eVects of ecosystem engineers in soft-sediment coastal ecosystems.

Biodiversity eVects of epibenthic and endobenthic ecosystem engineers: the epi-endo-engineering exclusion hypothesis (hypothesis 1)

Crooks ( 2002) suggested as a general pattern that autogenic ecosystem engineers often increase biodiversity by increasing habitat complexity, whereas allogenic engineers may decrease biodiversity by generating disturbances that destroy structures and habitat complexity. Other studies, however, hypothesise that in intertidal coastal zones, bioturbating allogenic ecosystem engineers may facilitate other organisms by oxygenation of otherwise anoxic sediments (see references in [START_REF] Reise | Sediment mediated species interactions in coastal waters[END_REF]Volkenborn et al. 2007a, b), making the picture somewhat more complex. Both these contentions are combined in Fig. 5. Basically, the Wrst half of this hypothesis states that the biodiversity of both epibenthic and endobenthic species have an optimum curve in response to the density of epibenthic structures formed by an autogenic ecosystem engineer (Fig. 5, top). As a result of these two optimum curves, with an increasing density of epibenthic structures, the biodiversity shifts from endobenthic to epibenthic. The second half of this hypothesis states that the biodiversity of both epibenthic and endobenthic species have also an optimum curve in response to the bioturbating activity by endobenthic ecosystem engineers (Fig. 5, bottom). As a result of these two optimum curves, with an Fig. 4 Schematic representation of how abiotic stresses change along the elevational gradient present at sedimentary shores for species of aquatic and terrestrial origin (see also [START_REF] Bertness | Atlantic shorelines: natural history and ecology[END_REF]. Because of tidal curves (spring tidal amplitude schematised by solid line; neap tide by dashed line), the inundation period and frequency vary along the elevational gradient. Combined with the requirements for species with a more aquatic or terrestrial physiology, stresses diVer along the elevational gradient (see numbers 1, 2 and 3). Habitat modiWcation by ecosystem engineers may mitigate the stresses occurring along these gradients (e.g. by attenuating hydrodynamic energy from waves; [START_REF] Bruno | Facilitation of cobble beach plant communities through habitat modiWcation by Spartina alterniXora[END_REF]. In areas where abiotic stresses become smaller, biotic stresses will increase in importance [START_REF] Bertness | Atlantic shorelines: natural history and ecology[END_REF]

Aquatic organisms (epi and endo benthic)

Terrestrial organisms -Emersion period 3)

Tidal curves

increasing bioturbating activity, the biodiversity shifts from epibenthic to endobenthic. It is noted that this hypothesis diVers from the trophic group amensalism hypothesis [START_REF] Rhoads | InXuence of deposit-feeding organisms on sediment stability and community trophic structure[END_REF] in that the present hypothesis is based on engineering groups which have very diVerent feedbacks and thereby causing very diVerent dynamics than trophic interactions [START_REF] Van Wesenbeeck | Biomechanical warfare in ecology; negative interactions between species by habitat modiWcation[END_REF]). The attractiveness of the epi-endo-exclusion hypotheses lies in its simplicity, and thereby the ability for testing.

On a small local scale, a mixture of autogenic above-and below-ground ecosystem engineering in combination with the allogenic sediment reworking and irrigation activity will entail a high total diversity of both epibenthic and endobenthic species (e.g. [START_REF] Zaiko | Habitat engineering by the invasive zebra mussel Dreissena polymorpha (Pallas) in a boreal coastal lagoon: impact on biodiversity[END_REF]). However, as soon as one of these ecosystem engineers achieves dominance, it is expected that either epibenthic or endobenthic diversity is facilitated at the expense of the other and that total diversity may decline (Fig. 5). On a landscape scale, alternating patches with autogenic and allogenic ecosystem engineers are expected to produce the highest possible total diversity and species richness. It is hypothesised that high densities of both autogenic and allogenic ecosystem engineers never coincide in coastal sediments (cf. Fig. 5). Low densities, on the other hand, may coincide during succession and where harsh physical or disturbed conditions prevail.

Where epibenthic structures generated by autogenic ecosystem engineering cover most of the sediment surface, endobenthic ecosystem engineering is assumed to be excluded. Also for other endobenthos, living conditions will tend to deteriorate with increasing intensity of epibenthic ecosystem engineering [START_REF] Kochmann | Shift from native mussels to alien oysters: diVerential eVects of ecosystem engineers[END_REF][START_REF] Bouma | Density-dependent linkage of scaledependent feedbacks: a Xume study on the intertidal macrophyte Spartina anglica[END_REF][START_REF] Ysebaert | Impacts of bottom and suspended cultures of mussels Mytilus spp. on the surrounding sedimentary environment and macrobenthic biodiversity[END_REF]). However, more complex relations arise within beds of semi-infaunal mussels [START_REF] Commito | Species diversity in the soft-bottom intertidal zone: biogenic structure, sediment, and macrofauna across mussel bed spatial scales[END_REF][START_REF] Buschbaum | Mytilid mussels: global habitat engineers in coastal sediments[END_REF]. It is also important to include the eVects of accumulating shells [START_REF] Gutiérrez | Mollusks as ecosystem engineers: the role of shell production in aquatic habitats[END_REF]. Primary reasons for a decrease in infaunal diversity can be anoxia in the sediment, soil compaction and limited access to the sediment surface. However, the response may not be linear and a low intensity of epibenthic engineering may actually facilitate endobenthos [START_REF] Norkko | Conditional outcomes of facilitation by a habitat-modifying subtidal bivalve[END_REF]). This eVect may not show up in cohesive mud but in permeable sand. Sand may become stabilised and enriched with biodeposits. Also, individual above-ground structures may cause an advective Xow ameliorating the sediment below [START_REF] Hüttel | Impact of bioroughness on interfacial solute exchange in permeable sediments[END_REF]. Finally, endobenthic organisms may beneWt from erect epibenthic structures where these oVer shelter from hydrodynamic stress, mitigate low tide exposure and provide refuge against epibenthic predators such as crabs, Wsh and birds [START_REF] Woodin | Refuges, disturbance, and community structure: a marine soft-bottom example[END_REF]. However, all these facilitating eVects will soon be replaced by inhibiting eVects when epibenthic structures achieve a dense cover of the sediment surface.

Sediment reworking and irrigation may be the most important modes of allogenic ecosystem engineering in coastal sediments [START_REF] Reise | Sediment mediated species interactions in coastal waters[END_REF]. Sediment reworking destabilises the sediment and generates a dynamic sediment surface layer. This allogenic ecosystem engineering is suggested to inhibit the development of autogenic aboveground structures and keeps epibenthic biodiversity at a low level with a decrease being associated with increasing sediment reworking rate (Fig. 5, bottom). At a low density or intensity of sediment reworking, the development of epibenthic structures cannot be prevented. Where these become established, a balance between sediment reworking and epibenthic structures may allow for a relatively high combined epibenthic and endobenthic diversity. However, low sediment reworking rate does not necessarily entail epibenthic structures. These also may depend on physical stress (hydrodynamics, low tide exposure) and supply of propagules. Together, these will account for a high variability of epibenthic diversity where sediment reworking rates are low.

