Examination of the effects of toxicity and nutrition on a two-prey one-predator system with a metabolomics-inspired model

Abstract

Mercury (Hg) sequestration by phytoplankton results in intracellular concentrations that are multiple times greater than ambient water levels, and therefore the consumption of contaminated phytoplankton by herbivorous zooplankton, such as Daphnia, and their inefficient excretion of methylmercury (MeHg) can mediate the transfer to higher trophic levels. Employing a modified version of a metabolomics-inspired Daphnia ecophysiological model, the present study introduces two prey species to a simple Lotka-Volterra predator-prey system in order to shed light on the implications for the integrity of zooplankton assemblages, when experiencing multiple prey items of different toxicity and nutritional quality. We also examine the capacity of adaptive strategies of the predator (homeostatic rigidity, energetic investments to cope with toxicity) to shape predator-prey interactions. Our analysis suggests that the degree of nutritional quality of the prey items is a predominant driver of the predator-prey relationships, shifting from prey- to predator-dominated food webs with increasing nutritional quality. Increasing prey nutritional content leads to the emergence of oscillatory behaviour, which can be further modulated by the growth rates and degree of toxicity of different prey species. Severe exposure to contamination could lead to a decline of the predator biomass with faster growth rates of low nutritional quality prey, even though the increase of its MeHg somatic quota is only modest. In stark contrast, when a prey assemblage of superior nutritional quality prevails in an environment of elevated toxicity, faster prey growth rates are conducive to higher predator biomass levels, albeit its distinctly higher internal contaminant content. Owing to the heightened somatic growth dilution, the ingestion of carbon and nutritional metabolites is significantly higher relative to the MeHg intake rates, which leads to faster net growth of the predator and thus reinforces the benefits brought about by the nutritional value of their diet. Our results suggest that the homeostatic rigidity of the predator can assist in coping with toxic exposure. With a tighter range between the minimum and optimum somatic quotas, the predator population appears to be more resilient and its decline begins at higher levels of MeHg exposure. The predator-prey system displays a greater propensity for oscillatory behaviour, with their amplitude being driven by the interplay between the degree of saturation for nutritionally beneficial metabolites, and the energetic investments allotted to cope with toxicity and/or the excretion of excess metabolic by-products. We conclude by highlighting the prospect of our modelling work to guide new directions of research, to test a multitude of hypotheses pertaining to various ecophysiological facets of predator-prey systems, and extend its use to other contexts, such as the implications of toxin-producing algae for the predator physiology.