The distribution of coastal fish eDNA sequences in the Anthropocene

Aim

Coastal fishes have a fundamental role in marine ecosystem functioning and contributions to people, but face increasing threats due to climate change, habitat degradation and overexploitation. The extent to which human pressures are impacting coastal fish biodiversity in comparison with geographic and environmental factors at large spatial scale is still under scrutiny. Here, we took advantage of environmental DNA (eDNA) metabarcoding to investigate the relationship between fish biodiversity, including taxonomic and genetic components, and environmental but also socio-economic factors.

Location

Tropical, temperate and polar coastal areas.

Time period

Present day.

Major taxa studied

Marine fishes.

Methods

We analysed fish eDNA in 263 stations (samples) in 68 sites distributed across polar, temperate and tropical regions. We modelled the effect of environmental, geographic and socio-economic factors on α- and β-diversity. We then computed the partial effect of each factor on several fish biodiversity components using taxonomic molecular units (MOTU) and genetic sequences. We also investigated the relationship between fish genetic α- and β-diversity measured from our barcodes, and phylogenetic but also functional diversity.

Results

We show that fish eDNA MOTU and sequence α- and β-diversity have the strongest correlation with environmental factors on coastal ecosystems worldwide. However, our models also reveal a negative correlation between biodiversity and human dependence on marine ecosystems. In areas with high dependence, diversity of all fish, cryptobenthic fish and large fish MOTUs declined steeply. Finally, we show that a sequence diversity index, accounting for genetic distance between pairs of MOTUs, within and between communities, is a reliable proxy of phylogenetic and functional diversity.

Main conclusions

Together, our results demonstrate that short eDNA sequences can be used to assess climate and direct human impacts on marine biodiversity at large scale in the Anthropocene and can further be extended to investigate biodiversity in its phylogenetic and functional dimensions.     

How accessible are coral reefs to people? A global assessment based on travel time

The depletion of natural resources has become a major issue in many parts of the world, with the most accessible resources being most at risk. In the terrestrial realm, resource depletion has classically been related to accessibility through road networks. In contrast, in the marine realm, the impact on living resources is often framed into the Malthusian theory of human density around ecosystems. Here, we develop a new framework to estimate the accessibility of global coral reefs using potential travel time from the nearest human settlement or market. We show that 58% of coral reefs are located < 30 min from the nearest human settlement. We use a case study from New Caledonia to demonstrate that travel time from the market is a strong predictor of fish biomass on coral reefs. We also highlight a relative deficit of protection on coral reef areas near people, with disproportional protection on reefs far from people. This suggests that conservation efforts are targeting low‐conflict reefs or places that may already be receiving de facto protection due to their isolation. Our global assessment of accessibility in the marine realm is a critical step to better understand the interplay between humans and resources.     

The back-calculation of size and growth from otoliths: Validation and comparison of models at an individual level

Multiple internal and external tagging experiments tested the applicability of five back-calculation models (Biological Intercept, Modified-Fry, Body Proportional Hypothesis, Time-Varying Growth, and an Age-Effects model) as predictors of individual growth trajectories of two marine cleaning gobies, Elacatinus evelynae and E. prochilos, that were raised in aquaria under conditions that resulted in variable growth. Mixed-effect model analyses of longitudinal records of otoliths and somatic growth collected at the individual level revealed that E. evelynae and E. prochilos produced daily increments on their otoliths for up to two months post-settlement and that the Modified-Fry model provided the most accurate size-at-age estimates despite the presence of age, growth and time-varying growth effects in the dataset. Very large errors in predicted size were produced by the Age-Effects model. The four other back-calculation models all provided slightly biased estimates of back-calculated size-at-age, with the Modified-Fry model providing the least biased estimates. Regardless of bias, both experimental and theoretical evidence indicated that back-calculated size was a better proxy of fish length than otoliths radius. Relationships between fish length and otoliths radius were allometric at the level of individuals, which explained why the Modified-Fry model performed better. However, this allometry was undetectable at the population level. This study represents the first attempt to validate modern back-calculation models using longitudinal data collected and analysed at the individual level. Our results suggest the use of the Modified-Fry model as a conservative approach in routine back-calculations of fish size at age from otoliths.     

Global mismatch between species richness and vulnerability of reef fish assemblages

The impact of anthropogenic activity on ecosystems has highlighted the need to move beyond the biogeographical delineation of species richness patterns to understanding the vulnerability of species assemblages, including the functional components that are linked to the processes they support. We developed a decision theory framework to quantitatively assess the global taxonomic and functional vulnerability of fish assemblages on tropical reefs using a combination of sensitivity to species loss, exposure to threats and extent of protection. Fish assemblages with high taxonomic and functional sensitivity are often exposed to threats but are largely missed by the global network of marine protected areas. We found that areas of high species richness spatially mismatch areas of high taxonomic and functional vulnerability. Nevertheless, there is strong spatial match between taxonomic and functional vulnerabilities suggesting a potential win–win conservation‐ecosystem service strategy if more protection is set in these locations.     

