The Tree of Life eDNA metabarcoding reveals a similar taxonomic richness but dissimilar evolutionary lineages between seaports and marine reserves.

Coastal areas host a major part of marine biodiversity but are seriously threatened by ever-increasing human pressures. Transforming natural coastlines into urban seascapes through habitat artificialization may result in loss of biodiversity and key ecosystem functions. Yet, the extent to which seaports differ from nearby natural habitats and marine reserves across the whole Tree of Life is still unknown. This study aimed to assess the level of α and ß-diversity between seaports and reserves, and whether these biodiversity patterns are conserved across taxa and evolutionary lineages. For that, we used environmental DNA (eDNA) metabarcoding to survey six seaports on the French Mediterranean coast and four strictly no-take marine reserves nearby. By targeting four different groups-prokaryotes, eukaryotes, metazoans and fish-with appropriate markers, we provide a holistic view of biodiversity on contrasted habitats. In the absence of comprehensive reference databases, we used bioinformatic pipelines to gather similar sequences into molecular operational taxonomic units (MOTUs). In contrast to our expectations, we obtained no difference in MOTU richness (α-diversity) between habitats except for prokaryotes and threatened fishes with higher diversity in reserves than in seaports. However, we observed a marked dissimilarity (ß-diversity) between seaports and reserves for all taxa. Surprisingly, this biodiversity signature of seaports was preserved across the Tree of Life, up to the order. This result reveals that seaports and nearby marine reserves share few taxa and evolutionary lineages along urbanized coasts and suggests major differences in terms of ecosystem functioning between both habitats.

Early signals of Posidonia oceanica meadows recovery in a context of wastewater treatment improvements.

Natural ecological restoration is a cornerstone of modern conservation science and managers need more documented "success stories" to lead the way. In French mediterranean sea, we monitored Posidonia oceanica lower limit using acoustic telemetry and photogrammetry and investigated the descriptors driving its variations, at a national scale and over more than a decade. We showed significant effects of environmental descriptors (region, sea surface temperature and bottom temperature) but also of wastewater treatment plant (WWTP) effluents proxies (size of WWTP, time since conformity, and distance to the closest effluent) on the meadows lower limit progression. This work indicates a possible positive response of P. oceanica meadows to improvements in wastewater treatment and a negative effect of high temperatures. While more data is needed, the example of French wastewater policy should inspire stakeholders and coastal managers in their efforts to limit anthropogenic pressures on vulnerable ecosystems.

Anchoring pressure and the effectiveness of new management measures quantified using AIS data and a mobile application.

Large boats can have a major impact on sensitive marine habitats like seagrass meadows when anchoring. The anchoring preference of large boats and their impacts can be mapped using Automatic Identification System (AIS). We found a constant increase in the number of anchoring events with, until recently, a large part of them within the protected Posidonia oceanica seagrass meadows. French authorities adopted a new regulation in 2019 forbidding any anchoring within P. oceanica seagrass meadows for boats larger than 24 m. The number of large ships (>24 m) anchoring in P. oceanica meadows significantly decreased after the enforcement of the regulation. The surface of avoided impact thanks to the new regulation corresponds to 134 to 217 tons of carbon sequestered by the preserved meadow in 2022. This work illustrates that a strict regulation of anchoring, based on accurate habitat maps, is effective in protecting seagrass meadows.

Biogeography of acoustic biodiversity of NW Mediterranean coralligenous reefs.

Monitoring the biodiversity of key habitats and understanding the drivers across spatial scales is essential for preserving ecosystem functions and associated services. Coralligenous reefs are threatened marine biodiversity hotspots that are challenging to monitor. As fish sounds reflect biodiversity in other habitats, we unveiled the biogeography of coralligenous reef sounds across the north-western Mediterranean using data from 27 sites covering 2000 km and 3 regions over a 3-year period. We assessed how acoustic biodiversity is related to habitat parameters and environmental status. We identified 28 putative fish sound types, which is up to four times as many as recorded in other Mediterranean habitats. 40% of these sounds are not found in other coastal habitats, thus strongly related to coralligenous reefs. Acoustic diversity differed between geographical regions. Ubiquitous sound types were identified, including sounds from top-predator species and others that were more specifically related to the presence of ecosystem engineers (red coral, gorgonians), which are key players in maintaining habitat function. The main determinants of acoustic community composition were depth and percentage coverage of coralligenous outcrops, suggesting that fish-related acoustic communities exhibit bathymetric stratification and are related to benthic reef assemblages. Multivariate analysis also revealed that acoustic communities can reflect different environmental states. This study presents the first large-scale map of acoustic fish biodiversity providing insights into the ichthyofauna that is otherwise difficult to assess because of reduced diving times. It also highlights the potential of passive acoustics in providing new aspects of the correlates of biogeographical patterns of this emblematic habitat relevant for monitoring and conservation.