Endobenthos is facilitated by allogenic ecosystem engineering through burrow structures and burrow ventilation. In permeable sediment, oxygenation and modiWed biogeochemistry extend beyond burrows and improve living conditions for endobenthos living in the surrounding sediment. This will tend to increase endobenthic diversity. These Fig. 5 Schematic representation of the epi-endo-exclusion hypothesis (hypothesis 1). The presence of epibenthic structures on soft-bottoms promotes the diversity of epibenthic organisms, whilst restricting the diversity of endobenthic ecosystem engineers (top). On the other hand, an increased sediment reworking rate due to the presence of endobenthic ecosystem engineers strongly restricts the chances for epibenthic establishment whilst endobenthic diversity is enhanced (bottom). Epibenthic and endobenthic engineers may induce alternative stable states in the same ecosystem facilitative eVects may be partly reversed by allelochemical inhibition [START_REF] Woodin | Allelochemical inhibition of recruitment in a sedentary assemblage[END_REF]) and destabilisation of the sediment. The latter eVect will be more pronounced at a very high intensity of sediment reworking, particularly aVecting small tube builders or organisms that rely on stable sediments for settling and feeding.

Autogenic ecosystem engineering may also occur below the sediment surface, i.e. roots of vascular plants, infaunal bivalves and their dead hard parts [START_REF] Gutiérrez | Mollusks as ecosystem engineers: the role of shell production in aquatic habitats[END_REF], and also solid worm tubes as of Lanice conchilega (e.g. [START_REF] Rabaut | Do Lanice conchilega (sandmason) aggregations classify as reefs? Quantifying habitat modifying eVects[END_REF]. Some of these below-ground structures are obviously associated to above-ground structures, but this is not necessarily the case. The presence of belowground, autogenic structures may further facilitate the development of above-ground structures and thus increase epibenthic diversity [START_REF] Volkenborn | Sediment destabilizing and stabilizing bio-engineers on tidal Xats: cascading eVects of experimental exclusion[END_REF]. Autogenic structures below the surface may also have eVects on endobenthic diversity. At low structural density, there may be some positive eVects on endobenthos, but allelochemicals may also cause the reverse. The main eVect of autogenic structures below the sediment surface will be to inhibit sediment reworking. This results in a decline of bioturbating species and thereby endobenthic diversity with increasing number of space occupation by autogenic structures. Autogenic ecosystem engineering below the sediment surface is assumed to be important in salt marshes and seagrass beds and where infaunal bivalves attain high packing. The corresponding conceptual model for endobenthic and epibenthic diversity resembles roughly the pattern shown in Fig. 5 (top) for autogenic ecosystem engineering above the surface. However, as shown for mussels by [START_REF] Buschbaum | Mytilid mussels: global habitat engineers in coastal sediments[END_REF], the eVects of autogenic bioengineers on biodiversity may vary among environments and the regional species pool as well as among life styles of mussels ranging from epibenthic to endobenthic modes.

EVects of alien engineers on biodiversity in coastal sediments: the engineering-strength hypothesis (hypothesis 2)

It is a widely seen paradox that new additions can make the world much more boring, if those additions are very successful and become dominant, and thereby replace a wide diversity of things that were there before. One of the clearest examples in daily society may be the invasion of fastfood and hotel chains. Adding one will increase the local restaurant/hotel diversity. However, if the formula of a chain becomes highly successful, over time several of the local restaurants and hotels will be displaced, reducing the overall local diversity. The loss of diversity is directly related to the competitive strength of the concept behind the fast-food or hotel chains. The similar paradox is likely to apply to the eVect on invasive species, as invasions may cause biotic homogenisation [START_REF] Olden | Ecological and evolutionary consequences of biotic homogenization[END_REF]). Invasive ecosystem engineers may deserve a special interest in this respect, as they do not only invade a habitat but also modify the habitat [START_REF] Crooks | Characterizing ecosystem-level consequences of biological invasions: the role of ecosystem engineers[END_REF][START_REF] Cuddington | Invasive engineers[END_REF][START_REF] Wallentinus | Introduced marine organisms as habitat modiWers[END_REF]. Hence, invasive ecosystem engineers can exert a strong inXuence on ecosystem properties and biodiversity. If invasive species are ecosystem engineers, they should be regarded as high impact/high risk species. The latter is important for coastal habitats, as a wide range of alien plants and invertebrates may modify the benthic and pelagic environment through physico-chemical changes to the substrate, changes in sediment transport and water Xow, modiWcation of nutrient regime and transparency of water as well as replacement of the keystone habitat forming species [START_REF] Wallentinus | Introduced marine organisms as habitat modiWers[END_REF]. Moreover, in coastal habitats, there is a high risk for invasions due to anthropogenic activities that signiWcantly increase the conductivity between ecosystems.

With respect to the local biodiversity eVect of invasive ecosystem engineers, we pose the hypothesis that the impact depends on the engineering strength of the invasive species (Fig. 6). For the purpose of this hypothesis, we deWne "engineering strength" as the number of habitats that can be transformed by the invading ecosystem engineering species and deWne "local" as the scale of the habitats that were replaced by the habitat created by the invasive engineer. The invasion by an ecosystem engineer will create a new biogenic habitat, thereby generating habitat for biodiversity that matches these conditions (Fig. 6 left, upper dashed line). However, as the engineering species only generates one type of new habitat, the number of species that it will facilitate is limited to a maximum. (Note: for simplicity we ignore the fact that a slight increase in species number may occur in response to increasing total area covered.) A stronger ecosystem engineer can invade more habitats, thereby replacing more original habitats that were supporting another biodiversity (Fig. 6 left, lower dashed line). Hence, the stronger the ecosystem engineer, the greater the loss in biodiversity of the habitats that were transformed. As a result of these two opposing processes, the biodiversity in the invaded area will Wrst increase and then decrease with increasing strength of the invasive ecosystem engineer (Fig. 6 right). On a larger (estuary, coastal bay) scale that also accounts for the areas that are not occupied by the invasive ecosystem engineer, the diversity does not necessarily decrease, regardless of the strength of the ecosystem engineer. The diversity eVect will then of course strongly depend on the overall number of habitats that remain present in the part of the estuary or coastal bay that is regarded. But on an estuary/ecosystem scale, the diversity is always likely to increase, as complete species/habitat replacements tend to be rare in coastal ecosystems (e.g. see WolV 2005; [START_REF] Reise | Are aliens threatening European aquatic coastal ecosystems?[END_REF]. As the invasive engineers can be either endobenthic or epibenthic species invading areas with endobenthic or epibenthic communities, the responses predicted in Fig. 6 are of course closely related to the mechanisms hypothesised in Fig. 5.

Evaluating the ecological impact of invasive species on local ecosystems may be complicated by the observation that invasive engineering species may also facilitate (endangered or rare) native species by providing novel habitat structures [START_REF] Rodriguez | Can invasive species facilitate native species? Evidence of how, when, and why these impacts occur[END_REF]. For coastal habitats this has been exempliWed for the Japanese seaweed Sargassum muticum in European waters [START_REF] Buschbaum | How an introduced seaweed can aVect epibiota diversity in diVerent coastal systems[END_REF][START_REF] Polte | Native pipeWsh Entelurus aequoreus are promoted by the introduced seaweed Sargassum muticum in the northern Wadden Sea[END_REF]. This large alga hosts a diversity of regional taxa including Wsh which have been rare or absent before the invasion but once occurred in seagrass meadows which had vanished long ago. Such facilitation also applies to other alien species which may give rise to an 'invasional meltdown' [START_REF] Simberlov | Positive interactions of nonindigenous species: invasional meltdown?[END_REF]. Near the island of Sylt in the North Sea, where the above-mentioned S. muticum is invading, it is primarily anchored by clusters of PaciWc oysters and American slipper limpets (Reise and Buschbaum, pers. observation). Without these other aliens, S. muticum would have been more limited in its spread. For a proper method to assess the impact of invasive ecosystem engineering species, we refer to [START_REF] Olenin | Assessment of biopollution in aquatic ecosystems[END_REF], who integrated criteria for habitat alteration, habitat fragmentation and habitat loss.

