Alternative functional strategies and altered carbon pathways facilitate broad depth ranges in coral‐obligate reef fishes

Abstract

Spatial refuges in peripheral habitats will become increasingly important for species persistence as climate change and other disturbances progressively impact habitat quality and assemblage compositions. However, the capacity for persistence will be determined in part by species‐specific abilities to absorb costs related to altered or decreased quantities and quality of resources at range peripheries. We compared variations in dietary strategies and energy acquisition trade‐offs along depth gradients in two obligate corallivores that differ in level of diet specialization. We also assessed depth‐related changes in energy pathways and energy content of their mixotrophic prey. We found no changes in feeding effort or total resource availability (total coral cover) towards deep range margins, but availability of the preferred resource (Acropora coral) decreased. While both species selectively targeted Acropora, the more specialized species (Chaetodon baronessa) exhibited limited feeding plasticity along the depth gradient. The degree of selectivity towards the preferred coral increased rather than decreased with depth, being 40 times greater than expected, given availability, at their range periphery. In contrast, the generalist's diet (Chaetodon octofasciatus) varied greatly in response to changes in resource availability with depth. Unexpectedly, the energy content of Acropora did not decline with depth, likely due to increased coral heterotrophy in deeper water, indicated by shifts in their molecular isotope geochemistry. This shift was accompanied by a 20% increase in plankton‐sourced carbon in the muscle tissue of deep‐resident fish, despite no observations of direct feeding on plankton food sources. Our results indicate that deep ranges in coral‐obligate reef fishes are supported by multiple mechanisms of trophic versatility in both the fish and corals. This nutritional plasticity likely serves a compensatory role in the resilience and eventual adaptation of organisms at their range peripheries. For species vulnerable to increasing anthropogenic impacts at range cores, variable and multi‐trophic functional responses can act to buffer against costs and increase the refuge potential of range peripheries. Specialist consumers may also be supported indirectly at range margins via trophic plasticity within their preferred prey. A free Plain Language Summary can be found within the Supporting Information of this article.

Spatial subsidies drive sweet spots of tropical marine biomass production

“…To eliminate any reef inputs, “planktivorous” species that are also reliant on reef-based material were specifically excluded (see Methods ) and do not contribute towards our conclusions. Furthermore, we do not consider indirect trophic interactions that often result in pelagic energy incorporated by other guilds of fishes (e.g., [ 40 , 54 – 56 ]). Thus, our estimates of net production of planktivorous fishes provide a robust, time-integrated, yet conservative measure of realised spatial subsidies (i.e., after plankton consumption) to coral reef fish assemblages.…”

“…This definition of plankton/pelagic subsidies is narrower than the one used previously (e.g., [ 11 ]) but was required because of the vast number of species with uncertain or unavailable quantitative dietary information, as well as the large spatial scale of our study. This narrow definition excludes indirect trophic links that may also result in pelagic subsidies being incorporated by reef communities (e.g., preying on planktivorous fishes or heterotrophic corals, coprophagy of planktivore waste, feeding on plankton-enriched detritus [ 40 , 50 , 54 , 55 ]). Conversely, this definition may not completely exclude reef-based material consumed by planktivores (e.g., resuspended algae material, fish, and crustacean eggs, emerging zooplankton [ 39 , 73 , 76 ]).…”

Resource Niches of Co-occurring Invertebrate Species at an Offshore Wind Turbine Indicate a Substantial Degree of Trophic Plasticity

“…In general, the seven consumer species investigated here covered three different resource strategies: resource specialization (D. cincta), intermediate dietary shifts with depth (N. puber) and trophic plasticity (all five other consumers). When species are exposed to anthropogenic stress -as may for instance be increasingly the case as a consequence of climate change -flexible and differential resource strategies may provide them with (extra) spatial refuges and thus buffer their populations against costs imposed by the impacts of stressors on their environment (MacDonald et al, 2019). Our results extend the well-recognized importance of trophic plasticity as a major driver of vertical zonation in, for instance, shallow coral-reef (Palardy et al, 2008;Friedlander et al, 2010;Fox et al, 2019) and deep-sea communities (Carney, 2005) to hard-substrate fauna in shallow coastal waters, where zonation patterns are commonly explained in relation to predation, competition for space and food (the latter mostly among suspension feeders), and tolerance to environmental conditions toward the limits of a species' depth range (Kaiser et al, 2011).…”

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“…To eliminate any reef inputs, "planktivorous" species that are also reliant on reef-based material were specifically excluded (see Methods) and do not contribute towards our conclusions. Furthermore, we do not consider indirect trophic interactions that often result in pelagic energy incorporated by other guilds of fishes (e.g., [40,[54][55][56]). Thus, our estimates of net production of planktivorous fishes provide a robust, time-integrated, yet conservative measure of realised spatial subsidies (i.e., after plankton consumption) to coral reef fish assemblages.…”

“…previously (e.g., [11]) but was required because of the vast number of species with uncertain or unavailable quantitative dietary information, as well as the large spatial scale of our study. This narrow definition excludes indirect trophic links that may also result in pelagic subsidies being incorporated by reef communities (e.g., preying on planktivorous fishes or heterotrophic corals, coprophagy of planktivore waste, feeding on plankton-enriched detritus [40,50,54,55]). Conversely, this definition may not completely exclude reef-based material consumed by planktivores (e.g., resuspended algae material, fish, and crustacean eggs, emerging zooplankton [39,73,76]).…”