Isolation drives taxonomic and functional nestedness in tropical reef fish faunas

Taxonomic nestedness, the degree to which the taxonomic composition of species‐poor assemblages represents a subset of richer sites, commonly occurs in habitat fragments and islands differing in size and isolation from a source pool. However, species are not ecologically equivalent and the extent to which nestedness is observed in terms of functional trait composition of assemblages still remains poorly known. Here, using an extensive database on the functional traits and the distributions of 6316 tropical reef fish species across 169 sites, we assessed the levels of taxonomical vs functional nestedness of reef fish assemblages at the global scale. Functional nestedness was considerably more common than taxonomic nestedness, and generally associated with geographical isolation, where nested subsets are gradually more isolated from surrounding reef areas and from the center of biodiversity. Because a nested pattern in functional composition implies that certain combinations of traits may be represented by few species, we identified these groups of low redundancy that include large herbivore‐detritivores and omnivores, small piscivores, and macro‐algal herbivores. The identified patterns of nestedness may be an outcome of the interaction between species dispersal capabilities, resource requirements, and gradients of isolation among habitats. The importance of isolation in generating the observed pattern of functional nestedness within biogeographic regions may indicate that disturbance in depauperate and isolated sites can have disproportionate effects on the functional structure of their reef fish assemblages.     

Historical and contemporary processes drive global phylogenetic structure across geographical scales: Insights from bat communities

Aim

Patterns of evolutionary relatedness among co-occurring species are driven by scale-dependent contemporary and historical processes. Yet, we still lack a detailed understanding of how these drivers impact the phylogenetic structure of biological communities. Here, we focused on bats (one of the most species-rich and vagile groups of mammals) and tested the predictions of three general biogeographical hypotheses that are particularly relevant to understanding how palaeoclimatic stability, local diversification rates and geographical scales shaped their present-day phylogenetic community structure.

Location

World-wide, across restrictive geographical extents: global, east–west hemispheres, biogeographical realms, tectonic plates, biomes and ecoregions.

Time period

Last Glacial Maximum (~22,000 years ago) to the present.

Major taxa studied

Bats (Chiroptera).

Methods

We estimated bat phylogenetic community structure across restrictive geographical extents and modelled it as a function of palaeoclimatic stability and in situ net diversification rates.

Results

Limiting geographical extents from larger to smaller scales greatly changed the phylogenetic structure of bat communities. The magnitude of these effects is less noticeable in the western hemisphere, where frequent among-realm biota interchange could have been maintained through the adaptive traits of bats. Bat communities with high phylogenetic relatedness are generally more common in regions that have changed less in climate since the Last Glacial Maximum, supporting the expectation that stable climates allow for increased phylogenetic clustering. Finally, increased in situ net diversification rates are associated with greater phylogenetic clustering in bat communities.

Main conclusions

We show that the world-wide phylogenetic structure of bat assemblages varies as a function of geographical extents, dispersal barriers, palaeoclimatic stability and in situ diversification. The integrative framework used in our study, which can be applied to other taxonomic groups, has not only proved useful to explain the evolutionary dynamics of community assembly, but could also help to tackle questions related to scale dependence in community ecology and biogeography.     

Spatial mismatch in morphological,ecological and phylogenetic diversity,in historical and contemporary European freshwater fish faunas

Biodiversity encompasses multiple facets, among which taxonomic, functional and phylogenetic aspects are the most often considered. Understanding how those diversity facets are distributed and what are their determinants has become a central concern in the current context of biodiversity crisis, but such multi‐faceted measures over large geographical areas are still pending. Here, we measured the congruence between the biogeographical patterns of freshwater fish morphological, ecological and phylogenetic diversity across Europe and identified the natural and anthropogenic drivers shaping those patterns. Based on freshwater fish occurrence records in 290 European river catchments, we computed richness and evenness for morphological, ecological and phylogenetic diversity using standardized effect sizes for each diversity index. We then used linear models including climatic, geo‐morphological, biotic and human‐related factors to determine the key drivers shaping freshwater fish biodiversity patterns across Europe. We found a weak spatial congruence between facets of diversity. Patterns of diversity were mainly driven by elevation range, climatic seasonality and species richness while other factors played a minor role. Finally, we found that non‐native species introductions significantly affected diversity patterns and influenced the effects of some environmental drivers. Morphological, ecological and phylogenetic diversity constitute complementary facets of fish diversity rather than surrogates, testifying that they deserve to be considered altogether to properly assess biodiversity. Although the same environmental and anthropogenic factors overall explained those diversity facets, their relative influence varied. In the current context of global change, non‐native species introductions may also lead to important reshuffling of assemblages resulting in profound changes of diversity patterns.     

