Applying landscape metrics to species distribution model predictions to characterize internal range structure and associated changes.

Distributional shifts in species ranges provide critical evidence of ecological responses to climate change. Assessments of climate-driven changes typically focus on broad-scale range shifts (e.g. poleward or upward), with ecological consequences at regional and local scales commonly overlooked. While these changes are informative for species presenting continuous geographic ranges, many species have discontinuous distributions-both natural (e.g. mountain or coastal species) or human-induced (e.g. species inhabiting fragmented landscapes)-where within-range changes can be significant. Here, we use an ecosystem engineer species (Sabellaria alveolata) with a naturally fragmented distribution as a case study to assess climate-driven changes in within-range occupancy across its entire global distribution. To this end, we applied landscape ecology metrics to outputs from species distribution modelling (SDM) in a novel unified framework. SDM predicted a 27.5% overall increase in the area of potentially suitable habitat under RCP 4.5 by 2050, which taken in isolation would have led to the classification of the species as a climate change winner. SDM further revealed that the latitudinal range is predicted to shrink because of decreased habitat suitability in the equatorward part of the range, not compensated by a poleward expansion. The use of landscape ecology metrics provided additional insights by identifying regions that are predicted to become increasingly fragmented in the future, potentially increasing extirpation risk by jeopardising metapopulation dynamics. This increased range fragmentation could have dramatic consequences for ecosystem structure and functioning. Importantly, the proposed framework-which brings together SDM and landscape metrics-can be widely used to study currently overlooked climate-driven changes in species internal range structure, without requiring detailed empirical knowledge of the modelled species. This approach represents an important advancement beyond predictive envelope approaches and could reveal itself as paramount for managers whose spatial scale of action usually ranges from local to regional.

Seascape genomics reveals population isolation in the reef-building honeycomb worm, Sabellaria alveolata (L.).

BACKGROUND: Under the threat of climate change populations can disperse, acclimatise or evolve in order to avoid fitness loss. In light of this, it is important to understand neutral gene flow patterns as a measure of dispersal potential, but also adaptive genetic variation as a measure of evolutionary potential. In order to assess genetic variation and how this relates to environment in the honeycomb worm (Sabellaria alveolata (L.)), a reef-building polychaete that supports high biodiversity, we carried out RAD sequencing using individuals from along its complete latitudinal range. Patterns of neutral population genetic structure were compared to larval dispersal as predicted by ocean circulation modelling, and outlier analyses and genotype-environment association tests were used to attempt to identify loci under selection in relation to local temperature data. RESULTS: We genotyped 482 filtered SNPs, from 68 individuals across nine sites, 27 of which were identified as outliers using BAYESCAN and ARLEQUIN. All outlier loci were potentially under balancing selection, despite previous evidence of local adaptation in the system. Limited gene flow was observed among reef-sites (FST = 0.28 ± 0.10), in line with the low dispersal potential identified by the larval dispersal models. The North Atlantic reef emerged as a distinct population and this was linked to high local larval retention and the effect of the North Atlantic Current on dispersal. CONCLUSIONS: As an isolated population, with limited potential for natural genetic or demographic augmentation from other reefs, the North Atlantic site warrants conservation attention in order to preserve not only this species, but above all the crucial functional ecological roles that are associated with their bioconstructions. Our study highlights the utility of using seascape genomics to identify populations of conservation concern.

The dark side of soft tissues: Unexpected inorganic carbonate in the invasive slipper limpet Crepidula fornicata and its implications for stable isotope interpretations.

