Planktivores as trophic drivers of global coral reef fish diversity patterns

Abstract

One of the most prominent features of life on Earth is the uneven number of species across large spatial scales. Despite being inherently linked to energetic constraints, these gradients in species richness distribution have rarely been examined from a trophic perspective. Here we dissect the global diversity of over 3,600 coral reef fishes to reveal patterns across major trophic groups. By analyzing multiple nested spatial scales, we show that planktivores contribute disproportionally to the formation of the Indo-Australian Archipelago (IAA) marine biodiversity hotspot. Besides being "hotter" at the hotspot, planktivorous fishes display the steepest decline in species numbers with distance from the IAA when compared to other trophic groups. Surprisingly, we did not detect differences in diversification, transition, and dispersal rates in extant species phylogenies that would explain this remarkable gradient in planktivorous fish richness. Thus, we identify two potential complementary drivers for this pattern. First, exceptional levels of partitioning among planktivorous coral reef fishes were driven by temporally stable oceanographic conditions and abundant planktonic resources in the IAA. Second, extinctions of planktivores outside the IAA have been particularly pronounced during Quaternary climate fluctuations. Overall, our results highlight trophic ecology as an important component of global species richness gradients.

Keywords: Indo-Australian Archipelago; extinction; macroecology; species richness; trophic groups.

Fig. 1.

Global coral reef fish richness per trophic group. Maps show the absolute number of species per grid cell (n = 2,800) in each classified trophic group. Cell colors correspond to the scale bar and range from low (blue) to intermediate (yellow) and high (red) richness. Grid cell resolution is 150 km² (see Rabosky et al., 27).

Fig. 2.

Global coral reef fish species richness (A) and proportion (B) per guild with distance from the IAA. (A) Number of species per grid cell (mean [black line] ± 95% CI [colored shading]) predicted from a negative binomial model per trophic group. The inset displays the model coefficient (±95% CI) per trophic group along with the R² value of each model. Lines in the main figure represent the interaction between mean body size and trophic group; therefore, their perceived inclination may not match the size-independent coefficient represented in the Inset. (B) Proportion of species per grid cell in each trophic group (mean [black line] and interquartile range [colored shading]) predicted from beta regression models. Respective pseudo-R² values are shown in the top left corners. Semitransparent dots represent sampled grid cells (n = 2,800). Predictions from all models were performed with body size fixed in the estimated value for the cells closer to the center of the IAA. Trophic groups: generalized carnivores, red; herbivores/detritivores, green; mobile invertivores, yellow; omnivores, beige; planktivores, blue; sessile invertivores, brown.

Fig. 3.

Coral reef fish species richness at the regional scale per trophic group. (A) Mean planktivorous fish species richness per transect in 31 ecoregions (sensu Spalding et al., 28) across the Indo-Pacific. Ecoregions comprise multiple aggregated values from sites (see Materials and Methods), with each site sampled using standardized fish counts covering 250 m² in area (Edgar and Stuart-Smith, 29). (B) Regional-level mean species richness per transect for each trophic group (from visual surveys, points) at increasing distances from the IAA. Curves show predictions from a generalized linear model (mean [black line] ± 95% CI [colored shading]) with respective R² values (top left corner). Model predictions were performed with body size fixed in the estimated value for the regions closer to the center of the IAA. Trophic groups: generalized carnivores, red; herbivores/detritivores, green; mobile invertivores, yellow; omnivores, beige; planktivores, blue; sessile invertivores, brown.

Fig. 4.

Potential evolutionary mechanisms underpinning the richness gradient in coral reef fish planktivores. (A) Mean net diversification rate per geographic cell (n = 2,800) in planktivorous lineages against distance from the IAA. The black line shows prediction from a generalized linear model with the respective R² value (top left). (B) Proportion of transitions toward planktivory per biogeographic province. Black points show mean proportions, and shading shows the interquartile range. Semitransparent points represent individual simmap simulations per province (n = 1,000). Provinces: central Pacific (CP), western Indian (WI), tropical eastern Pacific (TEP), eastern Atlantic (EA), and western Atlantic (WA). Colors in A and B depict a gradient of distance from the IAA, with red shades representing locations closest to the IAA and blue shades being farthest from the IAAc. (C) Dispersal rates from (orange) and into (purple) the IAA in planktivorous reef fish lineages. Black points underneath the posterior distributions represent modal values with respective 95% CI (n = 3,600 iterations).