Evolutionary patterns in tropical marine reef fish feeding

The majority of tropical reef fishes are acanthopterygians. Most of them are percomorphs and thus are likely monophyletic. In accordance to modern systematics, the primitive types among the latter are large-mouthed suction feeders. Species from advanced families often have biting oral jaws with a reduced number and complexly shaped teeth. Mouth sizes decrease from the primitive towards the advanced reef fishes when ranked according to increasing family numbers (Nelson 1984). To create a functional resource axis, Randall's (1967) and Hobson's (1974) data on tropical reef fish feeding were re-interpreted by ranking food items from mobile to sessile prey. The primitive paracantho pterygian and acanthopterygian reef fishes are large-mouthed, suction-feeding predators on mobile prey. Most of the advanced, small-mouthed species are browsers and grazers, but often feed on mobile prey too. Obligatory specialists (monophagous and unable to switch) seem to be relatively rare among modern reef fishes. The trends stated above indicate a wealth of parallel developments in many advanced families of reef fishes towards small, often biting oral jaws. This parallelism may be the result of comparable regimes of selection pressures in reefs and of the need for newly evolved species to establish themselves within the already existing guilds.     

Predators favour mimicry in a tropical reef fish

Batesian mimicry evolves when the 'umbrella' of protection provided by resemblance to a conspicuous unpalatable model species is sufficient to overcome increased predation risk associated with greater conspicuousness. However, the shape and extent of this umbrella, that is, how the level of protection provided by mimicry changes with degree of resemblance between model and mimic, is poorly known. We investigated the response of wild predatory fishes to plastic replicas of a model-mimic species pair of tropical reef fishes, Canthigaster valentini (a toxic pufferfish, the model) and Paraluteres prionurus (the putative mimic), and additional replicas with progressively lower degrees of resemblance to the mimic species. Our results reveal a relatively broad region of protection, indicated by a reduced approach rate by piscivorous fishes, surrounding the colour pattern of the model species. Protection increased with increasing resemblance. By contrast, the response of non-piscivorous fishes was unrelated to degree of resemblance of replicas to the model. Our results suggest that piscivorous fishes on the reef are educated regarding the toxicity of C. valentini, and that avoidance of fish having the pufferfish colour pattern has generated selection favouring mimetic resemblance by the palatable P. prionurus. The relatively broad protective umbrella has probably facilitated the initial evolution of resemblance in the palatable prey species despite the potential hazards of greater conspicuousness.     

Determinants of reef fish assemblages in tropical Oceanic islands

Diversity patterns are determined by biogeographic, energetic, and anthropogenic factors, yet few studies have combined them into a large‐scale framework in order to decouple and compare their relative effects on fish faunas. Using an empirical dataset derived from 1527 underwater visual censuses (UVC) at 18 oceanic islands (five different marine provinces), we determined the relative influence of such factors on reef fish species richness, functional dispersion, density and biomass estimated from each UVC unit. Species richness presented low variation but was high at large island sites. High functional dispersion, density, and biomass were found at islands with large local species pool and distance from nearest reef. Primary productivity positively affected fish richness, density and biomass confirming that more productive areas support larger populations, and higher biomass and richness on oceanic islands. Islands densely populated by humans had lower fish species richness and biomass reflecting anthropogenic effects. Species richness, functional dispersion, and biomass were positively related to distance from the mainland. Overall, species richness and fish density were mainly influenced by biogeographical and energetic factors, whereas functional dispersion and biomass were strongly influenced by anthropogenic factors. Our results extend previous hypotheses for different assemblage metrics estimated from empirical data and confirm the negative impact of humans on fish assemblages, highlighting the need for conservation of oceanic islands.     