Environmental DNA metabarcoding reveals and unpacks a biodiversity conservation paradox in Mediterranean marine reserves.

Although we are currently experiencing worldwide biodiversity loss, local species richness does not always decline under anthropogenic pressure. This conservation paradox may also apply in protected areas but has not yet received conclusive evidence in marine ecosystems. Here, we survey fish assemblages in six Mediterranean no-take reserves and their adjacent fishing grounds using environmental DNA (eDNA) while controlling for environmental conditions. We detect less fish species in marine reserves than in nearby fished areas. The paradoxical gradient in species richness is accompanied by a marked change in fish species composition under different managements. This dissimilarity is mainly driven by species that are often overlooked by classical visual surveys but detected with eDNA: cryptobenthic, pelagic, and rare fishes. These results do not negate the importance of reserves in protecting biodiversity but shed new light on how under-represented species groups can positively react to fishing pressure and how conservation efforts can shape regional biodiversity patterns.

Species diversity and composition drive the aesthetic value of coral reef fish assemblages.

Cultural and recreational values of biodiversity are considered as important dimensions of nature's contribution to people. Among these values, the aesthetics can be of major importance as the appreciation of beauty is one of the simplest forms of human emotional response. Using an online survey, we disentangled the effects of different facets of biodiversity on aesthetic preferences of coral reef fish assemblages that are among the most emblematic assemblages on Earth. While we found a positive saturating effect of species' richness on human preference, we found a net negative effect of species abundance, no effect of species functional diversity and contrasting effects of species composition depending on species' attractiveness. Our results suggest that the biodiversity-human interest relationship is more complex than has been previously stated. By integrating several scales of organization, our study is a step forward in better evaluating the aesthetic value of biodiversity.

Integrating the aesthetic value of landscapes and biological diversity.

As a cultural ecosystem service, the aesthetic value of landscapes contributes to human well-being, but studies linking biodiversity and ecosystem services generally do not account for this particular service. Therefore, congruence between the aesthetic perception of landscapes, ecological value and biodiversity remains poorly understood. Here, we describe the conceptual background, current methodologies and future challenges of assessing landscape aesthetics and its relationship with biodiversity. We highlight the methodological gaps between the assessment of landscape aesthetics, ecological diversity and functioning. We discuss the challenges associated with connecting landscape aesthetics with ecological value, and the scaling issues in the assessment of human aesthetics perception. To better integrate aesthetic value and ecological components of biodiversity, we propose to combine the study of aesthetics and the understanding of ecological function at both the species and landscape levels. Given the urgent need to engage society in conservation efforts, this approach, based on the combination of the aesthetic experience and the recognition of ecological functioning by the general public, will help change our culture of nature and promote ecologically oriented conservation policies.

Confronting species aesthetics with ecological functions in coral reef fish.

The biodiversity crisis has spurred scientists to assess all facets of biodiversity so that stakeholders can establish protection programs. However, species that are perceived as beautiful receive more attention than less attractive species. This dynamic could have tremendous consequences on people's willingness to preserve biodiversity. Coral reefs might be particularly affected by this issue as they are key ecosystems that provide many services, such as aesthetic and cultural benefits attracting millions of tourists each year. Here we show the results of an online photographic questionnaire completed by 8,000 participants whereby preferences were assessed for a set of 116 reef fishes. Based on these preferences, we compared the functional richness, i.e. the amount of functional space filled, by groups of fishes based on their perceived attractiveness. We present evidence indicating that the least attractive coral reef fishes have a much higher functional richness than the most attractive species. Our results highlight the extent to which species aesthetic values' may be disconnected from their ecological values and could be misleading for conservation purposes. There is thus an urgent need to increase the attention of scientists and the general public towards less attractive species to better appreciate and protect the species that crucially support functional diversity in endangered ecosystems.

