The high biodiversity of benthic organisms in a coastal ecosystem revealed by an integrative approach / A alta biodiversidade de organismos bentônicos em um ecossistema costeiro revelada por uma abordagem integrativa

Abstract Increasing habitat modification and species loss demand consistent efforts to describe and understand biodiversity patterns. The BIOTA/FAPESP Program was created in this context and it has been a successful initiative to promote studies on biodiversity and conservation in Brazil. The BIOTA/Araçá is an interdisciplinary project that provided a detailed evaluation of the biodiversity of Araçá Bay, a coastal seascape located on the North coast of the state of São Paulo, Southeast Brazil. The bay encompasses multiple habitats, such as beaches, mangroves, rocky shores, and a tidal flat, and provides important ecosystem services. Unfortunately, the bay is the subject of complex social-environmental conflicts that oppose economic, social, and environmental demands (i.e., the expansion of neighboring harbor activities vs. small-scale artisanal fisheries and protection of biodiversity). The present study presents a survey of the benthic species occurring in the different habitats of Araçá Bay, including data obtained during the BIOTA/Araçá project and previous assessments of the area. The benthic species play an important role in marine environments and studying the diversity of these organisms that live associated with the bottom is indispensable for comprehending the environment's functioning. The macrofauna, meiofauna, and microorganisms associated with soft and hard bottom were listed, and additional information, such as the habitat and geographical distribution, were provided for each species. The checklist includes 826 species, almost 70% recorded during the BIOTA/Araçá project. The most speciose taxa were the annelids (225 spp.), mollusks (194 spp.), and crustaceans (177 spp.). Seven benthic species are endemic to Araçá Bay, 14 are considered threatened, and seven are economically exploited. Furthermore, the bay is the type locality of many taxa, and 11 new benthic species were described based on specimens sampled during the project. This project shows the importance of Araçá Bay as a unique biologically rich environment and highlights the need for conservation efforts in light of the current threats.

Resumo O aumento da modificação dos habitats e da perda de espécies demanda esforços consistentes para descrever e compreender os padrões de biodiversidade. O programa BIOTA/FAPESP foi criado nesse contexto e é uma iniciativa de sucesso para promover estudos em biodiversidade e conservação no Brasil. O BIOTA/Araçá é um projeto interdisciplinar que promoveu uma avaliação detalhada da biodiversidade da Baía do Araçá, um ecossistema costeiro localizado ao Norte do estado de São Paulo, Sudeste do Brasil. A baía engloba múltiplos habitats, tais como praias, manguezais, costões rochosos, e uma planície de maré, e também fornece importantes serviços ecossistêmicos. Infelizmente, a baía está sujeita à conflitos sócio-ambientais complexos que contrastam demandas econômicas, sociais e ambientais (i.e. a expansão das atividades do porto vizinho vs. a pesca artesanal de pequena escala e a proteção da biodiversidade). O presente estudo apresenta um levantamento das espécies bentônicas que ocorrem nos diferentes habitats da Baía do Araçá, incluindo dados obtidos durante o projeto BIOTA/Araçá e de investigações realizadas anteriormente na área. As espécies bentônicas desempenham um papel importante no ambiente marinho, e estudar a diversidade desses organismos que vivem associados ao fundo é indispensável para compreender o funcionamento do meio ambiente. A macrofauna, meiofauna, e microorganismos associados aos fundos consolidado e inconsolidado foram listados, e informações adicionais foram fornecidas para cada espécie, tais como a distribuição geográfica e nos habitats. O checklist inclui 826 espécies, quase 70% registradas durante o projeto BIOTA/Araçá. Os taxa mais especiosos foram os anelídeos (225 spp.), moluscos (194 spp.), e crustáceos (177 spp.). Entre as espécies bentônicas listadas, sete são endêmicas da Baía do Araçá, 14 são consideradas ameaçadas de extinção, e sete são exploradas economicamente. A baía é a localidade tipo de vários taxa, e 11 novas espécies bentônicas foram descritas com base em espécimes amostrados durante o projeto. Este projeto mostra a importância da Baía do Araçá como um ambiente de riqueza biológica única e demonstra a necessidade de esforços para a sua conservação considerando as atuais ameaças.

The efficacy of benthic indices to evaluate the ecological quality and urbanization effects on sandy beach ecosystems.