Validation of daily increment formation in otoliths for three Diplodus species in the Mediterranean sea

The efficacy of two fluorochromes, chlorhydrate of tetracycline (CHTC) and alizarin complexone (ALC), to induce a label on the otoliths of juvenile sparid fishes by immersion techniques was tested in different experimental conditions. CHTC did not mark otoliths in natural sea water and was toxic in divalent cation-free sea water. Immersing fish in a 50-mg 1⁻¹ ALC natural seawater solution for 24 h induced a well-defined mark on the otoliths and had no effect on survival. A daily periodicity of increment formation on otoliths was observed in captivity for Diplodus vulgaris and D. puntazzo , and was conserved in natural environment for D. sargus . The frequency of increment deposition did not vary with the age of juvenile fishes. Thus, otolith microstructure analysis will be a reliable method to give age estimates in these three sparid species during their juvenile life.     

Cytochrome b barcoding, molecular systematics and geographic differentiation in rabbitfishes (Siganidae)

The fish genus Siganus (Siganidae) is widely distributed in the coastal habitats of all the tropical Indo-Pacific, with 28 nominal species recognized so far, based on general morphology and coloration patterns. A mitochondrial phylogeny of 16 Siganidae species, based on the partial nucleotide sequences of the cytochome b gene, was produced. Individual haplotypes of given nominal species generally clustered at the extremity of long branches, thus validating the current taxonomy. However, S. lineatus haplotypes formed a paraphyletic group including S. guttatus, while S. fuscescens haplotypes were apparently splitted in two groups, calling for further investigation. S. woodlandi and S. argenteus formed a monophyletic group, as expected from their close morphological relatedness, although they were separated by a substantial, 14.5-16.3% nucleotide distance. Among eight species sampled from different locations across the Indo-West Pacific, S. argenteus and S. spinus showed the lowest degree of geographic differentiation, a result that correlated well with their extended pelagic larval stage. Fixation index estimates were high in all six other species tested (S. doliatus, S. fuscescens, S. lineatus, S. puellus, S. punctatus, S. vulpinus). The cytochrome b gene fragment chosen here proved useful as a barcode in Siganidae.     

Functional redundancy patterns reveal non-random assembly rules in a species-rich marine assemblage

The relationship between species and the functional diversity of assemblages is fundamental in ecology because it contains key information on functional redundancy, and functionally redundant ecosystems are thought to be more resilient, resistant and stable. However, this relationship is poorly understood and undocumented for species-rich coastal marine ecosystems. Here, we used underwater visual censuses to examine the patterns of functional redundancy for one of the most diverse vertebrate assemblages, the coral reef fishes of New Caledonia, South Pacific. First, we found that the relationship between functional and species diversity displayed a non-asymptotic power-shaped curve, implying that rare functions and species mainly occur in highly diverse assemblages. Second, we showed that the distribution of species amongst possible functions was significantly different from a random distribution up to a threshold of ～90 species/transect. Redundancy patterns for each function further revealed that some functions displayed fast rates of increase in redundancy at low species diversity, whereas others were only becoming redundant past a certain threshold. This suggested non-random assembly rules and the existence of some primordial functions that would need to be fulfilled in priority so that coral reef fish assemblages can gain a basic ecological structure. Last, we found little effect of habitat on the shape of the functional-species diversity relationship and on the redundancy of functions, although habitat is known to largely determine assemblage characteristics such as species composition, biomass, and abundance. Our study shows that low functional redundancy is characteristic of this highly diverse fish assemblage, and, therefore, that even species-rich ecosystems such as coral reefs may be vulnerable to the removal of a few keystone species.     

Global patterns and predictors of tropical reef fish species richness

In the marine realm, the tropics host an extraordinary diversity of taxa but the drivers underlying the global distribution of marine organisms are still under scrutiny and we still lack an accurate global predictive model. Using a spatial database for 6336 tropical reef fishes, we attempted to predict species richness according to geometric, biogeographical and environmental explanatory variables. In particular, we aimed to evaluate and disentangle the predictive performances of temperature, habitat area, connectivity, mid‐domain effect and biogeographical region on reef fish species richness. We used boosted regression trees, a flexible machine‐learning technique, to build our predictive model and structural equation modeling to test for potential ‘mediation effects’ among predictors. Our model proved to be accurate, explaining 80% of the total deviance in fish richness using a cross‐validated procedure. Coral reef area and biogeographical region were the primary predictors of reef fish species richness, followed by coast length, connectivity, mid‐domain effect and sea surface temperature, with interactions between the region and other predictors. Important indirect effects of water temperature on reef fish richness, mediated by coral reef area, were also identified. The relationship between environmental predictors and species richness varied markedly among biogeographical regions. Our analysis revealed that a few easily accessible variables can accurately predict reef fish species richness. They also highlight concerns regarding ongoing environmental declines, with region‐specific responses to variation in environmental conditions predicting a variable response to anthropogenic impacts.