Boat anchoring pressure on coastal seabed: Quantification and bias estimation using AIS data.

Global shipping is economically important, but has many adverse environmental effects. Anchoring contributes greatly to this adverse impact, as it is responsible for mechanical disturbance of highly sensitive marine habitats. Recovery of these ecosystems is limited by slow regrowth. Anchoring pressure on coastal seabed habitats was estimated using AIS (Automatic Identification System) data along 1800km of Mediterranean coastline between 2010 and 2015. A comparison with field observations showed that these results were most consistent for large boats (>50m). An analysis of AIS data coupled with a seabed map showed that around 30% of the habitats between 0 and -80m exhibited anchoring pressure. Posidonia oceanica seagrass beds were the most impacted habitat in terms of duration. This methodology efficiently estimates spatial and temporal anchoring pressure principally due to large boats and should interest managers of marine protected areas as much as coastline managers.

Taxonomic and functional diversity increase the aesthetic value of coralligenous reefs.

The aesthetic value of landscapes contributes to human well-being. However, studies which have investigated the link between biodiversity and ecosystem services have not taken aesthetic value into account. In this study we evaluated how the aesthetics of coralligenous reefs, a key marine ecosystem in the Mediterranean, is perceived by the general public and how aesthetic preferences are related to biodiversity facets (taxonomic, phylogenetic and functional diversities). We performed both biodiversity measures and online-surveys of aesthetic perception on photographic quadrats sampled along the French Mediterranean coast. Our results show that species richness and functional richness have a significant positive effect on aesthetic value. Most of the ecological literature, exploring the relationship between biodiversity and ecosystem functioning and service has focused so far on 'economical' aspects of biodiversity (provision or regulation). Our results illustrate that cultural facets, such as 'beauty', should also be central in our motivations to preserve ecological diversity.

Fine-Scale Cartography of Human Impacts along French Mediterranean Coasts: A Relevant Map for the Management of Marine Ecosystems.

Ecosystem services provided by oceans and seas support most human needs but are threatened by human activities. Despite existing maps illustrating human impacts on marine ecosystems, information remains either large-scale but rough and insufficient for stakeholders (1 km² grid, lack of data along the coast) or fine-scale but fragmentary and heterogeneous in methodology. The objectives of this study are to map and quantify the main pressures exerted on near-coast marine ecosystems, at a large spatial scale though in fine and relevant resolution for managers (one pixel = 20 x 20 m). It focuses on the French Mediterranean coast (1,700 km of coastline including Corsica) at a depth of 0 to 80 m. After completing and homogenizing data presently available under GIS on the bathymetry and anthropogenic pressures but also on the seabed nature and ecosystem vulnerability, we provide a fine modeling of the extent and impacts of 10 anthropogenic pressures on marine habitats. The considered pressures are man-made coastline, boat anchoring, aquaculture, urban effluents, industrial effluents, urbanization, agriculture, coastline erosion, coastal population and fishing. A 1:10 000 continuous habitat map is provided considering 11 habitat classes. The marine bottom is mostly covered by three habitats: infralittoral soft bottom, Posidonia oceanica meadows and circalittoral soft bottom. Around two thirds of the bottoms are found within medium and medium high cumulative impact categories. Seagrass meadows are the most impacted habitats. The most important pressures (in area and intensity) are urbanization, coastal population, coastal erosion and man-made coastline. We also identified areas in need of a special management interest. This work should contribute to prioritize environmental needs, as well as enhance the development of indicators for the assessment of the ecological status of coastal systems. It could also help better apply and coordinate management measures at a relevant scale for biodiversity conservation.

The seagrass Posidonia oceanica: Ecosystem services identification and economic evaluation of goods and benefits.

