Threshold elemental ratios and the temperature dependence of herbivory in fishes

Abstract

Herbivorous ectothermic vertebrates are more diverse and abundant at lower latitudes. While thermal constraints may drive this pattern, its underlying cause remains unclear. We hypothesized that this constraint stems from an inability to meet the elevated phosphorus demands of bony vertebrates feeding on P‐poor plant material at cooler temperatures because low gross growth efficiency at warmer temperatures facilitates higher P ingestion rates. We predicted that dietary carbon:phosphorus (C:P) should exceed the threshold elemental ratio between carbon and P‐limited growth (TERC:P) for herbivores feeding at cooler temperatures, thereby limiting the range of herbivorous ectothermic vertebrates facing P‐limited growth. We tested this hypothesis using the Andean suckermouth catfishes Astroblepus and Chaetostoma. Astroblepus are invertivores that inhabit relatively cool, high‐elevation streams while Chaetostoma are grazers that inhabit relatively warm, low‐elevation streams. We calculated TERC:P for each genus across its elevational range and compared these values to measured values of food quality over an elevational gradient in the Andes. We also broadly summarized measurements of TERC:P across diverse groups of fishes. Supporting our hypothesis, we found that dietary C:P was predicted to exceed the TERC:P for the grazer Chaetostoma near the highest elevation where this genus has been recorded. Conversely, the TERC:P for the invertivore Astroblepus was consistently higher than that of Chaetostoma and thus its dietary C:P never approached the TERC:P. We found that, among all fishes, omnivores had higher average TERC:P than invertivores, and TERC:P did not vary with temperature. Our results suggest that, at least for Andean suckermouth catfishes, cool temperatures constrain herbivory at higher elevations. Increased gross growth efficiency at cooler temperatures evidently restricts the ability of P‐limited consumers to meet P demand. However, our survey of fish TERC:P estimates suggests that some fishes are able to circumvent this constraint through behavioural and life‐history adaptations that reduce P demand or increase P use efficiency. The physiological trade‐offs underlying these functional shifts reveal that geographic dietary patterns can be predicted by stoichiometric theory, but variation in food quality and consumer traits that reduce P demand and/or increase P efficiency can create exceptions to these patterns. A plain language summary is available for this article.

Nutrient limitation, bioenergetics and stoichiometry: A new model to predict elemental fluxes mediated by fishes

“…There is a growing consensus that many fishes are limited by nutrients (Benstead et al, 2014;El-Sabaawi et al, 2016;Hood et al, 2005;Moody et al, 2019). Yet, fish growth and maintenance are often assumed to be limited by energy (C) when applying coupled bioenergetic and stoichiometric models (Allgeier et al, 2013;Burkepile et al, 2013;Kraft, 1992;Schindler & Eby, 1997).…”

“…Thus, applying the traditional approach of combining stoichiometry and bioenergetics (Kraft, 1992) to fish species that are limited by N or P normally results in biologically implausible predictions of excretion rates. Indeed, there is mounting evidence that fishes can be limited by nutrients, rather than energy (Benstead et al, 2014;El-Sabaawi et al, 2016;Hood, Vanni, & Flecker, 2005;Moody, Lujan, Roach, & Winemiller, 2019). While, negative predicted excretion rates can provide evidence for nutrient limitation (e.g.…”

Climate effects on fish body size–trophic position relationship depend on ecosystem type

“…On the other hand, cooler temperatures decreases TER C:nutrients , increasing the consumer demand for nutrient rich resources i.e. meat (Boersma et al 2016, Moody et al 2019. Carbon-limited organisms in warmer climates, therefore, should prefer to ingest a food source with higher carbon-to-nutrient ratio, while in colder temperatures nutrients should assume the limiting role (Moody et al 2019).…”

“…meat (Boersma et al 2016, Moody et al 2019. Carbon-limited organisms in warmer climates, therefore, should prefer to ingest a food source with higher carbon-to-nutrient ratio, while in colder temperatures nutrients should assume the limiting role (Moody et al 2019). In warmer waters, the preference to forage on carbon-rich resources can manifest for both carnivorous and omnivorous fish, as prey carbon-to-nutrient ratios tend to increase at lower trophic levels (Gonzalez et al 2011, Scharler et al 2015.…”

“…This may imply that larger consumers in tropical regions are required to feed more directly on plant, algae or detritus than their temperate counterparts, a prediction which agrees with the fact that digestion of plant tissue is easier at higher temperatures (Floeter et al 2005). On the other hand, lower temperatures change diet preferences and increase the need for other nutrients relative to carbon, therefore increasing the need for animal food sources (Boersma et al 2016, González-Bergonzoni et al 2016, Moody et al 2019. Therefore, the expected temperature sensitivity to food quality limitation might increase the incidence of herbivory/omnivory in larger consumers in the tropics, affecting the trophic position-body size relationship.…”