Variability in relative importance of determinants of reef fish recruitment

Multiple processes can act together to determine abundance of organisms and structure of communities. Recently, appreciation of this fact has motivated development of conceptual and statistical frameworks that quantitatively assess the relative importance of multiple causal factors. However, little consideration has been given to variability in the "importance" of processes through space and time (i.e. robustness), which represents another facet of a process's importance. Here, I focused on populations of a coral reef fish ( Thalassoma hardwicke ) and used an existing analytical method to assess the relative importance of initial population inputs (larval supply) and subsequent juvenile mortality in determining the average abundances of juvenile fish populations in different locations and times. The relative importance of processes varied significantly both temporally and spatially across a range of scales, and indicate a need for future assessments of relative importance to incorporate this variability.     

Historical and contemporary factors govern global biodiversity patterns

A novel hierarchical framework integrates the effects of time, area, productivity, and temperature at their respective relevant scales and successfully predicts the latitudinal gradient in global vertebrate diversity.     

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.     

Morphological structure in a reef fish assemblage

Two key morphological traits, horizontal gape and eye diameter, were measured in a large representative group of coral reef fishes. These morphological traits were used concurrently to assess their utility in exploring abilities of coral reef fishes at an assemblage level. A total of 1,218 specimens from 181 species found on the Great Barrier Reef were examined. Cryptobenthic fishes were included to provide a broader representation of reef fish groups. In the analyses, a clear morphological distinction was found between nocturnal and diurnal fishes. Nocturnal fishes had larger relative horizontal gapes and relative eye diameters by factors of 1.6 and 1.5, respectively. A bivariate plot separated into quadrants was used to assess the implications of morphological variation. The morphological measures reflected distinct ecological traits in each quadrant. Whilst nocturnal fishes had large relative gapes and eye diameters, diurnal predators and detritivores had the same wide gapes, but small relative eye diameters. Highly selective, visual feeders such as the Chaetodontidae and Pseudochromidae had large eyes and small gapes, whilst non-selective feeders with low visual dependence such as the grazing herbivores (Acanthuridae, Siganidae, etc.) had both small eye diameters and gape sizes. The analysis proved to be robust enough to apply to a wide assemblage, but with enough subtlety to distinguish morphological differences within individual families. The methods used in this study may have broad applications to other fish assemblages, both fossil and extant. Electronic supplementary material  The online version of this article (doi:) contains supplementary material, which is available to authorized users.     

Similar regional effects among local habitats on the structure of tropical reef fish and coral communities

Aim We examined data on corals and reef fishes to determine how particular local habitat types contribute to variation in community structure across regions covering gradients in species richness and how consistent this was over time. Location Great Barrier Reef (GBR), Australia. Methods We compared large‐scale (1300 km), long‐term (11 years) data on fishes and corals that were collected annually at fixed sites in three habitats (inshore, mid‐shelf and outer‐shelf reefs) and six regions (latitudinal sectors) along a gradient of regional species richness in both communities. We used canonical approaches to partition variation in community structure (sites × species abundance data matrices) into components associated with habitat, region and time and Procrustes analyses to assess the degree of concordance between coral and fish community structure. Results Remarkably similar patterns emerged for both fish and coral communities occupying the same sites. Reefs that had similar coral communities also had similar fish communities. The fraction of the community data that could be explained by regional effects, independent of pure habitat effects, was similar in both fish (33%) and coral (36.9%) communities. Pure habitat effects were slightly greater in the fish (31.3%) than in the coral (20.1%) community. Time explained relatively little variation (fish = 7.9%, corals = 9.6%) compared with these two spatial factors. Conclusions Our results indicate either that fish and coral communities were structured in similar ways by processes associated with region, habitat and time, or that the variation in fish community structure tracked variation associated with the coral communities at these sites and thereby reflects an indirect link between the environment and the structure of fish communities mediated by corals. Irrespective of the causes of such commonality, we demonstrate that community structure, not just species richness, can be related to both habitat differences and regional setting simultaneously.     