The simplest way to predict the impact that a speciWc species may have upon invasion of a new area seems to be evaluating the eVect of that species on the habitats it currently occupies (either native or invaded). Such approach is however likely to be too simple as the impact of an invasive species will strongly depend on the conditions under which they occur, as exempliWed for mussels and oysters [START_REF] Kochmann | Shift from native mussels to alien oysters: diVerential eVects of ecosystem engineers[END_REF][START_REF] Buschbaum | Mytilid mussels: global habitat engineers in coastal sediments[END_REF][START_REF] Smaal | Introduction, establishment and expansion of the PaciWc oyster Crassostrea gigas in the Oosterschelde (SW Netherlands)[END_REF][START_REF] Zaiko | Habitat engineering by the invasive zebra mussel Dreissena polymorpha (Pallas) in a boreal coastal lagoon: impact on biodiversity[END_REF]). Moreover, it is diYcult to predict the invasiveness of a speciWc area based on observations from another area, as the chances for invasive species depend both on a mixture of competitive and positive interactions [START_REF] Bulleri | Beyond competition: incorporating positive interactions between species to predict ecosystem invisibility[END_REF] and other ecological factors such as propagule supply and the absence of predators, parasites and diseases (e.g. see [START_REF] Engelkes | Successful range-expanding plants experience less above-ground and below-ground enemy impact[END_REF][START_REF] Levine | Species diversity and biological invasions: relating local processes to community pattern[END_REF][START_REF] Reinhart | Plant-soil biota interactions and spatial distribution of black cherry in its native and invasive ranges[END_REF][START_REF] Theoharides | Plant invasion across space and time: factors aVecting nonindigenous species success during four stages of invasion[END_REF]. The strength of the residing ecosystem engineers will also strongly determine the chances of other engineering species to invade and take over their habitat as may be seen from the negative species interactions that may occur via habitat modiWcation (Ecosystem Engineering-exclusion or 'biomechanical warfare'; van [START_REF] Van Wesenbeeck | Biomechanical warfare in ecology; negative interactions between species by habitat modiWcation[END_REF]). Thus, predicting the eVect of an invasive engineering species on forehand is diYcult, but experience learns most invasive engineers have high impacts [START_REF] Crooks | Characterizing ecosystem-level consequences of biological invasions: the role of ecosystem engineers[END_REF].

There remains one last issue to be considered with respect to the impact of invasive species, which is diYcult to translate in numbers. Although we may make an assessment of the impact of an ecosystem engineer using the approach introduced by [START_REF] Olenin | Assessment of biopollution in aquatic ecosystems[END_REF], the visual eVect on the appearance of the landscape may be very large. For example, a relative small reef, e.g. Japanese oysters on a bare tidal Xat, may cause a visual impact that greatly exceeds their quantitative impact on the ecosystem (cf. the visual 'pollution' of identical fast-food restaurants all Fig. 6 Schematic representation of engineering-strength hypothesis (hypothesis 2). This hypothesis describes how local biodiversity eVects of an invasive ecosystem engineer are expected to depend on the strength of the engineering species, with engineering strength deWned as the number of habitats that can be invaded and transformed and local deWned as the areas invaded by the engineering species. An invading engineer is likely to create a single new habitat type, thereby putting a maximum on the species gain. The stronger the ecosystem engineer, the more existing habitat types with their communities it will displace. As a result, a stronger ecosystem engineer is likely to cause a net decrease of biodiversity when regarded at the local scale. On a larger scale, also accounting for the areas that are not occupied by the invasive ecosystem engineer, diversity eVects can be very diVerent and will strongly depend on the chosen scale ecosystem engineering strength net ecosystem diversity effect ecosystem engineering strength net ecosystem diversity effect species gain by facilitation species loss by displacement ecosystem engineering strength ecosystem engineering strength around the world; Fig. 7). Such esthetical factors are also important to take into account when evaluating the biotic homogenisation eVect of invasive species.

Human impacts on ecosystem engineers in coastal sediments: threats and opportunities

An in-depth understanding of the impacts of biodiversity loss [START_REF] Worm | Impacts of biodiversity loss on ocean ecosystem services[END_REF]) and reduction of ecosystem size [START_REF] Barbier | Coastal ecosystem-based management with nonlinear ecological functions and values[END_REF]) on ecosystem services is essential to the well being of mankind. Although it has been recognised that coastal ecosystems dominated by autogenic epibenthic engineers belong to the most valuable ecosystems among the world [START_REF] Costanza | The value of the world's ecosystem services and natural capital[END_REF], they remain threatened and declining [START_REF] Lotze | Depletion, degradation, and recovery potential of estuaries and coastal seas[END_REF][START_REF] Orth | A global crisis for seagrass ecosystems[END_REF]. Hence there is an urgent need to understand in depth how biodiversity and ecosystem functioning in coastal ecosystems is aVected by the presence (and the loss) of such habitat building ecosystem engineers. The presented conceptual hypotheses may help making predictions. For example, autogenic ecosystem engineers are generally more vulnerable to bottom trawling or other physical habitat disturbances than allogenic ecosystem engineers, for which mixed responses are observed [START_REF] Thrush | Disturbance to marine benthic habitats by trawling and dredging: implications for marine biodiversity[END_REF]. This is because the former reside mostly on the sediment surface, whilst the latter are usually deeply buried in the sediment. When physical disturbances by, e.g., bottom trawling increase in intensity and scale (i.e. shift towards left side x axis Fig. 3) causing more and more of the epibenthic structures become destroyed, then total diversity will be conWned to endobenthic species alone (cf. Fig. 5). This may also be seen as an example of the eVect of a strong invasive engineer (humans) that transform a multitude of habitats into a single type, thereby reducing overall biodiversity (cf. Fig. 6).

Hence it is likely that bottom trawling causes a reduction of the overall number of habitat types, thereby causing the overall diversity to decrease.

Although several commercially exploited marine invertebrate and vertebrate species are well recognised for being ecosystem engineers, the consequences of their removal from ecosystems remain largely unknown beyond the single species or population level [START_REF] Coleman | Overexploiting marine ecosystem engineers: potential consequences for biodiversity[END_REF]. However, (over)exploitation of engineering species is likely to have consequences that extend beyond their own decline and strongly aVect the rest of the ecosystem. For example, harvesting of oysters and the consequent destruction of oyster reefs resulted in multiple ecosystem eVects [START_REF] Reise | Long-term changes in the macrobenthic invertebrate fauna of the Wadden Sea: are polychaetes about to take over?[END_REF][START_REF] Lenihan | How habitat degradation through Wshery disturbance enhances impacts of hypoxia on oyster reefs[END_REF]. Recent (exclusion) experiments also demonstrated the role of endobenthic, allogenic ecosystem engineers on ecosystem function [START_REF] Thrush | Functional role of large organisms in intertidal communities: community eVects and ecosystem functioning[END_REF]Volkenborn et al. 2007b;[START_REF] Montserrat | Ecosystem engineering eVects of a benthic community: a defaunation study[END_REF]. These studies provide insight into the eVects of (human-induced) losses of ecosystem engineers on ecosystem functioning and performance, which are of great relevance for the conservation and management of these systems.