RATIONALE: Stable isotopic analysis is extensively used in trophic ecology. Inorganic carbonates, usually originating from shell fragments, are routinely removed from samples using an acid treatment because they affect δ13 C values. However, acid treatment can also change δ15 N values. For some taxa such as molluscs, the general assumption is that acid pre-treatment is not necessary since their shell is easily dissected from soft tissues and represents the only source of inorganic carbonates. However, other sources of non-dietary carbon (e.g., intracellular inorganic carbon) enriched in13 C thus get overlooked. METHODS: Soft tissues (foot) of the invasive gastropod Crepidula fornicata of different size classes were analysed for their δ13 C and δ15 N values with and without acid pre-treatment using isotope ratio mass spectrometry. In toto microscopic investigations coupled with acid treatment, scanning electron microscopy and energy-dispersive spectroscopy were used to highlight the presence of inorganic carbonate. A correction model was derived and applied to existing stable isotope data for C. fornicata. We used both seasonal variations in δ13 C signatures and mixing model outputs to assess the error in δ13 C values. RESULTS: Acid pre-treatment had a significant effect on the stable isotope compositions of C. fornicata foot tissue, especially on δ13 C values: isotopic differences increased with size, up to 3‰ for large females. No effect was detected for small (below ~20 mm) and motile males. In toto microscopic analysis revealed the presence of small spherules of inorganic carbonate, hence explaining the differences in δ13 C values. Mixing model outputs and seasonal variation of δ13 C values showed that untreated samples can lead to large misinterpretations about diet proportions and degree of trophic niche overlap, respectively. CONCLUSIONS: Spherules of inorganic carbonate in C. fornicata soft tissues are likely to be linked with the motility of this species and their mucus production. We recommend assessing the presence of inorganic carbonate in soft tissue of sessile gastropods.

Environmental filtering and biotic interactions act on different facets of the diversity of benthic assemblages associated with eelgrass.

Eelgrass supports diverse benthic communities that ensure a variety of ecosystem functions. To better understand the ecological processes that shape community composition in eelgrass at local and regional scales, taxonomic and functional α- and ß-diversity were quantified for communities inhabiting five meadows in France. The extent to which environmental factors affected local and regional benthic communities was quantified by considering their direct and indirect effects (through morphological traits of eelgrass) using piecewise structural equation modeling (pSEM). Communities supported by eelgrass had higher species abundances, as well as taxonomic and functional diversity compared to nearby bare sediments. No significant differences were found between communities from the center relative to the edges of meadows, indicating that both habitats provide similar benefits to biodiversity. The presence of a few abundant species and traits suggests moderate levels of habitat filtering and close associations of certain species with eelgrass. Nevertheless, high turnover of a large number of rare species and traits was observed among meadows, resulting in meadows being characterized by their own distinct communities. High turnover indicates that much of the community is not specific to eelgrass, but rather reflects local species pools. pSEM showed that spatial variation in community composition (ß-diversity) was primarily affected by environmental conditions, with temperature, current velocity, and tidal amplitude being the most significant explanatory variables. Local richness and abundance (α-diversity) were affected by both environment and morphological traits. Importantly, morphological traits of Zostera marina were also influenced by environmental conditions, revealing cascading effects of the environment on assemblages. In sum, the environment exerted large effects on community structure at both regional and local scales, while plant traits were only pertinent in explaining local diversity. This complex interplay of processes acting at multiple scales with indirect effects should be accounted for in conservation efforts that target the protection of biodiversity.

Inferences to estimate consumer's diet using stable isotopes: Insights from a dynamic mixing model.

Stable isotope ratios are used to reconstruct animal diet in trophic ecology via mixing models. Several assumptions of stable isotope mixing models are critical, i.e., constant trophic discrimination factor and isotopic equilibrium between the consumer and its diet. The isotopic turnover rate (λ and its counterpart the half-life) affects the dynamics of isotopic incorporation for an organism and the isotopic equilibrium assumption: λ involves a time lag between the real assimilated diet and the diet estimated by mixing models at the individual scale. Current stable isotope mixing model studies consider neither this time lag nor even the dynamics of isotopic ratios in general. We developed a mechanistic framework using a dynamic mixing model (DMM) to assess the contribution of λ to the dynamics of isotopic incorporation and to estimate the bias induced by neglecting the time lag in diet reconstruction in conventional static mixing models (SMMs). The DMM includes isotope dynamics of sources (denoted δs), λ and frequency of diet-switch (ω). The results showed a significant bias generated by the SMM compared to the DMM (up to 50% of differences). This bias can be strongly reduced in SMMs by averaging the isotopic variations of the food sources over a time window equal to twice the isotopic half-life. However, the bias will persist (∼15%) for intermediate values of the ω/λ ratio. The inferences generated using a case study highlighted that DMM enhanced estimates of consumer's diet, and this could avoid misinterpretation in ecosystem functioning, food-web structure analysis and underlying biological processes.

