Coral reef mesopredators switch prey, shortening food chains, in response to habitat degradation

Abstract

Diet specificity is likely to be the key predictor of a predator's vulnerability to changing habitat and prey conditions. Understanding the degree to which predatory coral reef fishes adjust or maintain prey choice, in response to declines in coral cover and changes in prey availability, is critical for predicting how they may respond to reef habitat degradation. Here, we use stable isotope analyses to characterize the trophic structure of predator–prey interactions on coral reefs of the Keppel Island Group on the southern Great Barrier Reef, Australia. These reefs, previously typified by exceptionally high coral cover, have recently lost much of their coral cover due to coral bleaching and frequent inundation by sediment‐laden, freshwater flood plumes associated with increased rainfall patterns. Long‐term monitoring of these reefs demonstrates that, as coral cover declined, there has been a decrease in prey biomass, and a shift in dominant prey species from pelagic plankton‐feeding damselfishes to territorial benthic algal‐feeding damselfishes, resulting in differences in the principal carbon pathways in the food web. Using isotopes, we tested whether this changing prey availability could be detected in the diet of a mesopredator (coral grouper, Plectropomus maculatus). The δ13C signature in grouper tissue in the Keppel Islands shifted from a more pelagic to a more benthic signal, demonstrating a change in carbon sources aligning with the change in prey availability due to habitat degradation. Grouper with a more benthic carbon signature were also feeding at a lower trophic level, indicating a shortening in food chains. Further, we found a decline in the coral grouper population accompanying a decrease in total available prey biomass. Thus, while the ability to adapt diets could ameliorate the short‐term impacts of habitat degradation on mesopredators, long‐term effects may negatively impact mesopredator populations and alter the trophic structure of coral reef food webs.

Regime shifts shorten food chains for mesopredators with potential sublethal effects

“…The reduction in small fish (<15 cm TL) on regime-shifted reefs in Seychelles, likely driven by loss of live coral and rugosity as reef structure degrades following bleaching (Dulvy, Polunin, Mill, & Graham, 2004;Graham et al, 2006;Munday & Jones, 1998), represents a decrease in the prey base available to mesopredators (Table S2). Despite their feeding adaptability (Hempson, Graham, MacNeil, Williamson, et al, 2017;Kingsford, 1992;Shpigel & Fishelson, 1989), reef mesopredators are physically limited in their prey choice by their gape size (Mumby et al, 2006), making them vulnerable to reduced biomass of suitably sized prey. Piscivorous mesopredators are therefore prone to experience deleterious effects of habitat degradation, mediated via their small-bodied prey base.…”

“…Many species have life expectancies in excess of 20 years (Froese & Pauly, 2016), allowing populations to persist for many years following a disturbance event, masking failed recruitment (Warner & Hughes, 1988) and producing a delayed effect that may last decades, suspending population decline (Bellwood, Hoey, Ackerman, & Depczynski, 2006;Graham et al, 2007). Mesopredators are also often more mobile than their prey (McCauley et al, 2012), with a broad dietary scope that allows them to adapt to changing prey availability (Hempson, Graham, MacNeil, Williamson et al, 2017;Kingsford, 1992;Shpigel & Fishelson, 1989). This adaptability allows fish to persist in the short term, but may carry a physiological cost that manifests at a sublethal level (Pratchett, Wilson, Berumen, & McCormick, 2004).…”

Ecosystem regime shifts disrupt trophic structure

“…Shifts in the composition of the reef fish community may represent a change in the prey base available to piscivorous mesopredators, requiring them to adapt their diets and alter their trophic niche (Hempson et al. ). Switching to a less preferred diet can be associated with potential sublethal effects, such as decreased energy reserves, condition, growth rates, survivorship, and fecundity (Kokita and Nakazono , Jones and McCormick , Pratchett et al.…”

“…Changes in the coral community can lead to changes in composition of the closely associated reef fish communities (Hempson et al 2017b), which may regain pre-disturbance abundances but have altered species composition (Berumen and Pratchett 2006). Shifts in the composition of the reef fish community may represent a change in the prey base available to piscivorous mesopredators, requiring them to adapt their diets and alter their trophic niche (Hempson et al 2017c). Switching to a less preferred diet can be associated with potential sublethal effects, such as decreased energy reserves, condition, growth rates, survivorship, and fecundity (Kokita and Nakazono 2001, Jones and McCormick 2002, Pratchett et al 2004, Berumen et al 2005, Hempson et al 2017a.…”

Integrating complementary methods to improve diet analysis in fishery‐targeted species

“…Indeed, the four main prey species (P. digramma, N. azysron, A. polyacanthus, and P. trichrourus) are predominantly planktivorous (Froese & Pauly, 2016). Changes in primary production and plankton-based trophodynamics (e.g., Doney, Fabry, Feely, & Kleypas, 2009) will likely have a strong effect on how mesopredators such as Plectropomus, select and partition prey (Audzijonyte, Kuparinen, Gorton, & Fulton, 2013;Hempson et al, 2017).…”