Posidonia oceanica is a marine angiosperm endemic from the Mediterranean. Despite their protection, its meadows are regressing. The economic valuation of ecosystem services (ES) assesses the contribution of ecosystems to human well-being and may provide local policy makers help in territorial development. To estimate the economic value of P. oceanica seagrass and the meadows that it forms to better account its presence in coastal development, identification and assessment of ES provided are first performed. Then goods and benefits (GB) and their economical values are estimated. In total, 25ES are identified and 7GB are economically evaluated. The economic value of GB provided by P. oceanica ranges between 25.3 million and 45.9 million€/year which means 283-513€/ha/year. Because of the lack of existing available data, only 7GB linked to 11/25ES have been estimated. Despite this overall undervaluation, this study offers a value for coastal development policies to take into account.

Fast and easy method for seagrass monitoring: application of acoustic telemetry to precision mapping of Posidonia oceanica beds.

Posidonia oceanica is an endemic seagrass from the Mediterranean Sea. It is an indicator of water quality and of the ecological state of coastal ecosystems. The aim of this paper is to test acoustic telemetry for monitoring the position of P. oceanica meadow limits with varied types. After evaluating the accuracy of the system, we present results from a spatiotemporal survey of P. oceanica meadows on nine sites located on the French coast. The method has been demonstrated to be highly efficient for high precision underwater mapping regardless of meadow type, with 1 cm accuracy for a distance of 40 m between the base and the pointer. A temporal survey led at Cerbere-Banyuls shows a weak global progression of 4 m² (progression of 26 m² - regression of 22 m²) between 2006 and 2010. Finally, we discuss the cost and efficiency of this method, and wether it should be generalized for further studies.

Negative relationships between cellular immune response, Mhc class II heterozygosity and secondary sexual trait in the montane water vole.

Heterogeneities in immune responsiveness may affect key epidemiological parameters and the dynamics of pathogens. The roles of immunogenetics in these variations remain poorly explored. We analysed the influence of Major histocompatibility complex (Mhc) genes and epigamic traits on the response to phytohaemagglutinin in males from cyclic populations of the montane water vole (Arvicola scherman). Besides, we tested the relevance of lateral scent glands as honest signals of male quality. Our results did not corroborate neither the hypotheses of genome-wide heterozygosity-fitness correlation nor the Mhc heterozygote advantage. We found a negative relationship between Mhc hetetozygosity and response to phytohaemagglutinin, mediated by a specific Mhc homozygous genotype. Our results therefore support the hypothesis of the Arte-Dqa-05 homozygous genotype being a 'good' Mhc variant in terms of immunogenetic quality. The development of the scent glands seems to be an honest signal for mate choice as it is negatively correlated with helminth load. The 'good gene' hypothesis was not validated as Arte-Dqa-05 homozygous males did not exhibit larger glands. Besides, the negative relationship observed between the size of these glands and the response to phytohaemagglutinin, mainly for Mhc homozygotes, corroborates the immunocompetence handicap hypothesis. The Mhc variants associated with larger glands remain yet to be determined.

Serological evidence of viruses naturally associated with the montane water vole (Arvicola scherman) in eastern France.

We surveyed 12 populations of the montane water vole (Arvicola scherman), previously known as the fossorial form of the water vole A. terrestris, in eastern France for antibodies (immunoglobulin G) to Puumala virus (PUUV), lymphocytic choriomeningitis virus (LCMV), and cowpox virus (CPXV). Antibodies to PUUV were found in 9 (5.5%) of 164 voles from 7 populations, antibodies to LCMV were found in 13 (26.0%) of 50 voles from 2 populations, and antibodies to CPXV were found in 66 (41.8%) of 158 voles from 7 populations. Antibody status to CPXV was statistically associated with the phase of the A. scherman population density cycle and the percentage of grassland areas surrounding the sampling sites.

Stress and demographic decline: a potential effect mediated by impairment of reproduction and immune function in cyclic vole populations.

