The Effect of Digestive Capacity on the Intake Rate of Toxic and Non-Toxic Prey in an Ecological Context

Abstract

Digestive capacity often limits food intake rate in animals. Many species can flexibly adjust digestive organ mass, enabling them to increase intake rate in times of increased energy requirement and/or scarcity of high-quality prey. However, some prey species are defended by secondary compounds, thereby forcing a toxin limitation on the forager’s intake rate, a constraint that potentially cannot be alleviated by enlarging digestive capacity. Hence, physiological flexibility may have a differential effect on intake of different prey types, and consequently on dietary preferences. We tested this effect in red knots (Calidris canutus canutus), medium-sized migratory shorebirds that feed on hard-shelled, usually mollusc, prey. Because they ingest their prey whole and crush the shell in their gizzard, the intake rate of red knots is generally constrained by digestive capacity. However, one of their main prey, the bivalve Loripes lucinalis, imposes a toxin constraint due to its symbiosis with sulphide-oxidizing bacteria. We manipulated gizzard sizes of red knots through prolonged exposure to hard-shelled or soft foods. We then measured maximum intake rates of toxic Loripes versus a non-toxic bivalve, Dosinia isocardia. We found that intake of Dosinia exponentially increased with gizzard mass, confirming earlier results with non-toxic prey, whereas intake of Loripes was independent of gizzard mass. Using linear programming, we show that this leads to markedly different expected diet preferences in red knots that try to maximize energy intake rate with a small versus a large gizzard. Intra- and inter-individual variation in digestive capacity is found in many animal species. Hence, the here proposed functional link with individual differences in foraging decisions may be general. We emphasize the potential relevance of individual variation in physiology when studying trophic interactions.

Individual diet differences in a molluscivore shorebird are associated with the size of body instruments for internal processing rather than for feeding

“…The latter was already known for red knots, but it is exciting to note that the exponent of 2.00 found in the current study (Fig. F) exactly matches the exponent found in two red knot studies (van Gils et al , Oudman et al ).…”

“…This study was carried out during April–May at the Yalu Jiang coastal wetland (39°40′–39°58′N, 123°34′–124°07′E), Liaoning, China (Zhang et al 2019a). About 44 000 great knots (Zhang et al ) stage here for nearly two months during northward migration (Ma et al 2013, Choi et al , Tan et al ). From the end of March, local fishermen set up many kilometers of very fine, almost invisible, monofilament nets to catch Mantis shrimp Oratosquilla oratoria in the lower intertidal zone.…”

Stomach fullness shapes prey choice decisions in crab plovers (Dromas ardeola)

“…The observed switch in prey choice could thus potentially also be explained by foragers aiming at achieving nutritional targets, or foragers being limited by toxic constraints. However, given that maximum intake rates in terms of ash were equal for both prey species, we don’t expect one of our prey species to be toxic [ 37 ]. Furthermore, studies showing that carnivores balance their diet based on nutrients do not report sudden shifts, as we observed in crab plovers, but rather show a balanced mixed diet [ 38 , 39 ] or a switch over relatively long time periods, i.e.…”

The Impact of Detoxification Costs and Predation Risk on Foraging: Implications for Mimicry Dynamics

“…Toxin mutualism is where sympatric prey species benefit from using the same toxin even if they are visually distinguishable and unequally toxic, and it has been demonstrated in starlings ( Sturnus vulgaris ), with a recent experiment showing that they reduce their ingestion of two unequally toxic live prey types when they co-occur compared to when they don’t [15]. This is because predators can only ingest a certain amount of a toxin in any given time period (toxin saturation theory'; [59]), and it could be due to either physiological constraints or the excessive costs of processing toxins; for example, red knots ( Calidris canutus canutus ) appear to be toxin-limited when feeding on the toxic bivalve Loripes lucinalis [60]. However, the reduced mortality of both toxic prey types may also be explained by the increased amount of energy available to the predators when there are three prey types compared to only two.…”