Extensive spatial impacts of oyster reefs on an intertidal mudflat community via predator facilitation.

Habitat engineers make strong and far-reaching imprints on ecosystem processes. In intertidal mudflats, the dominant primary producer, microphytobenthos (MPB), often forms high biomass patches around oyster reefs. We evaluate multiple hypotheses linking MPB with oyster reefs, including oyster biodeposition, meiofaunal grazing, and abiotic factors, aiming to help predict effects of reef removal or proliferation. We quantify spatial patterns of an Atlantic mudflat community and its environment around two large Crassostrea reefs before experimentally sacrificing one reef via burning. MPB biomass was enriched surrounding living oyster reefs although infaunal biomass and individual sizes were low. Structural equation modelling best supported the hypothesis that crab predation intensity, which decayed with distance from the reefs, locally freed MPB from grazing. Our results suggest that Crassostrea reef expansion may enrich local MPB patches and redirect trophic energy flows away from mudflat infauna, with potential implications for the sustainability of local fisheries and bird conservation.

The impact of aquaculture on the genetics and distribution of the onuphid annelid Diopatra biscayensis.

AIM: Evolutionary history of natural populations can be confounded by human intervention such as the case of decorator worm species Diopatra (Onuphidae), which have a history of being transported through anthropogenic activities. Because they build tubes and act as ecosystem engineers, they can have a large impact on the overall ecosystem in which they occur. One conspicuous member, Diopatra biscayensis, which was only described in 2012, has a fragmented distribution that includes the Bay of Biscay and the Normanno-Breton Gulf in the English Channel. This study explores the origin of these worms in the Normanno-Breton region, which has been debated to either be the result of a historic range contraction from a relic continuous population or a more recent introduction. LOCATION: Northeastern Atlantic, the Bay of Biscay, and the Normanno-Breton Gulf. METHODS: We utilized a RAD-tag-based SNP approach to create a reduced genomic data set to recover fine-scale population structure and infer which hypothesis best describes the D. biscayensis biogeographic distribution. The reduced genomic data set was used to calculate standard genetic diversities and genetic differentiation statistics, and utilized various clustering analyses, including PCAs, DAPC, and admixture. RESULTS: Clustering analyses were consistent with D. biscayensis as a single population spanning the Bay of Biscay to the Normanno-Breton Gulf in the English Channel, although unexpected genetic substructure was recovered from Arcachon Bay, in the middle of its geographic range. Consistent with a hypothesized introduction, the isolated Sainte-Anne locality in the Normanno-Breton Gulf was recovered to be a subset of the diversity found in the rest of the Bay of Biscay. MAIN CONCLUSIONS: These results are congruent with previous simulations that did not support connectivity from the Bay of Biscay to the Normanno-Breton Gulf by natural dispersal. These genomic findings, with support from previous climatic studies, further support the hypothesis that D. biscayensis phylogeographic connectivity is the result of introductions, likely through the regions' rich shellfish aquaculture, and not of a historically held range contraction.

Environmental optima for an ecosystem engineer: a multidisciplinary trait-based approach.

A complex interplay of biotic and abiotic factors underpins the distribution of species and operates across different levels of biological organization and life history stages. Understanding ecosystem engineer reproductive traits is critical for comprehending and managing the biodiversity-rich habitats they create. Little is known about how the reproduction of the reef-forming worm, Sabellaria alveolata, varies across environmental gradients. By integrating broad-scale environmental data with in-situ physiological data in the form of biochemical traits, we identified and ranked the drivers of intraspecific reproductive trait variability (ITV). ITV was highest in locations with variable environmental conditions, subjected to fluctuating temperature and hydrodynamic conditions. Our trait selection pointed to poleward sites being the most physiologically stressful, with low numbers of irregularly shaped eggs suggesting potentially reduced reproductive success. Centre-range individuals allocated the most energy to reproduction, with the highest number of intermediate-sized eggs, whilst equatorward sites were the least physiologically stressful, thus confirming the warm-adapted nature of our model organism. Variation in total egg diameter and relative fecundity were influenced by a combination of environmental conditions, which changed depending on the trait and sampling period. An integrated approach involving biochemical and reproductive traits is essential for understanding macro-scale patterns in the face of anthropogenic-induced climate change across environmental and latitudinal gradients.