The stress response is initially adaptive, operating to maintain homeostasis. However, chronic long-term exposure to stressors may have detrimental effects. We proposed that chronic stress may be a major factor in demographic vole cycles, inducing decline in high-density populations. We monitored four populations of the fossorial water vole Arvicola scherman, which undergo pluriannual demographic cycles in the Jura Mountains (France). Sampling was conducted during the high densities and the decline. We measured fecal corticosterone metabolites (FCMs) to assess stress levels and injected phytohemagglutinin to estimate the cell-mediated immune response. We demonstrated that stress levels increase between the high densities and the decline in most of the vole populations. At the individual level, FCM concentrations varied with reproductive status and body condition. During the outbreak, we observed significantly higher levels of FCM concentrations in nulliparous females than in females that had previously reproduced. Moreover, a significant negative correlation was observed between concentrations of FCMs and both immunocompetence and body condition during population decline. These results might reflect an impairment of the female reproductive capability in high densities and accelerated senescence affecting immune function during decline, both arising from chronic stress.

Association between the DQA MHC class II gene and Puumala virus infection in Myodes glareolus, the bank vole.

Puumala virus (PUUV) is a hantavirus specifically harboured by the bank vole, Myodes (earlier Clethrionomys) glareolus. It causes a mild form of hemorrhagic fever with renal syndrome (HFRS) in humans, called Nephropathia epidemica (NE). The clinical severity of NE is variable among patients and depends on their major histocompatibility complex (MHC) genetic background. In this study we investigated the potential role of class II MHC gene polymorphism in the susceptibility/resistance to PUUV in the wild reservoir M. glareolus. We performed an association study between the exon 2 of the DQA gene and PUUV antibodies considering a natural population of bank voles. Because immune gene polymorphism is likely to be driven by multiple parasites in the wild, we also screened bank voles for other potential viral and parasitic infections. We used multivariate analyses to explore DQA polymorphism/PUUV associations while considering the potential antagonist and/or synergistic effects of the whole parasite community. Our study suggests links between class II MHC characteristics and viral infections including PUUV and Cowpox virus. Several alleles are likely to be involved in the susceptibility or in the resistance of bank voles to these infections. Alternatively, heterozygosity does not seem to be associated with PUUV or any other parasite infections. This result thus provides no evidence in favour of the hypothesis of selection through overdominance. Finally this multivariate approach reveals a strong antagonism between ectoparasitic mites and PUUV, suggesting direct or indirect immunogenetic links between infections by these parasites. Other datasets are now required to confirm these results and to test whether the associations vary in space and/or time.

Puumala and Tula hantaviruses in France.

The first genome sequences of Tula (TULV) and Puumala (PUUV) hantaviruses undoubtedly originated from France were recovered from tissue samples of European common voles and bank voles captured in Jura region. Genetic analysis of S and M segments of French PUUV strain revealed its highest similarity to strains from neighboring Belgium and Germany and also from Slovakia. On phylogenetic trees, French PUUV strain was placed within the central European lineage formed by strains from these three countries. Both of our French TULV strains clustered together and formed a distinct, well-supported genetic lineage.

Linking demography and host dispersal to Trichuris arvicolae distribution in a cyclic vole species.

Spatial structure in the distribution of pathogen infection can influence both epidemiology and host-parasite coevolutionary processes. It may result from the spatial heterogeneity of intrinsic and extrinsic factors, or from the local population dynamics of hosts and parasites. In this study, we investigated the effects of landscape, host dispersal and demography (population abundance and phase of the fluctuation) on the distribution of a gastro-intestinal nematode Trichuris arvicolae in the fossorial water vole Arvicola terrestris sherman. This rodent exhibits outbreaks occurring regularly in Franche-Comté (France). Thirteen out-of-phase populations were studied in autumn 2003. They exhibited highly different T. arvicolae prevalences. The heterogeneity in prevalences was not explained by population structure, landscape or vole abundance, but by the phase of the vole population fluctuations. Populations at the end of the high density phase showed null prevalence whereas populations in increase or outbreak phases exhibited higher prevalences. Population genetic analyses based on microsatellites revealed significant differentiation between vole populations, and higher dispersal rates of young voles compared with old ones. These younger individuals were also infected more frequently than older voles. This suggested a role of host dispersal in the distribution of T. arvicolae. However, there was a strong discrepancy between the spatial patterns of prevalence and of host genetics or demographic phase. Genetic differentiation and differences in demographic phase exhibited significant spatial autocorrelations whereas prevalence did not. We concluded that the distribution of T. arvicolae is influenced by vole dispersal, although this effect might be overwhelmed by local adaptation processes or environmental conditions.