The ecosystem engineer concept oVers promising opportunities for restoration ecology [START_REF] Crain | Ecosystem engineering across environmental gradients: implications for conservation and management[END_REF]), but has yet to be formally and explicitly applied. Identifying and managing probable engineering species and responsive ecosystems should be a key priority for conservation. The latter will necessitate a shift to a process-based understanding of the functioning of whole systems, which is a large and important step toward ecosystem-based management [START_REF] Byers | Using ecosystem engineers to restore ecological systems[END_REF]. Posing testable generalising hypotheses on the eVect of ecosystem engineers is an important step in obtaining a broadly applicable processbased understanding.

Fig. 2 Fig. 3

 23 Fig.2Schematic representation of the general mechanism by which an ecosystem engineer may aVect biodiversity. The abiotic environment aVects the ability of organisms to establish (arrows 1, 4). Established ecosystem engineers will modify the abiotic environment (arrow 2), with the extent of the habitat modiWcation depending on the traits of that organism in combination with the abiotic conditions (level of environmental stress) present (arrow 3). This habitat modiWcation will aVect the ability of both the ecosystem engineer itself (arrow 1) as well as other species (arrow 4) to live in such engineered area. The latter may cause facilitation for some species and inhibition for others. The integral of the impact on all other organisms (arrow 5) describes the overall biodiversity eVect of an ecosystem engineer

Fig. 7

 7 Fig. 7The visual eVect of strong invasive ecosystem engineers may qualitatively greatly exceed the quantitative biodiversity inXuence, by creating a strong resemblance in a heterogeneous environment. Will

Acknowledgments

We greatly acknowledge the European network of excellence "MarBEF" for funding the research group "The role of native and/or invasive ecosystem engineers in explaining biodiversity". We like to thank the following European partners for their inputs in the discussions at the various MarBEF workshops: NIOO: P. Herman, B. van Wesenbeeck, E. Cacabellos, F. Brun, F. Montserrat, L. van Duren; UIB-IMEDEA: I. Hendriks, S. Deudero; AWI:

Open Access This article is distributed under the terms of the Creative Commons Attribution Noncommercial License which permits any noncommercial use, distribution, and reproduction in any medium, provided the original author(s) and source are credited.


Marko Herrmann Ae

Jose F ´e

A E Alfaya

L Mauro

A E Lepore

E Pablo

A E Penchaszadeh

¨rgen Ju

Laudien

H.-D M Franke

J Herrmann

M Herrmann
email: marko.herrmann@gmx.de

Á J E F Alfaya

Á M L Lepore

P E Penchaszadeh

Reproductive cycle and gonad development of the Northern Argentinean Mesodesma mactroides (Bivalvia: Mesodesmatidae)

Keywords: Yellow clam, Histology, Condition index, Ash-free, shell-free dry mass, Oocyte size and abundance

The reproductive cycle and gonad development of the yellow clam Mesodesma mactroides was studied over a period of 24 months (January 2005-December 2006) at the Argentinean sandy beach Santa Teresita. Histological examination of gonadal tissue revealed that sex ratios did not significantly deviate from the proportion of 1:1 and no case of hermaphroditism was found. The reproductive cycle of M. mactroides followed an annual cyclicality, which was significantly correlated to monthly mean sea surface temperatures (SST). Oocytes showed highest abundance in winter, indicating a process of gonadal development and sexual maturation. The mean oocyte size decreased significantly during spring. Modal oocyte sizes decreased significantly during winter and late spring of each year, suggesting spawning events. The condition index was not useful in describing the annual reproductive cycle of M. mactroides. Ash-free, shell-free dry mass was chosen to detect the condition of the specimens, and this significantly correlated with monthly mean SST and the gametogenic cycle. Annual recruitment patterns during summer-autumn indicated a 3-month-long planktonic phase of M. mactroides. The reproduction cycle and gonad development of M. mactroides showed only weak differences between data from the present study and those collected 40 years ago.

Introduction

The yellow clam Mesodesma mactroides 1 Reeve,2 1854 (Bivalvia: Mesodesmatidae), locally called 'almeja amarilla', was historically the most common bivalve in its geographic distribution [START_REF] Parodiz | Transgressiones ocea ´nicas y fauna del Mar Epicontinental Argentino[END_REF][START_REF] Stuardo | Distribucio ´n de los moluscos marinos litorales en Latinoame ´rica[END_REF][START_REF] Defeo | Development and management of artisanal fishery for yellow clam Mesodesma mactroides in Uruguay[END_REF]). However, recently, its abundance has significantly decreased [START_REF] Lima | Population dynamics of the yellow clam Mesodesma mactroides: recruitment variability, density-dependence and stochastic processes[END_REF][START_REF] Bergonci | Vertical distribution, segregation by size and recruitment of the yellow clam Mesodesma mactroides Deshayes, 1854 (Mollusca, Bivalvia, Medodesmatidae) in exposed sandy beaches of the Rio Grande do Sul state, Brazil[END_REF][START_REF] Herrmann | Population dynamics of the surf clams Donax hanleyanus and Mesodesma mactroides from open-Atlantic beaches off Argentina[END_REF]. The suspension-feeder currently inhabits intertidal Atlantic sandy beaches from tropical (23°S Ilha Grande, Rio de Janeiro State, Brazil) to temperate regions (40°S Isla del Jabalı ´, Province of Buenos Aires, Argentina; [START_REF] Rios | Seashells of Brazil, 2nd edn[END_REF][START_REF] Fiori | Age and individual growth of Mesodesma mactroides (Bivalvia) in the southernmost range of its distribution[END_REF]. Thus, its distributional range covers about 1,800 km of South Brazilian sandy beaches, 22 km in Uruguay, and 375 km in Argentina, where it represents the only Mesodesma species occurring throughout the mediolitoral (Olivier et al. 1971). On the beaches of northern Argentina, it is found together with the sympatric and dominant surf clam Donax hanleyanus (Olivier et al. 1971;[START_REF] Penchaszadeh | Ecologı ´a de una poblacio ´n de 'berberecho' (Donax hanleyanus) en Villa Gesell, Argentina[END_REF][START_REF] Herrmann | Population dynamics of the surf clams Donax hanleyanus and Mesodesma mactroides from open-Atlantic beaches off Argentina[END_REF]. During the 1940s and 1950s, M. mactroides was an important economic resource for Argentina, with a maximum exploitation rate of 1,079 tonnes in 1953. As a consequence of overfishing, the clam fishery was closed in 1956 [START_REF] Coscaro ´n | La almeja amarilla (Mesodesma (T.) mactroides Deshayes) de la costa de la Provincia de Buenos Aires[END_REF]. Argentinean M. mactroides populations never recuperated and in the 1990s and recently populations were further depleted by mass mortality events. Although red tides and high heavy metal concentrations were given as possible reasons for the massive decimation, the actual cause was never found [START_REF] Odebrecht | Shellfish mortality and red tide event in southern Brazil[END_REF][START_REF] Fiori | Mass mortality of the yellow clam, Mesodesma mactroides (Bivalvia: Mactracea) in Monte Hermoso beach, Argentina[END_REF][START_REF] Thompson | Mortandad masiva de Mesodesma mactroides (Bivalvia: Mactracea) en el partido de la costa, Buenos Aires, Argentina, en Septiembre[END_REF]. Various authors have suggested illegal extractions and the impact of tourist activities as probable main factors for the failure of stock recovery [START_REF] Axiovision | Estructura poblacional de la almeja amarilla (Mesodesma mactroides) durante el verano de 1989 en la Provincia de[END_REF][START_REF] Bastida | The yellow clam (Mesodesma mactroides): a case study of a coastal resource in risk from the South-West Atlantic Ocean[END_REF][START_REF] Herrmann | Population dynamics of the surf clams Donax hanleyanus and Mesodesma mactroides from open-Atlantic beaches off Argentina[END_REF].