On the diversity and distribution of a data deficient habitat in a poorly mapped region: The case of Sabellaria alveolata L. in Ireland.

Data that can be used to monitor biodiversity through time are essential for conservation and management. The reef-forming worm, Sabellaria alveolata (L. 1767) is currently classed as 'Data Deficient' due to an imbalance in the spread of data on its distribution. Little is known about the distribution of this species around Ireland. Using data archaeology, we collated past and present distribution records and discovered that S. alveolata has a discontinuous distribution with large gaps between populations. Many regions lack data and should be targeted for sampling. Biodiversity surveys revealed that S. alveolata supported diverse epibiotic algal communities. Retrograding (declining) reefs supported greater infaunal diversity than prograding (growing) reefs or sand, suggesting that S. alveolata is a dynamic ecosystem engineer that has a lasting legacy effect. Similar research should be carried out for other Data Deficient species, habitats and regions. Such data are invaluable resources for management and conservation.

Linking multiple facets of biodiversity and ecosystem functions in a coastal reef habitat.

Reef-building species play key roles in promoting local species richness and regulating ecosystem functions like biogeochemical fluxes. We evaluated the functioning of a habitat engineered by the reef-building polychaete Sabellaria alveolata, by measuring oxygen and nutrient fluxes in the reef structures and in the soft-sediments nearby. Then, we investigated the relative importance of temperature, the engineer S. alveolata, and different facets of macrofauna diversity (taxonomic, functional diversity and identity), on the reef biogeochemical fluxes using multiple linear regressions and effect sizes. The reef fluxes were more intense than the soft-sediment fluxes and mainly driven by the engineer biomass and abundance, stressing the importance of these biogenic structures. Higher water temperatures and an intermediate level of associated macrofauna functional dispersion weighted only by abundance (i.e. intermediate biological trait variability) maximized the reef's global biogeochemical functioning. Ultimately, the physical degradation of the reefs could lead to lower levels of functioning.

Functional roles of an engineer species for coastal benthic invertebrates and demersal fish.

Through their tissues or activities, engineer species create, modify, or maintain habitats and alter the distribution and abundance of many plants and animals. This study investigates key ecological functions performed by an engineer species that colonizes coastal ecosystems. The gregarious tubiculous amphipod Haploops nirae is used as a biological model. According to previous studies, the habitat engineered by H. nirae (i.e., Haploops habitat) could provide food and natural shelter for several benthic species such as benthic diatoms belonging to the gender Navicula, the micrograzer Geitodoris planata, or the bivalve Polititapes virgineus. Using data from scientific surveys conducted in two bays, this study explored whether (1) the Haploops sandy-mud community modifies invertebrate and ichthyologic community structure (diversity and biomass); (2) H. nirae creates a preferential feeding ground; and (3) this habitat serves as a refuge for juvenile fish. Available Benthic Energy Coefficients, coupled with more traditional diversity indices, indicated higher energy available in Haploops habitat than in two nearby habitats (i.e., Sternaspis scutata and Amphiura filiformis/Owenia fusiformis habitats). The use of isotopic functional indices (IFIs) indicated (1) a higher functional richness in the Haploops habitat, related to greater diversity in food sources and longer food chains; and (2) a higher functional divergence, associated with greater consumption of a secondary food source. At the invertebrate-prey level, IFIs indicated little specialization and little trophic redundancy in the engineered habitat, as expected for homogenous habitats. Our results partly support empirical knowledge about engineered versus nonengineered habitats and also add new perspectives on habitat use by fish and invertebrate species. Our analyses validated the refuge-area hypothesis for a few fish species. Although unique benthic prey assemblages are associated with Haploops habitat, the hypothesis that it is a preferential feeding area was not verified. However, specialist feeding behavior was observed for predators, which calls for further investigation.