Separating the determinants of phylogenetic community structure

The role of competition in forbidding similar species from co-occurring has long been debated. A difficulty in identifying this repulsion of similar species is that similar species share similar environmental requirements and hence show an attraction to communities where these requirements are met. To disentangle these opposing patterns, we use phylogenetic relatedness as an objective metric of species similarities. Studying 11 sunfishes (Centrarchidae) from 890 lakes, we first show no phylogenetic pattern in the raw community data. We then regressed sunfish presence/absence against seven environmental variables and show that lakes with similar water clarity and latitude likely contain closely related species. After statistically removing the environmental effects, phylogenetic repulsion was apparent, with closely related sunfishes less likely to co-occur. Thus, both phylogenetic attraction, driven by environmental filtering, and phylogenetic repulsion, possibly caused by competition, simultaneously occur and obscure one another in the overall phylogenetic structure of sunfish communities.     

Disturbance and the structure of coral reef fish communities on the reef slope

Three levels of physical disturbance were applied to corals in permanent 10x10 m quadrats along a section of fringing reef at Lizard Island on the Great Barrier Reef to investigate the response of fish assemblages. Tabular and corymbose corals were overturned and left in situ, reducing total hard coral cover from ˜55% to ˜47%, ˜43%, and ˜34%. Despite pre-existing associations with benthic cover, all fish groups examined (pomacentrids, labrids, chaetodontids, and acanthurids) were resistent to benthic disturbances at the level and scale at which they were applied. Partial Mantel's tests, in combination with partial Canonical Correspondence Analysis enabled spatial and temporal variation to be factored out from experimental effects. Most of the variation in the fish community could be assigned to spatio-temporal variables, indicating that spatial structure over the reef landscape may moderate localised disturbance effects. This study indicates that coral reef fish assemblages may be more resistant to disturbance than many correlative studies would suggest, and highlights a need for further information on levels and scales of natural habitat disturbance in order to apply a structured approach to the experimental investigation of the importance of habitat in structuring coral-reef fish assemblages.     

The relationship between habitat structure and fish faunas on New Zealand reefs

Reef fish abundances were sampled at 11 shallow reef localities extending over 1000 km of coastline in northern New Zealand. Sampling was restricted to the 4–10-m depth stratum and included six coastal and five island localities. These were either coralline reef flats dominated by echinoids, or algal reefs with high densities of laminarian and fucoid algae. Reefs dominated by macroscopic algae supported large numbers of small fishes, mainly labrids, and few large benthic-feeding fishes. Echinoid-dominated reefs supported a different fish fauna with more large benthic-feeding species. Additional sampling of echinoiddominated reefs and algal stands in deeper water provided confirmation of these findings. A second sampling programme was carried out at a series of eight sites within a single locality covering 5 km of coastline. These spanned a moderate exposure gradient and ranged from algal dominated reefs to typical coralline reef flats with high densities of grazing invertebrates. The relationship between habitat structure and reef fish species composition and size frequency was similar to that of the large-scale sampling programme. Thirdly, observations on reef fish foraging and feeding patterns within a single reef site suggested that larger benthic-feeding reef fishes were less likely to feed within macroscopic algal stands. Experimental reductions of grazing invertebrates designed to produce brown algal stands on echinoid-dominated reef flats supported these observations. Larger individuals capable of removing echinoids and grazing gastropods did not frequent or feed in laminarian and fucoid algal stands. This pattern is discernible at several spatial scales. Our conclusion is that the type of shallow reef habitat, echinoid- as opposed to algal-dominated, will have an important rôle in determining the associated reef fish fauna.     

