Consuming Costly Prey: Optimal Foraging and the Role of Compensatory Growth

Abstract

Some prey are exceptionally difficult to digest, and yet even non-specialized animals may consume them—why? Durophagy, the consumption of hard-shelled prey, is thought to require special adaptations for crushing or digesting the hard shells to avoid the many potential costs of this prey type. But many animals lacking specializations nevertheless include hard-bodied prey in their diets. We describe several non-mutually exclusive adaptive mechanisms that could explain such a pattern, and point to optimal foraging and compensatory growth as potentially having widespread importance in explaining costly-prey consumption. We first conducted a literature survey to quantify the regularity with which non-specialized teleost fishes consume hard-shelled prey: stomach-content data from 325 teleost fish species spanning 82 families (57,233 stomach samples) demonstrated that non-specialized species comprise ~75% of the total species exhibiting durophagy, commonly consuming hard-shelled prey at low to moderate levels (~10–40% as much as specialists). We then performed a diet survey to assess the frequency of molluscivory across the native latitudinal range of a small livebearing fish, Gambusia holbrooki, lacking durophagy specializations. Molluscivory was regionally widespread, spanning their entire native latitudinal range (>14° latitude). Third, we tested for a higher frequency of molluscivory under conditions of higher intraspecific resource competition in Bahamian mosquitofish (Gambusia spp.). Examining over 5,300 individuals, we found that molluscivory was more common in populations with higher population density, suggesting that food limitation is important in eliciting molluscivory. Finally, we experimentally tested in G. holbrooki whether molluscivory reduces growth rate and whether compensatory growth follows a period of molluscivory. We found that consumption of hard-shelled gastropods results in significantly reduced growth rate, but compensatory growth following prior snail consumption can quickly mitigate growth costs. Our results suggest that the widespread phenomenon of costly-prey consumption may be partially explained by its relative benefits when few alternative prey options exist, combined with compensatory growth that alleviates temporary costs.

Resource competition explains rare cannibalism in the wild in livebearing fishes

“…In total, we examined 8,081 adult Bahamian mosquitofish. Cannibalism was assessed using x‐ray imaging as described above for 7,586 fish, while we conducted a direct examination of gut contents during diet analyses for 495 additional fish (all from Abaco Island; see Araújo et al, 2014; Langerhans et al, 2021). We further dissected and visually examined the guts of 1,680 of the x‐rayed specimens as part of life‐history and/or diet analyses (716 from tidal creeks, 882 from blue holes, 82 from ponds; e.g., see Riesch et al, 2013; Riesch et al, 2015; Riesch et al, 2016, Riesch et al, 2020).…”

“…Widespread fragmentation of Bahamian tidal creeks throughout The Bahamas, primarily caused by road construction (mostly during the 1960s and 1970s), has resulted in severe restriction of hydrological connectivity with the ocean. This pervasive ecosystem fragmentation has caused strong and consistent ecological changes in tidal creeks—for example, reduced tidal exchange, reduced species diversity, increased density of Gambusia , decreased density (or extirpation) of piscivorous fish (e.g., Layman et al, 2004; Valentine‐Rose et al, 2007a, 2007b)—and led to a number of phenotypic shifts in Bahamian mosquitofish (e.g., Giery et al, 2015; Heinen‐Kay et al, 2014; Jenkins et al, 2021; Riesch et al, 2015), including dietary changes (Araújo et al, 2014; Langerhans et al, 2021). Prior work has characterized many of these tidal creeks regarding the population density of Gambusia and the density of predatory fish using visual surveys, and we aimed to use general linear models to test for associations between these variables and cannibalism in this study ( N = 3,173 specimens from 24 fragmented and 22 unfragmented tidal creeks).…”

“…Specifically, we dissected each fish, removed reproductive tissues, and examined the gut under a stereo microscope for the presence of a conspecific that had been eaten. For the invasive populations, we assessed cannibalism by capturing a digital x‐ray image of each fish in the lateral perspective using a custom‐built digital x‐ray unit comprising a micro‐focus x‐ray source (Hamamatsu L6731‐01) and a digital x‐ray detector (PaxScan 2520E) housed in a lead‐shielded cabinet (e.g., see Beckmann et al, 2015; Langerhans et al, 2021). We inspected each image for the presence/absence of fish within the guts: consumed fish were visible in the x‐ray images due to their dense otoliths, vertebrae, and skulls (body outline also often visible).…”

“…All G. affinis were photographed for measurement of standard length (SL, using the program tpsDig2 ver. 2.14,Rohlf, 2009) and weighed to the nearest 0.0001 g the day before they were introduced into mesocosms; all surviving G. affinis were collected and re-weighed at the conclusion of the experiment to measure their change in weight.These methods for body-size estimation have been shown to have very low measurement error (i.e., very high repeatability measured as intraclass correlation coefficient;Langerhans et al, 2021). To estimate average weight change per replicate, we first subtracted the initial weight from the final weight of each individual, and then regressed this against log 10 -transformed SL and saved the residuals.…”

Examination of the Trexler-DeAngelis Model of Maternal Provisioning Reveals That Matrotrophy Is Costly

“…First, stomachs of females could be quite full, but most of their content may be of low nutritional value. For instance, females may have consumed abundant sediment or shells of mollusks that provide little to no energy (Langerhans et al, 2021). If this were the case, stomach fullness may not be correlated with the actual availability of nutritious food items.…”