Lipid remodelling in the reef-building honeycomb worm, Sabellaria alveolata, reflects acclimation and local adaptation to temperature.

Acclimation and adaptation, which are key to species survival in a changing climate, can be observed in terms of membrane lipid composition. Remodelling membrane lipids, via homeoviscous adaptation (HVA), counteracts membrane dysfunction due to temperature in poikilotherms. In order to assess the potential for acclimation and adaptation in the honeycomb worm, Sabellaria alveolata, a reef-building polychaete that supports high biodiversity, we carried out common-garden experiments using individuals from along its latitudinal range. Individuals were exposed to a stepwise temperature increase from 15 °C to 25 °C and membrane lipid composition assessed. Our results suggest that S. alveolata was able to acclimate to higher temperatures, as observed by a decrease in unsaturation index and 20:5n-3. However, over the long-term at 25 °C, lipid composition patterns are not consistent with HVA expectations and suggest a stress response. Furthermore, unsaturation index of individuals from the two coldest sites were higher than those from the two warmest sites, with individuals from the thermally intermediate site being in-between, likely reflecting local adaptation to temperature. Therefore, lipid remodelling appears limited at the highest temperatures in S. alveolata, suggesting that individuals inhabiting warm environments may be close to their upper thermal tolerance limits and at risk in a changing climate.

Food-Web Complexity in Guaymas Basin Hydrothermal Vents and Cold Seeps.

In the Guaymas Basin, the presence of cold seeps and hydrothermal vents in close proximity, similar sedimentary settings and comparable depths offers a unique opportunity to assess and compare the functioning of these deep-sea chemosynthetic ecosystems. The food webs of five seep and four vent assemblages were studied using stable carbon and nitrogen isotope analyses. Although the two ecosystems shared similar potential basal sources, their food webs differed: seeps relied predominantly on methanotrophy and thiotrophy via the Calvin-Benson-Bassham (CBB) cycle and vents on petroleum-derived organic matter and thiotrophy via the CBB and reductive tricarboxylic acid (rTCA) cycles. In contrast to symbiotic species, the heterotrophic fauna exhibited high trophic flexibility among assemblages, suggesting weak trophic links to the metabolic diversity of chemosynthetic primary producers. At both ecosystems, food webs did not appear to be organised through predator-prey links but rather through weak trophic relationships among co-occurring species. Examples of trophic or spatial niche differentiation highlighted the importance of species-sorting processes within chemosynthetic ecosystems. Variability in food web structure, addressed through Bayesian metrics, revealed consistent trends across ecosystems. Food-web complexity significantly decreased with increasing methane concentrations, a common proxy for the intensity of seep and vent fluid fluxes. Although high fluid-fluxes have the potential to enhance primary productivity, they generate environmental constraints that may limit microbial diversity, colonisation of consumers and the structuring role of competitive interactions, leading to an overall reduction of food-web complexity and an increase in trophic redundancy. Heterogeneity provided by foundation species was identified as an additional structuring factor. According to their biological activities, foundation species may have the potential to partly release the competitive pressure within communities of low fluid-flux habitats. Finally, ecosystem functioning in vents and seeps was highly similar despite environmental differences (e.g. physico-chemistry, dominant basal sources) suggesting that ecological niches are not specifically linked to the nature of fluids. This comparison of seep and vent functioning in the Guaymas basin thus provides further supports to the hypothesis of continuity among deep-sea chemosynthetic ecosystems.

Population structure and spread of the polychaete Diopatra biscayensis along the French Atlantic coast: human-assisted transport by-passes larval dispersal.