Aspects of population dynamics for M. mactroides such as recruitment, growth, production, and mortality are very well studied for the Argentinean [START_REF] Bastida | The yellow clam (Mesodesma mactroides): a case study of a coastal resource in risk from the South-West Atlantic Ocean[END_REF][START_REF] Fiori | Individual biomass and allometry of Mesodesma mactroides from the Southern coast of Buenos Aires, Argentina (Bivalvia, Mactracea)[END_REF]Fiori et al. 2004;[START_REF] Fiori | Age and individual growth of Mesodesma mactroides (Bivalvia) in the southernmost range of its distribution[END_REF][START_REF] Fiori | Biogeographic patterns in life-history traits of the yellow clam, Mesodesma mactroides, in sandy beaches of South America[END_REF][START_REF] Herrmann | Population dynamics of the surf clams Donax hanleyanus and Mesodesma mactroides from open-Atlantic beaches off Argentina[END_REF], the Uruguayan [START_REF] Defeo | Spatial and temporal structure of the yellow clam Mesodesma mactroides (Deshayes 1854) in Uruguay[END_REF][START_REF] Defeo | Estimaciones de stock del recurso almeja amarilla (Mesodesma mactroides) en base al ana ´lisis de cohortes (Pope, 1972)[END_REF][START_REF] Defeo | Dina ´mica espacial del esfuerzo pesquero en una pesquerı ´a artesanal de la costa Atla ´ntica Uruguaya[END_REF][START_REF] Defeo | Growth, mortality and recruitment of the yellow clam Mesodesma mactroides on Uruguayan beaches[END_REF][START_REF] Defeo | Development and management of artisanal fishery for yellow clam Mesodesma mactroides in Uruguay[END_REF][START_REF] Brazeiro | Effects of harvesting and density dependence on the demography of sandy beach populations: the yellow clam Mesodesma mactroides of Uruguay[END_REF][START_REF] Lima | Population dynamics of the yellow clam Mesodesma mactroides: recruitment variability, density-dependence and stochastic processes[END_REF], and the Brazilian coasts [START_REF] Narchi | Aspects of the adaptive morphology of Mesodesma mactroides (Bivalvia: Mesodesmatidae)[END_REF]; Gil and Thome ´2000; Bergonci and Thome ´2008). However, with the exception of [START_REF] Christiansen | Estructura de la Comunidad, Dina ´mica de la Poblacio ´n y Biologı ´a de la Almeja Amarilla (Mesodesma mactroides) en Mar Azul[END_REF], we know of no further studies dealing with the reproductive cycle of this species.

The present study aims to describe the reproductive cycle and gonad development of the yellow clam population of the northern Argentinean sandy beach Santa Teresita in comparison with the above-mentioned study, which was carried out 40 years ago.

Materials and methods

Study area

The present study was carried out at the three south Atlantic sandy beaches Santa Teresita (36°32 0 S, 56°41 0 W), Mar de las Pampas (37°19 0 S, 57°00 0 W), and Faro Querandı (37°29 0 S, 57°07 0 W; Fig. 1), whereby we want to highlight that M. mactroides was only abundant at the first mentioned location during the entire sampling period. Therefore, the reproductive cycle and gonad development of the intertidal yellow clam was studied during alternate spring tides only from the sandy beach Santa Teresita. According to [START_REF] Mclachlan | The definition of sandy beaches in relation to exposure: a simple rating system[END_REF] rating scale for exposure and [START_REF] Short | Physical variability of sandy beaches[END_REF] classifications of beach types, Santa Teresita can be characterised as sheltered and dissipative (for detailed parameters see [START_REF] Herrmann | Population dynamics of the surf clams Donax hanleyanus and Mesodesma mactroides from open-Atlantic beaches off Argentina[END_REF].

This is an open ocean beach receiving continuous wave action and is subject to semidiurnal tides, with a maximum tide range of 1.6 m; spring tides average 1.7 m and mean neap tides 0.2 m. The sea surface temperature (SST) varies between 11°C in winter and 23°C in summer. The study site is composed of good-moderate fine sand, with a mean particle diameter of 2.26 phi [START_REF] Herrmann | Population dynamics of the surf clams Donax hanleyanus and Mesodesma mactroides from open-Atlantic beaches off Argentina[END_REF]. The sandy beach of Santa Teresita is affected by a freshwater seepage and a southward current that brings water masses from the 290 km long and up to 220 km wide estuary of the Rı ´o de la Plata and is thus characterized by a mean salinity of 31. This beach is well drained and oxygenated.

Sampling and histological examination

Samples of M. mactroides were collected monthly between January 2005 and December 2006 at a series of stations (4 m intervals). The stations were positioned along three transects separated by 20 m intervals and located perpendicular to the shoreline from the spring tide high water mark to the neap tide low water mark. At each station, three replicated sand samples were excavated to 35 cm depth using a 0.16 m 2 steel corer, and thereafter sieved individually on a 1 mm mesh. For biomass determinations as well as for calculations of the condition index (CI), a total of 720 sampled specimens were preserved in 70% ethanol and subsequently analysed in the laboratory, as described in the following paragraph. For histological examinations, again, a total of 720 individuals were sampled and gonads, covering the full range of sizes of specimens under gametogenic activity (2-64 mm anteriorposterior shell length [apSL]), were selected for histological analysis. The apSL of clams was measured in situ to the nearest 0.01 mm with a digital vernier calliper (Mitutoyo,. For histological processing, intact clams with cut through adductor muscles were fixed in Bouin's solution for two hrs, afterwards transferred into a 70% ethanol solution and later processed in the laboratory using standard methods [START_REF] Romeis | Mikroskopische Technik[END_REF], including embedding in paraffin, sectioning at 5 lm and staining with hematoxylin-eosin. Photographical analyses were carried out with a Zeiss Axio Imager Z1 light microscope equipped with a Sound Vision digital camera using the imaging software AxioVision 4.4 (2008). Abundance (mm -2 ) and size of oocytes (mean diameter obtained from measurements of 30 oocytes per specimen) were determined from histological slides, except for the period of January to February 2005 and January 2006, where clams showed only the gonad stage 0 (sexual rest stage with apSL \ 10 mm). Gonads of M. mactroides were classified into five developmental stages following [START_REF] Christiansen | Estructura de la Comunidad, Dina ´mica de la Poblacio ´n y Biologı ´a de la Almeja Amarilla (Mesodesma mactroides) en Mar Azul[END_REF], but combining the early active with the late active stage and the early ripe with the ripe stage (Fig. 2, Table 1). Individuals without germ cells were categorized in the sexual rest stage. Using chi-square (v 2 ) analysis, the sex ratio of M. mactroides was calculated according to the presence of oocytes and sperms. As clams were in a resting stage between January and March of both years, the respective sex ratio could not be determined. The SST was measured daily at 13:00 pm using a digital thermometer to a precision of 0.1°C. Data of length-frequency distributions of M. mactroides and their consequent cohort analyses were taken from [START_REF] Herrmann | Population dynamics of the surf clams Donax hanleyanus and Mesodesma mactroides from open-Atlantic beaches off Argentina[END_REF].

Condition index, biomass and recruitment

The CI of preserved M. mactroides was calculated to trace seasonal variation in the visceral mass. After blotting on filter paper, the total wet mass was recorded immediately to the nearest 0.1 mg. After this, valves, mantle, siphons, retractor and adductor muscles were removed. The wet mass of the resulting standard compact unit consisting of the visceral mass and foot was recorded. The CI was calculated according to the equation of de [START_REF] De Villiers | Reproduction of the sand mussel Donax serra Roding[END_REF], namely CI = 100 M v /(M t -M v ), where M v is the wet visceral mass (including the foot) and M t is the total wet mass.

