Phylogeny, body morphology, and trophic level shape intestinal traits in coral reef fishes

Abstract

Trait-based approaches are increasingly used to study species assemblages and understand ecosystem functioning. The strength of these approaches lies in the appropriate choice of functional traits that relate to the functions of interest. However, trait-function relationships are often supported by weak empirical evidence.Processes related to digestion and nutrient assimilation are particularly challenging to integrate into trait-based approaches. In fishes, intestinal length is commonly used to describe these functions. Although there is broad consensus concerning the relationship between fish intestinal length and diet, evolutionary and environmental forces have shaped a diversity of intestinal morphologies that is not captured by length alone.Focusing on coral reef fishes, we investigate how evolutionary history and ecology shape intestinal morphology. Using a large dataset encompassing 142 species across 31 families collected in French Polynesia, we test how phylogeny, body morphology, and diet relate to three intestinal morphological traits: intestinal length, diameter, and surface area.We demonstrate that phylogeny, body morphology, and trophic level explain most of the interspecific variability in fish intestinal morphology. Despite the high degree of phylogenetic conservatism, taxonomically unrelated herbivorous fishes exhibit similar intestinal morphology due to adaptive convergent evolution. Furthermore, we show that stomachless, durophagous species have the widest intestines to compensate for the lack of a stomach and allow passage of relatively large undigested food particles.Rather than traditionally applied metrics of intestinal length, intestinal surface area may be the most appropriate trait to characterize intestinal morphology in functional studies.

Keywords: Bayesian phylogenetic comparative method; convergent evolution; digestive traits; evolutionary conservatism; fish diet; gut length.

FIGURE 1

Phylogenetic reconstruction of the 139 reef fish species collected in Mo'orea (generated from the Fish Tree of Life, Chang et al., 2019) with each surrounding ring indicating mean fitted intestinal traits at a standardized fish standard length (SL = 15 cm). Intestinal trait predictions were obtained from Bayesian phylogenetic hierarchical linear models. Colored tip points represent species’ trophic level. Each external arc represents a reef fish family, with silhouettes included for the most speciose families (sourced from Schiettekatte et al., 2019)

FIGURE 2

Partitioning of intestinal morphology among (a) reef fish families and (b) trophic guilds (as predicted by Parravicini et al., 2020). Dots (i.e., species) (n = 142) are ordered in a morphospace based on intestinal length and diameter and are size‐coded to represent variation in intestinal surface area. Intestinal traits are mean fitted values at a standardized fish standard length (SL = 15 cm), estimated through Bayesian phylogenetic hierarchical linear models. Dashed lines represent the estimated average intestinal length and diameter of non‐durophagous fishes with a stomach (model intercept at SL = 15 cm). Colored polygons show the minimum convex hull plotted per (a) family and (b) trophic guild. Dots are colored according to (a) families represented by at least three species and for which a convex hull could be drawn (for clarity of presentation) and (b) trophic guilds. Gray dots depict (a) species (n = 22) belonging to families represented by less than three species and (b) species (n = 3) for which Parravicini et al. (2020) did not predict a trophic guild. Fish silhouettes were sourced from Schiettekatte et al., (2019). HMD, herbivores, microvores, and detritivores

FIGURE 3

Relationship between three intestinal traits and body elongation (a, c, e) and trophic level (b, d, f) for 142 species of coral reef fishes. Thick, darkened lines represent the mean predicted fits of Bayesian phylogenetic hierarchical linear models after controlling for the remaining fixed and random effects. Categorical variables were set to their most common value (stomach = present, durophagy = non‐durophagous). Thin lines represent 1,000 draws randomly chosen from the posterior fits and show model fit uncertainty. Model predictions are for natural‐log intestinal traits, but are transformed here to show the fitted function on the original scale of the data. Raw data are displayed as marks along the x‐axis

FIGURE 4

Effects of a stomach and durophagous diet on (a) intestinal length, (b) diameter, and (c) surface area for 142 species of coral reef fishes. Estimates are posterior medians (circles), 50% credible intervals (CIs; thick lines) and 95% CIs (thin lines) from Bayesian phylogenetic hierarchical linear models after controlling for the remaining fixed and random effects. Posterior densities are also displayed (shaded regions)

FIGURE 5

Species‐specific scaling parameters of three natural‐log intestinal traits against natural‐log fish standard length for 21 species of coral reef fishes. Estimates are posterior medians (circles), 80% credible intervals (CIs; thick lines) and 95% CIs (thin lines) from Bayesian phylogenetic hierarchical linear models. Vertical dashed lines represent isometric scaling (β = 1 for intestinal length and diameter; β = 2 for intestinal surface area). Colored intervals indicate allometric scaling, indicating that more than 90% (if 80% CIs) or 97.5% (if 95% CIs) of the posterior density was either above (blue; positive allometry) or below (red; negative allometry) the isometric scaling parameter, whereas gray intervals indicate that they overlap the parameter. For each trait, species were selected based on a minimum sample size of ten individuals whose size range covered at least 25% of the reported maximum body size (retrieved from FishBase) and a posterior 95% CI above zero to provide reliable estimates of scaling parameters. This selection resulted in missing estimates for one or two traits in five species