Intertidal populations of the ecosystem engineering polychaete, Diopatra biscayensis, were analyzed on the French Atlantic coast for three years with individual size estimated from tube-cap aperture. All but the northernmost population along the Bay of Biscay have yearly recruitment. Individuals live 3-5 years and are likely reproductive as one year olds. Simulations indicate dispersal distances are <50 km; yet, populations also exist within the Normano-Breton Gulf in the western English Channel, more than 450 km from the northernmost Bay of Biscay population at La Trinité-sur-Mer. Three of the four populations in the Normano-Breton Gulf have no young of the year, but are near to active mussel culture where mussel seed is transported on ropes from dense D. biscayensis areas in the Vendée-Charente region in the Bay of Biscay. The majority of D. biscayensis were adjacent to the likely source, mussel seed ropes. Transport assisted by aquaculture is the likely explanation for the populations in the Normano-Breton Gulf.

Isotopic diversity indices: how sensitive to food web structure?

Recently revisited, the concept of niche ecology has lead to the formalisation of functional and trophic niches using stable isotope ratios. Isotopic diversity indices (IDI) derived from a set of measures assessing the dispersion/distribution of points in the δ-space were recently suggested and increasingly used in the literature. However, three main critics emerge from the use of these IDI: 1) they fail to account for the isotopic sources overlap, 2) some indices are highly sensitive to the number of species and/or the presence of rare species, and 3) the lack of standardization prevents any spatial and temporal comparisons. Using simulations we investigated the ability of six commonly used IDI to discriminate among different trophic food web structures, with a focus on the first two critics. We tested the sensitivity of the IDI to five food web structures along a gradient of sources overlap, varying from two distinct food chains with differentiated sources to two superimposed food chains sharing two sources. For each of the food web structure we varied the number of species (from 10 to 100 species) and the type of species feeding behaviour (i.e. random or selective feeding). Values of IDI were generally larger in food webs with distinct basal sources and tended to decrease as the superimposition of the food chains increased. This was more pronounced when species displayed food preferences in comparison to food webs where species fed randomly on any prey. The number of species composing the food web also had strong effects on the metrics, including those that were supposedly less sensitive to small sample size. In all cases, computing IDI on food webs with low numbers of species always increases the uncertainty of the metrics. A threshold of ~20 species was detected above which several metrics can be safely used.

Ephemeral bio-engineers or reef-building polychaetes: how stable are aggregations of the tube worm Lanice conchilega (Pallas, 1766)?

Dense aggregations of tube-worms can stabilize sediments and generate oases for benthic communities that are different and often more diverse and abundant than those of the surroundings. If these features are to qualify as biogenic reefs under nature-conservation legislation such as the EC Habitats Directive, a level of stability and longevity is desirable aside from physical and biological attributes. Lanice conchilega (Pallas, 1766) is widely distributed around the European coast and aggregations of this tube-dwelling polychaete are known to have a positive effect on the biodiversity of associated species in inter- and sub-tidal areas. This increases the value of L. conchilega-rich habitats for higher trophic levels such as birds and fish. However, L. conchilega is currently not recognized as a reef builder primarily due to uncertainty about the stability of their aggregations. We carried out three studies on different spatial and temporal scales to explore a number of properties relating to stability: (1) Individual aggregations of L. conchilega of ∼1 m(2) were monitored for up to 1 year, (2) records of L. conchilega from a 258-ha area over a 35-year period were analyzed, (3) the recovery of a population of L. conchilega subjected to disturbances by cultivation of Manila clams (Ruditapes philippinarum) was followed over 3 years. The studies provided evidence about the longevity of L. conchilega aggregations, their resistance to disturbance, their resilience in recovering from negative impact and their large-scale persistence. The results showed that populations of L. conchilega were prone to considerable fluctuation and the stability of aggregations depended on environmental factors and on recruitment. The tube-worms proved to be susceptible to disturbance by cultivation of Manila clams but demonstrated the potential to recover from that impact. The long-term monitoring of a large L. conchilega population in the Bay of Mont Saint Michel (France) indicated that aggregations can persist over many decades with a constant, densely populated core area and an expanding and contracting more thinly populated fringe zone. The stability of aggregations of L. conchilega and the structures they form do not unequivocally fit the currently accepted definition of a reef. However, given L. conchilega's accepted reef-like potential to influence diversity and abundance in benthic communities, we suggest clarifying and expanding the definition of reefs so that species with records of significant persistence in particular areas and which otherwise meet expectations of reefs are included within the definition.