As shown below, the CI was not the best proxy to evaluate the condition of the individuals, since the gonadfoot unit could not separated very accurately. Therefore, ash-free, shell-free dry mass (AFDM) of preserved yellow clams was recorded throughout the sampling time as an estimator of specimens' condition, whereby the conversion factor of 0.186 was empirically determined according to [START_REF] Brey | Energy content of macrobenthic invertebrates: general conversion factors from weight to energy[END_REF].

Recruits, here defined as clams ranging from 2 to 6 mm apSL, were sampled and measured as described in the previous chapter.

Statistical analysis

Sex ratios (male:female) of yellow clams were calculated according to the presence of oocytes and spermatozoa using v 2 analysis. The influence of SST on the gametogenic cycle, as well as its correlation with CI and AFDM were statistically analyzed by Spearman's rank order correlation. Furthermore, to evaluate the null hypothesis of no difference in the gametogenic cycle throughout the year, one-way analysis of variance (ANOVA) was preformed with subsequent Tukey HSD post hoc test when differences were found, using months or seasons as factor and proportion of ripe and spawning individuals as dependent variable. Temporal differences of oocyte abundance were tested by one-way ANOVA. All statistical analyses were carried out using the statistical package SPSS version 17.0 (SPSS 2008). Differences were considered significant at a level of a = 5% [START_REF] Zar | Biostatistical analysis[END_REF].

Results

Gonad development

Histological examinations of the gonads from the 24 month sampling series demonstrated that the reproductive cycle of M. mactroides has a distinct seasonality. The sex ratio did not deviate significantly from the proportion of 1:1 (v 2 = 1.711, df = 1, p [ 0.05) during the study period. About 42% (N = 302) of the individuals were identified as females, 38% (N = 274) as males, and 20% (N = 144) were in a sexual rest stage, which occurs mainly in summer. No case of hermaphroditism was found. Male (Fig. 2a,b) and female (Fig. 3a,b) gonads were active from austral autumn-spring with maximum values in winter and in the ripe stage (male: Fig. 2c-e, female: Fig. 3c-e) during the same period (Fig. 4a,b). Spawning of males (Fig. 2f,g) took place mainly in winter-spring (from July to November 2005 and from August to December 2006; Fig. 4a). Females spawned (Fig. 3f,g) between October and November (2005) and June, and November and December (2006) (Fig. 4b). Male gonads were cytolysed (Fig. 2h) during winter and spring (Fig. 4a), whereas cytolysed stages of females (Fig. 3h) were present between autumn and winter (in June, July) and in late spring (November to December 2005 and December 2006; Fig. 4b).

Reproduction cycle

The examination of histological sections confirmed a seasonal gonadal development in M. mactroides. SST (Fig. 5a) was significantly correlated twice with the gametogenic cycle (gonad stages ripe and spawning, Fig. 5b); between February and March of both years (Spearman's rank order correlation, r s = -0.833, p \0.05, N = 8) and between July and October of both years (Spearman's rank order correlation, r s = 0.850, p \ 0.05, N = 8). Furthermore, the relative proportion of ripe and spawning individuals was significantly different between months (F 11,12 = 7.623, p \ 0.05) and seasons (F 3,20 = 7.305, p \ 0.05), whereas the proportion of ripe and spawning female individuals was significantly higher in spring and autumn (Tukey HSD post hoc test; Fig. 5b).

In both years, yellow clam oocytes showed highest abundance in winter with a maximum in September (oneway ANOVA, August to October vs. remaining year, F 1,15 = 6.594, p \ 0.05; Fig. 5c), indicating a seasonal process of gonadal development and sexual maturation. Minimum oocyte abundance was observed in autumnwinter and in late spring of both years (one-way ANOVA, May to July and December vs. rest of the year, F 1,15 = 4.847, p \ 0.05; Fig. 5c), where most of the clams were in the cytolysed stage (Fig. 4).

Mean oocyte size decreased significantly in spring of both years (one-way ANOVA, October-December vs. April-September, F 1,15 = 4.692, p \ 0.05) (Table 2).

Unimodal histograms of monthly oocyte size classes ranged from 5 lm in November-December to 60 lm in August-September (Fig. 6). Modal oocyte sizes decreased significantly twice each year in winter and late spring, suggesting two spawning events (one-way ANOVA testing August and December vs. the other months, F 1,12 = 35.368, p \ 0.05; see dotted arrows in Fig. 6). increase of AFDM occurred alongside higher SST (Fig. 5a,e). Values of AFDM were also significantly correlated with mature gonad stages (ripe and spawning) during winter and spring (July-November) of 2005 and 2006 (Spearman's rank correlation, r s = 0.721, p \ 0.05, N = 10). The AFDM increased concurrently with the maturation of the gonad (Fig. 5c,e). In the second year, higher values of AFDM indicated growth and gonad development in the same cohort analyzed already in the previous year.

Recruits of the yellow clam settled on the Santa Teresita sandy beach in both years during summer and autumn (in 2005: January-July; in 2006: February-May; Fig. 5f). Thus, the settling period of recruits is again significantly correlated with SST: abundance of recruits increased significantly during summer-autumn in both years (Spearman's rank order correlation, r s = 0.421, p \ 0.05, N = 24; Fig. 5a,f).

Discussion

Gonadal development

The reproductive strategy of M. mactroides from Santa Teresita (present study) is summarized in Table 3 and compared with the 40-year-old historical data obtained from a Mesodesma-population approximately 100 km south of the Santa Teresita population (Mar Azul, Christiansen 1971). Table 3 shows a clear difference between the gonad stages during summer. Whereas [START_REF] Christiansen | Estructura de la Comunidad, Dina ´mica de la Poblacio ´n y Biologı ´a de la Almeja Amarilla (Mesodesma mactroides) en Mar Azul[END_REF] found nearly all developmental stages all year round, in the present study, the active, ripe, spawning, and cytolysed stages were only recorded from autumn to spring and the sexual rest stage occurred only in summer. The existence of a sexual rest period has also been described for other bivalves (Donax serra: [START_REF] Laudien | Reproduction and recruitment patterns of the surf clam Donax serra (Bivalvia, Donacidae) on two Namibian sandy beaches[END_REF]; Ensis siliqua and E. arcuatus: [START_REF] Darriba | Reproductive cycle of the razor clam Ensis arcuatus (Jeffreys, 1865) in northwest Spain and its relation to environmental conditions[END_REF][START_REF] Darriba | Gametogenic cycle of Ensis siliqua (Linnaeus, 1758) in the Rı ´a de Corcubio ´n, northwestern Spain[END_REF]. The absence of active gonad stages in both summers studied is attributed to a single cohort with a small shell length (mean apSL of 8 mm in summer seasons: Herrmann 2009) and to the consequent immaturity (sexual rest stage) of M. mactroides during this period. In contrast to the recent population structure of the yellow clam, Olivier and Penchaszadeh (1971) found three cohorts where individuals of commercial size ([60 mm, Coscaro ´n 1959) were found throughout the year. However, comparison of data from areas with different beach morphodynamics (Santa Teresita: dissipative and sheltered; Mar Azul: exposed and intermediate) is difficult; [START_REF] Delgado | Tisular and population level responses to habitat harshness in sandy beaches: the reproductive strategy of Donax hanleyanus[END_REF] found differential behavior patterns in the reproductive strategy of D. hanleyanus when comparing reflective and dissipative beaches.