Benthic indices have been widely used across different coastal ecosystems to assess ecological quality and detect anthropic impacts, but very few studies investigated their effectiveness on sandy beaches. Here, we evaluated and compared the efficacy of 12 assemblage-based benthic indices in assessing ecological quality in beaches, across a gradient of anthropic pressure and natural variability in 90 sandy beach sites. Overall, when sandy beaches were considered collectively, benthic indices had a poor performance in identifying decreases in ecological quality with increasing urbanization. However, when each morphodynamic type was evaluated separately, a few indices, especially those that were calibrated by reference conditions (i.e., M-AMBI, BAT, and BEQI-2), showed promising results for dissipative, and to a lesser extent, intermediate beaches. For reflective beaches, indices performed poorly, likely a reflection of the stronger natural disturbance these beaches are subjected to. Among functional indices, richness was found to be lower in urbanized beaches, but only in dissipative ones. Overall, our results show that benthic indices have the potential to be incorporated in sandy beach management and monitoring programs, especially for dissipative and intermediate beaches. For reflective beaches, given the early stage of studies with benthic indices in beaches, more research is needed to corroborate the observed patterns.

Does coastal armoring affect biodiversity and its functional composition on sandy beaches?

Sandy beaches are increasingly squeezed due to the construction of backshore man-made structures (i.e., coastal armoring) and current global changes. Coastal armoring impacts beach sediment dynamics, inducing erosion and habitat loss, threatening biodiversity processes and the functional roles of sandy beach organisms. Here, we examine how the abundance, taxonomic richness, and functional richness of sandy beach fauna are affected by coastal armoring. We compared macrobenthic infaunal communities on five armored beaches (with backshore urban structures) and five vegetated beaches (not-armored). We also evaluated the abundance and biomass of upper-beach arthropods using pitfall traps, comparing armored and vegetated segments within the beaches. Infaunal richness and abundance were lower at armored beaches, mainly in the subtidal zones, because of a reduction in polychaete and molluscan abundance. There was no difference in overall functional richness between the armored and vegetated beaches. Nevertheless, we found that functional groups such as small suspension feeders were more associated with armored beaches, while large-bodied species and predators were more frequent at vegetated beaches. Pitfall traps showed that coastal armoring also reduced the abundance of the upper-beach coleopteran Phaleria testacea, leading to a loss of biomass. Therefore, our data suggest that coastal armoring can influence the functional composition of sandy beach biodiversity and significantly impact macrobenthic abundance and biomass.

Evaluation of the effects of urbanization and environmental features on sandy beach macrobenthos highlights the importance of submerged zones.

To assess how sandy beach biodiversity is influenced by the effects of environmental features and urbanization, we sampled the macrofauna in the whole across-shore gradient of 90 beach sites in Southeast Brazil. We found that morphodynamic features were the main drivers of macrobenthos, but urbanization-related variables, such as number of beachgoers and number of constructions on the upper shore, decreased species richness and biomass. We also found that submerged zones sustained the highest number of species and biomass in the across-shore gradient, but were the most impacted by human activities. By demonstrating the ecological importance of submerged zones, our results show that beach management practices, which are mainly focused on the upper shore, are missing important components of beach biodiversity. To secure the sustainability of beach ecosystems, management initiatives should include both their social and ecological components and consider the entire Littoral Active Zone as the proper management unit.

Nestedness patterns and the role of morphodynamics and spatial distance on sandy beach fauna: ecological hypotheses and conservation strategies.

Sandy beach fauna is hypothesized to be mainly structured by environmental variables. As such, it is expected that morphodynamic characteristics are limiting factors, and the species pool inhabiting harsher reflective beaches would be a subset of (i.e., nested in) the fauna of nearby dissipative beaches. We investigated the existence of a nestedness pattern in sandy beach assemblages, as well as the contribution of environmental and spatial variables (i.e., factors that potentially affect an assemblage regardless of environmental conditions - typically related to distance between sites and dispersal of organisms) on sandy beach macrobenthic fauna. Dissipative beaches had higher species richness than reflective beaches but we found no nestedness pattern. Furthermore, almost every beach showed exclusive species. Spatial variables exerted stronger influence on macrobenthic assemblages than local environmental variables. Our results therefore suggest that local and small-scale recruitment is the predominant process structuring macrobenthic assemblages. These results bring important implications for sandy beach conservation: given that spatial distance is an important factor structuring macrobenthic fauna and different sandy beaches harbor different pools of species, conservation programs need to focus on sandy beaches across large spatial scales and with varied morphodynamic characteristics in order to preserve coastal biodiversity.