Influence of depth on sex-specific energy allocation patterns in a tropical reef fish

The effect of depth on the distribution and sex-specific energy allocation patterns of a common coral reef fish, Chrysiptera rollandi (Pomacentridae), was investigated using depth-stratified collections over a broad depth range (5–39 m) and a translocation experiment. C. rollandi consistently selected rubble habitats at each depth, however abundance patterns did not reflect the availability of the preferred microhabitat suggesting a preference for depth as well as microhabitat. Reproductive investment (gonado-somatic index), energy stores (liver cell density and hepatocyte vacuolation), and overall body condition (hepato-somatic index and Fulton’s K) of female fish varied significantly among depths and among the three reefs sampled. Male conspecifics displayed no variation between depth or reef. Depth influenced growth dynamics, with faster initial growth rates and smaller mean asymptotic lengths with decreasing depth. In female fish, relative gonad weight and overall body condition (Fulton’s K and hepato-somatic index) were generally higher in shallower depths (≤10 m). Hepatic lipid storage was highest at the deepest sites sampled on each reef, whereas hepatic glycogen stores tended to decrease with depth. Depth was found to influence energy allocation dynamics in C. rollandi. While it is unclear what processes directly influenced the depth-related patterns in energy allocation, this study shows that individuals across a broad depth gradient are not all in the same physiological state and may contribute differentially to the population reproductive output. Electronic supplementary material The online version of this article (doi:) contains supplementary material, which is available to authorized users.     

Comparative efficiency of clove oil and rotenone for sampling tropical reef fish assemblages

A quantitative examination of the reef fish assemblage at Orpheus Island, Great Barrier Reef, contrasting clove oil and rotenone, sampled 365 individuals of 47 species with clove oil v. 536 individuals of 53 species with rotenone. Number of species and individuals were not found to differ significantly between the two techniques, largely due to variation among samples. Neopomacentrus bankieri (Pomacentridae) and Eviota queenslandica (Gobiidae) were the most dominant in the samples using either technique. Although the samples appeared to be comparable, only 31 species (45%) in eight families were common to both techniques. Fishes often recovered before collection when using clove oil and were not driven out of the reef during induction to anaesthesia. Although the samples collected with clove oil approximate the results obtained using rotenone, enclosed rotenone stations are the preferred method for providing relatively complete quantitative samples.     

Biogenic habitat structure and characteristics of temperate reef fish assemblages

Assemblages of non-cryptic, substrate-oriented species of fish were compared on a series of reefs in Southern California, USA. Reefs were grouped according to algal cover: dense beds of giant kelp (Macrocystis pyrifera) with turf understorey; sparse beds of giant kelp with foliose algae understorey: foliose algae < 1 m in height; and open barrens. Despite affinities to particular algal substrates by many individual species, we detected no differences in fish species richness and only weak differences in species composition among reefs of different habitat types. Planktivores and species that consume macro-invertebrates were less likely to occur on reefs that supported giant kelp; the frequencies of occurrence of three other trophic groups (piscivores, herbivores and micro-carnivores) were unaffected by giant kelp. Algal composition on reefs in Southern California is temporally highly dynamic. Changes in macro-algal composition of reefs influenced population dynamics of two fish species (black surfperch and striped surfperch) examined. Overall, the weak spatial variation in fish assemblages on reefs in Southern California appears to result from relatively unspecialized ecological requirements of many species combined with temporal changes in algal structure on reefs that are rapid relative to generation times of the fish. We hypothesize that the degree of spatial differentiation in assemblages of substrate-associated species of fish may be inversely related to the temporal constancy of biogenic reef structure.     

Recent invasion of the tropical Atlantic by an Indo-Pacific coral reef fish

The last tropical connection between Atlantic and Indian-Pacific habitats closed c. 2 million years ago (Ma), with the onset of cold-water upwelling off southwestern Africa. Yet comparative morphology indicates more recent connections in several taxa, including reef-associated gobies (genus Gnatholepis). Coalescence and phylogenetic analyses of mtDNA cytochrome b sequences demonstrate that Gnatholepis invaded the Atlantic during an interglacial period approximately 145,000 years ago (d = 0.0054), colonizing from the Indian Ocean to the western Atlantic, and subsequently to the central ( approximately 100,000 years ago) and eastern Atlantic ( approximately 30,000 years ago). Census data show a contemporary range expansion in the northeastern Atlantic linked to global warming.