Coprophagy in Caribbean parrotfishes

Parrotfishes are widely considered to be important grazers on coral reefs that remove autotrophic biomass from the reef substrate and create bare space that is conducive to larval coral settlement and recruitment. Because of the top-down effects associated with their benthic foraging, this has been a major focus of parrotfish research. Another aspect of parrotfish foraging and trophic ecology that has received very little attention is coprophagy, the consumption of fecal matter. The feces of planktivorous fishes, including Chromis spp., have been identified as important sources of nutrients and trace elements to tropical and temperate reef ecosystems. Their feces are readily consumed by a variety of fishes, including parrotfishes. Although parrotfish coprophagy has been observed in prior studies, its frequency has not yet been quantified. In this study, we observed foraging in five parrotfishes on the fringing reefs of Bonaire, Netherlands: Scarus iseri, Scarus taeniopterus, Scarus vetula, Sparisoma aurofrenatum, and Sparisoma viride. For three of these species, we observed individuals of both ontogenetic phases (terminal and initial phase) to investigate ontogenetic differences in foraging. We found that coprophagy was common in four of these species (Sc. iseri, Sc. taeniopterus, Sc. vetula, and Sp. aurofrenatum), occurring in 46-90% of individuals (Sc. vetula and Sc. taeniopterus, respectively). Though we did not identify the origin of every fecal pellet consumed, we directly observed focal fishes targeting fecal pellets produced by planktivorous Chromis spp. that were often seen schooling above the reef during this feeding behavior. Additionally, most of the fecal pellets consumed by the parrotfishes were similar in appearance (i.e., relative size, shape, coloration, and consistency) to the feces produced by Chromis spp., predominantly Chromis multilineata, suggesting this common origin. However, bites on fecal matter were a relatively small proportion of the total bites taken by these species (< 5%). In contrast, a majority of bites taken by these species were taken on substrates classified as eplithic algal matrix (EAM) or crustose coralline algae (68.5-90.6% of total bites across all five species). Despite being an infrequent target of parrotfish foraging, we estimated that daily fecal C consumption is equivalent to approximately 27% of the daily algal C intake by parrotfishes targeting the major benthic foraging targets of parrotfishes (large turfs, small turfs on endolithic algae or crustose coralline algae, and crustose coralline algae) in Bonaire. The feces of plantivorous reef fishes like Chromis spp. are also likely a valuable source of nutrients to reef fishes, because the fecese of Chromis spp. has higher protein and lipid content and lower C:N and C:P than many benthic marine algae and cyanobacteria, including from the tropics. The absence of coprophagy in Sp. viride and reduced rates of coprophagy in Sc. vetula relative to the other coprophagic species could be the result of increased access to protein-rich endolithic components of the benthos. Access to endolithic components of the benthos increases with body size and the ability to excavate benthic substrate while foraging. Sparisoma viride is an important excavating parrotfish on Caribbean coral reefs, and Sc. vetula is generally larger than the other coprophagic species in our study. Future work should attempt to further quantify the contribution of fecal matter to the nutrition of parrotfishes relative to benthic foraging targets in order to provide a more complete understanding of parrotfish nutritional ecology and to elucidate the importance of coprophagy in nutrient recycling and retention on coral reefs. 

Methods
Data were collected across 5 fringing reef sites in Bonaire, NL: Angel City (AC; 12.10305º, -68.28852º), Aquarius (AQ; 12.09824º, -68.28624º), Bachelor’s Beach (BB; 12.12605º, -68.28819º), Invisibles (IV; 12.07805º, -68.28175º), and The Lake (TL; 12.10618º, -68.29079º) during May-July 2019.

We conducted visual censuses of initial and terminal phase parrotfish (forklength > 6 cm) along eight 100-m2 (25-m x 4-m) band transects at each site to quantify density and biomass of parrotfishes (parrotfishes.csv). We also quantified the cover of benthic functional groups using photoquadrats (n=10) placed at 1-m intervals along 10-m transects (n=4 at each site with 1 additional transect with 3 photoquadrats at AQ) running perpendicular to the reef slope at approximately 10-m depth at each site (benthic-cover.csv). In addition to quantifying the total cover of coral at these 5 sites, we also identified corals to the species level to explore differences in coral community composition across sites. Total coral cover was therefore broken down by species as well.

Finally, we conducted foraging observations of 162 unique individuals of the 5 most common parrotfishes across our 5 fringing reef sites: Scarus iseri, Scarus taeniopterus, Scarus vetula, Sparisoma aurofrenatum, and Sparisoma viride. For 3 species (Scarus taeniopterus, Scarus vetula, and Sparisoma viride), we conducted observations of both ontogenetic phases (initial and terminal phase) to investigate ontogenetic differences in foraging. During these foraging observations we video recorded parrotfish behavior and later scored videos, recording all bites taken, the target of those bites (benthic functional groups and bites on feces in the water column), and when coral was bitten, the species of coral targeted was identified (bites.csv). The standard length (cm) of every fish, the total duration of each observation (mins), the time during each video recorded observation that the fish was not visible (mins), and the final follow time (total time - lost time; mins) are also reported for each fish (follow-data.csv). The final follow time (Final.Time) is what we used for analyses of foraging rates. All fish were followed between ~1000-1600 hrs local time in Bonaire (AST, UTC/GMT -4).