When time affects space: Dispersal ability and extreme weather events determine metacommunity organization in marine sediments.

Community ecology has traditionally assumed that the distribution of species is mainly influenced by environmental processes. There is, however, growing evidence that environmental (habitat characteristics and biotic interactions) and spatial processes (factors that affect a local assemblage regardless of environmental conditions - typically related to dispersal and movement of species) interactively shape biological assemblages. A metacommunity, which is a set of local assemblages connected by dispersal of individuals, is spatial in nature and can be used as a straightforward approach for investigating the interactive and independent effects of both environmental and spatial processes. Here, we examined (i) how environmental and spatial processes affect the metacommunity organization of marine macroinvertebrates inhabiting the intertidal sediments of a biodiverse coastal ecosystem; (ii) whether the influence of these processes is constant through time or is affected by extreme weather events (storms); and (iii) whether the relative importance of these processes depends on the dispersal abilities of organisms. We found that macrobenthic assemblages are influenced by each of environmental and spatial variables; however, spatial processes exerted a stronger role. We also found that this influence changes through time and is modified by storms. Moreover, we observed that the influence of environmental and spatial processes varies according to the dispersal capabilities of organisms. More effective dispersers (i.e., species with planktonic larvae) are more affected by spatial processes whereas environmental variables had a stronger effect on weaker dispersers (i.e. species with low motility in larval and adult stages). These findings highlight that accounting for spatial processes and differences in species life histories is essential to improve our understanding of species distribution and coexistence patterns in intertidal soft-sediments. Furthermore, it shows that storms modify the structure of coastal assemblages. Given that the influence of spatial and environmental processes is not consistent through time, it is of utmost importance that future studies replicate sampling over different periods so the influence of temporal and stochastic factors on macrobenthic metacommunities can be better understood.

Unraveling the performance of the benthic index AMBI in a subtropical bay: The effects of data transformations and exclusion of low-reliability sites.

We investigated the relationship between the AMBI index and different contamination proxies in an urbanized bay in South America (SE Brazil), and the effect of (a) abundance data transformation and (b) exclusion of low-reliability sites (high SD; low N) on the index' performance. Poor ecological quality and opportunistic species were related to an increase in contaminants concentrations and mud content. Good ecological status and sensitive species (EG I) were mainly related to increased hydrodynamics. Data transformation caused minimal changes to the overall relationships, but exclusion of low-reliability sites improved the relationship between ecological groups and contamination proxies. Our results show that AMBI is robust in detecting effects of different contaminants in the area and reinforce the importance of the index as a tool for coastal management, but local joint efforts are needed to improve and adjust local species classification in ecological groups to improve the index' performance.

Storm effects on intertidal invertebrates: increased beta diversity of few individuals and species.

Climate change is predicted to lead to more extreme weather events, including changes to storm frequency, intensity and location. Yet the ecological responses to storms are incompletely understood for sandy shorelines, the globe's longest land-ocean interface. Here we document how storms of different magnitude impacted the invertebrate assemblages on a tidal flat in Brazil. We specifically tested the relationships between wave energy and spatial heterogeneity, both for habitat properties (habitat heterogeneity) and fauna (ß-diversity), predicting that larger storms redistribute sediments and hence lead to spatially less variable faunal assemblages. The sediment matrix tended to become less heterogeneous across the flat after high-energy wave events, whereas ß-diversity increased after storms. This higher ß-diversity was primarily driven by species losses. Significantly fewer species at a significantly lower density occurred within days to weeks after storms. Negative density and biomass responses to storm events were most prominent in crustaceans. Invertebrate assemblages appeared to recover within a short time (weeks to months) after storms, highlighting that most species typical of sedimentary shorelines are, to some degree, resilient to short-term changes in wave energy. Given that storm frequency and intensity are predicted to change in the coming decades, identifying properties that determine resilience and recovery of ecosystems constitute a research priority for sedimentary shorelines and beyond.