Reproduction cycle

The present investigation of M. mactroides gonads suggests two reproductive events per year; the first one in winter and the second one in spring. [START_REF] Christiansen | Estructura de la Comunidad, Dina ´mica de la Poblacio ´n y Biologı ´a de la Almeja Amarilla (Mesodesma mactroides) en Mar Azul[END_REF] also recorded two spawning events for the same species at the same beach; however, these occurred later in the season (spring and early summer). For the congener M. donacium, two spawning events were also observed by Filun [START_REF] Villablanca | Ecologia reproductiva de Mesodesma donacium (Lamarck, 1818) (Bivalvia: Mesodesmatidae), en la playa de Mehuin[END_REF] in northern Chile where reproductive events occurred in spring-summer and autumn. However, [START_REF] Peredo | Gametogenesis and reproductive cycle of the surf clam Mesodesma donacium (Lamarck, 1818) (Bivalvia: Mesodesmatidae) at Queule Beach, southern Chile[END_REF] observed only one spawning period for M. donacium from the southern Chilean coast. These differences may be attributed to distinct environmental conditions such as SST, salinity, and food availability [START_REF] Sastry | Reproductive physiological variation in latitudinally separated populations of the bay scallop Aequipecten irradians Lamarck[END_REF][START_REF] De Villiers | Reproduction of the sand mussel Donax serra Roding[END_REF][START_REF] Peredo | Gametogenesis and reproductive cycle of the surf clam Mesodesma donacium (Lamarck, 1818) (Bivalvia: Mesodesmatidae) at Queule Beach, southern Chile[END_REF][START_REF] Penchaszadeh | Reproductive cycle of the south American scallop Amusium laurenti (Gmelin, 1791) (Bivalvia, Pectinidae)[END_REF][START_REF] Kraeuter | Biology of the hard clam[END_REF][START_REF] Laudien | Reproduction and recruitment patterns of the surf clam Donax serra (Bivalvia, Donacidae) on two Namibian sandy beaches[END_REF]. Seasonal changes in SST trigger gametogenesis, and further to this, short-term temperature changes may stimulate spawning [START_REF] Ansell | Reproduction, growth and mortality of Venus striatula (da Costa) in Kames Bay, Millport[END_REF][START_REF] Seed | Ecology[END_REF]). The present results show that changes in SST are ) and an increase in the number of individuals in ripe and spawning stages (Fig. 5a,b). Maximum gamete ripeness and size observed in winter (July-August) was related to seasonal minimum SST. Noticeable decreases in oocyte sizes (Fig. 6), abundance, and the increased number of spawned and spent individuals was associated with rapid increases in SST during spring (Fig. 5a). Multiple stages of gonad conditions were also observed in late spring (November). However, several authors (e.g. [START_REF] Sastry | The relationships among food, temperature, and gonad development of the bay scallops Aequipecten irradians Lamarck[END_REF][START_REF] Giese | Introduction: general principles[END_REF][START_REF] Sastry | Pelecypoda (excluding Ostreidae)[END_REF]) have mentioned that the reproductive cycle of suspension feeders is not only influenced by physical parameters such as SST, but also by changes in phytoplankton biomass and species compositions. The increase of chlorophyll a concentrations in the Buenos Aires shelf region observed during winter and summer by [START_REF] Carreto | Hydrography and chlorophyll a in a transect from the coast to the shelf-break in the Argentinian Sea[END_REF] with a main peak in spring and a secondary peak in autumn, correspond considerably with the dominance of M. mactroides in ripe and spawning stages (Fig. 5b). This suggests that phytoplankton may also have a direct impact on the reproductive cycle of M. mactroides.

Monthly oocyte size-frequency distribution histograms (Fig. 6) have proved to be a useful method for studying the gonad development of the yellow clam, as they have also been for several bivalves from previous studies (e.g. et al. 2008). However, for M. mactroides, the CI was not useful as it did not significantly correlate with the gametogenic cycle (cf. Fig. 5b,d). Although CI decreased in spring 2005 marking the main spawning period, in winter to Fall 2005, the values of CI were still low despite the gonads being mature and a high percentage of clams being ripe. A decrease in the CI as a result of spawning activity in 2006 was not identified. Thus, the CI is not useful to describe the spawning of the yellow clam. As a consequence of the prolonged spawning period of the population, all reproductive stages were present between May and December (Fig. 4). However, seasonal variation of the AFDM was positively correlated with SST as well as with the gametogenic cycle (Fig. 5a,c,e). When assuming that the collected recruits originated from the studied adult population, the results indicate a meroplanktonic phase of approximately 3 months. Recruits appeared in the intertidal zone of Santa Teresita in summer-autumn of both years (from January to July 2005 and from February to May 2006), where the latter occurrence is apparently the result of the spawning event between November and December 2005 (Figs. 4,5f,6). After weak gamete release periods in July-August 2005 and June-July 2006 (Fig. 6), recruits were not present in the sampling area (Fig. 5f). However, the absence of recruits does not necessarily indicate a lack of spawning activity [START_REF] Caddy | Enhancing or restoring the productivity of natural populations of shellfish and other marine invertebrate resources[END_REF] as environmental conditions, which strongly influence recruitment of marine invertebrates (e.g. hydrodynamic processes: [START_REF] Roughgarden | Recruitment dynamics in complex life cycles[END_REF]food limitation: Olson and Olson 1989;predators: Sale 1990), may not have been favourable for successful recruitment at the 'parent beach'. In contrast, four decades ago, [START_REF] Christiansen | Estructura de la Comunidad, Dina ´mica de la Poblacio ´n y Biologı ´a de la Almeja Amarilla (Mesodesma mactroides) en Mar Azul[END_REF] observed recruits during spring (November and December) as well as the recruitment event in summer (March). This may be due to changes in the population structure of M. mactroides during the last four decades; while Olivier and Penchaszadeh (1971) monitored three cohorts between 1968and 1969[START_REF] Herrmann | Population dynamics of the surf clams Donax hanleyanus and Mesodesma mactroides from open-Atlantic beaches off Argentina[END_REF] detected only one cohort during 2005-2006. In conclusion, only weak differences in the reproduction cycle and gonad development of M. mactroides between the present study and those of [START_REF] Christiansen | Estructura de la Comunidad, Dina ´mica de la Poblacio ´n y Biologı ´a de la Almeja Amarilla (Mesodesma mactroides) en Mar Azul[END_REF] were found. This could be due to the fact that recently just one cohort at one sandy beach was found [START_REF] Herrmann | Population dynamics of the surf clams Donax hanleyanus and Mesodesma mactroides from open-Atlantic beaches off Argentina[END_REF]) and the beaches were dissimilar.

Fig. 1

 1 Fig. 1 Map of the study sites Santa Teresita (S), Mar de las Pampas (M) and Faro Querandı (F), M. mactroides was only abundant at the first mentioned location during the entire sampling period (black ladled). Filled circle indicates the southern-most distribution limit of M. mactroides at Isla del Jabalı ´. Dotted areas present northern and southern sandy beaches of the Province of Buenos Aires where major M. mactroides populations existed in 1959 (Coscaro ´n)

Fig. 2

 2 Fig. 2 Microphotography (colour pictures of full size: Herrmann et al. 2008) of male gonad stages of M. mactroides: a early active stage, b late active stage, c early ripe stage, d, e ripe stage, f partially spawned stage, g spent stage, h recovery stage (aw alveolar wall, gn goias, s sperm, sd spermatids, tf transverse fibre, scale bars are 100 lm)

  Condition index, biomass, and recruitmentAlthough the annual reproductive cycle of M. mactroides did not significantly correlate with the CI (Spearman's rank order correlation, p [ 0.05), specimens showing periods of ripeness and spawning demonstrated an increasing trend of CI in autumn-winter, and specimens showing periods of cytolysed and active stages demonstrated a decreasing trend of CI in spring-summer of both years, respectively (Fig.5b, d).The seasonal variation of the yellow clams' biomass (AFDM) was significantly correlated with SST during winter and spring (July-December) of both years (Spearman's rank correlation, r s = 0.789, p \ 0.05, N = 12), an

Fig. 3

 3 Fig. 3 Microphotography (colour pictures of full size: Herrmann et al. 2008) of female gonad stages of M. mactroides: a early active stage, b late active stage, c early ripe stage, d, e ripe stage, f partially spawned stage, g spent stage, h recovery stage (aw alveolar wall, gn goias, o oocyte, tf transverse fibre, scale bars are 100 lm)

Fig. 4 Fig. 5 M

 45 Fig. 4 Proportion of distinct gonad stages in mature male (a) and female (b) M. mactroides, sampled at Santa Teresita

Fig. 6

 6 Fig. 6 Monthly oocyte size-frequency distribution of M. mactroides collected at Santa Teresita. The abrupt decreases of oocyte modal sizes in August/December 2005 and in July/December 2006 indicate two spawning events per year (dotted arrows). N number of oocytes

Table 1

 1 Explanation of the gametogenic scale and the use of descriptive terms (primer column: present study; second column: after Christiansen 1971), utilized in scoring histological analysis of gonad tissue to assess the gametogenic stages of M. mactroides

	Gonad stages			Brief description of gonad	*Photo
	Present study	After Christiansen (1971)
	Sexual rest	0	Sexual rest	A total absence of gametes, making it impossible to distinguish
				between sexes, empty follicles are observed
	Active	I	Early active stage	Follicles few and small, sex distinguishable, protogonia and gonia in	a
				mitosis
		II	Late active stage	Follicle size increases, spermatogonia and spermatocytes in males,	b
				oogonia and previtellogenic oocytes in females
	Ripe	III	Early ripe stage	Follicle size increases and occupies the entire tissue, germinal cells in	c
				all phases of gametogenesis
		IV	Ripe stage	Polygonal follicles almost full of ripe gametes, spermatozoa occupy	d and e
				most of follicle, free ripe polygonal oocytes in the lumen
	Spawning	V	Partially spawned stage	Gonoducts with mature gametes in emission. Spermatozoa lose radial	f
				disposition. Free ripe rounded oocytes in the lumen and empty
				spaces
		VI	Spent stage	Follicles small and practically empty, residual gametes degrading	g
	Cytolysed	VII	Recovery stage	Gonadal follicles at this stage are empty, except for residual gametes,	h
				amoebocytes are present within the follicles, close to the walls and
				in the centre
	The individual stages of male and female yellow clam gonads are imaged at Figs. 2 and 3, respectively (*Photo)

Table 2

 2 M. mactroides. Monthly SST (°C), values of oocyte size (lm), mean oocyte size ð" xÞ; number of females (f), number of measured oocytes (o), and stages of oocyte development (according to Table1)

	Year	Month	SST (°C)	Oocyte size (lm)	" x ± SD (lm)	f	o	Stage of development
	2005	Jan	21	-	-	-	-	Sexual rest
		Feb	21	-	-	-	-	Sexual rest
		Mar	20	-	-	-	-	Sexual rest
		Apr	17	-	-	-	-	Sexual rest
		May	14	29-30	29.00 ± 1.06	3	60	Ripe
		Jun	13	23-49	27.83 ± 1.19	3	30	Active
		Jul	12	12-43	36.80 ± 1.03	3	90	Cytolysed
		Aug	13	10-53	26.85 ± 0.55	17	289	Active
		Sep	15	15-48	32.43 ± 1.36	11	316	Active and spawning
		Oct	16	18-45	31.30 ± 1.27	6	208	Ripe
		Nov	19	8-58	30.95 ± 2.16	10	273	Spawning
		Dec	21	8-47	16.01 ± 1.56	3	25	Cytolysed
	2006	Jan	22	-	-	-	-	Sexual rest
		Feb	23	-	-	-	-	Sexual rest
		Mar	21	-	-	-	-	Sexual rest
		Apr	20	16-44	33.17 ± 4.27	3	54	Active and ripe
		May	15	23-45	34.66 ± 0.90	3	28	Ripe
		Jun	13	13-43	33.16 ± 2.08	3	90	Spawning and cytolysed
		Jul	12	13-45	36.01 ± 2.02	3	60	Cytolysed
		Aug	11	10-53	25.70 ± 2.71	10	286	Ripe
		Sep	13	10-55	30.53 ± 2.80	10	325	Ripe
		Oct	17	13-59	33.61 ± 0.87	13	454	Ripe
		Nov	20	8-45	24.21 ± 2.95	5	208	Spawning
		Dec	22	13-51	32.37 ± 2.43	7	195	Spawning

Table 3

 3 Reproductive strategy of M. mactroides comparing data from present study with data four decades ago[START_REF] Christiansen | Estructura de la Comunidad, Dina ´mica de la Poblacio ´n y Biologı ´a de la Almeja Amarilla (Mesodesma mactroides) en Mar Azul[END_REF] [START_REF] Hofmann | A population dynamics model of the hard clam, Mercenaria mercenaria: development of the age-and length-frequency structure of the population[END_REF]. This index generally indicates the gonadal mass changes throughout the year[START_REF] Grant | The analysis of data in studies of invertebrate reproduction. I. Introduction and statistical analysis of gonad indices and maturity indices[END_REF] with highest values when gonads are mature. The CI proved to indicate the gametogenic cycle even in bivalves with a gonad not easily separable from the foot such as Donax trunculus[START_REF] Gaspar | Growth and reproductive cycle of Donax trunculus L., (Mollusca: Bivalvia) off Faro, southern Portugal[END_REF], D. serra[START_REF] Laudien | Reproduction and recruitment patterns of the surf clam Donax serra (Bivalvia, Donacidae) on two Namibian sandy beaches[END_REF]), and M. donacium (Riascos

	Gonad	Summer Autumn Winter Spring
	stages

In previous studies, Deshayes 1854 was cited falsely as the author who first described M. mactroides. However, this description was not published by Deshayes but by his colleague Reeve; thus, the corresponding author of M. mactroides is Reeve (see Reeve 1854; Deshayes 1855).

Helgol MarRes (2009) 63:207-218

Acknowledgments This work was part of the doctor thesis of Marko Herrmann and subject of the diploma thesis (licenciatura) of Jose ´E. F. Alfaya, partly supported by 'Deutscher Akademischer Austauschdienst (DAAD)' and by the University of Bremen. The authors thank Sonia Cabrera, Maria Eugenia Segade Enrique, Juan Pablo Livore, my partner Sandra Noir, Francisco Villalba and Soledad Zabala for field assistance as well as the youngest helper Bele ´n Alvela who measured water surface temperature off Santa Teresita each day. Additional thanks are also expressed to all Argentinean colleagues from the laboratory 19 at the Facultad de Ciencias Exactas y Naturales (UBA) and from the laboratory 80 at the Museo Argentino de Ciencias Naturales -'Bernardino Rivadavia' (MACN).

1 M. mactroides reference specimens were deposited in the collec-