Bottom‐up and trait‐mediated effects of resource quality on amphibian parasitism

Abstract

Leaf litter subsidies are important resources for aquatic consumers like tadpoles and snails, causing bottom-up effects on wetland ecosystems. Recent studies have shown that variation in litter nutritional quality can be as important as litter quantity in driving these bottom-up effects. Resource subsidies likely also have indirect and trait-mediated effects on predation and parasitism, but these potential effects remain largely unexplored. We generated predictions for differential effects of litter nutrition and secondary polyphenolic compounds on tadpole (Lithobates sylvatica) exposure and susceptibility to Ribeiroia ondatrae, based on ecological stoichiometry and community-ecology theory. We predicted direct and indirect effects on key traits of the tadpole host (rates of growth, development and survival), the trematode parasite (production of the cercaria infective stages) and the parasite's snail intermediate host (growth and reproduction). To test these predictions, we conducted a large-scale mesocosm experiment using a natural gradient in the concentrations of nutrients (nitrogen) and toxic secondary compounds (polyphenolics) of nine leaf litter species. To differentiate between effects on exposure vs. susceptibility to infection, we included multiple infection experiments including one with constant per capita exposure. We found that increased litter nitrogen increased tadpole survival, and also increased cercaria production by the snail intermediate hosts, causing opposing effects on tadpole per capita exposure to trematode infection. Increased litter polyphenolics slowed tadpole development, leading to increased infection by increasing both their susceptibility to infection and the length of time they were exposed to parasites. Based on these results, recent shifts in forest composition towards more nitrogen-poor litter species should decrease trematode infection in tadpoles via density- and trait-mediated effects on the snail intermediate hosts. However, these shifts also involve increased abundance of litter species with high polyphenolic levels, which should increase trematode infection via trait-mediated effects on tadpoles. Future studies will be needed to determine the relative strength of these opposing effects in natural wetland communities. [Correction added after online publication on 5 January 2017: wording changed to 'which should increase trematode infection via trait-mediated effects on tadpoles'.].

Nitrogen and Phosphorus Retranslocation of Leaves and Stemwood in a Mature Eucalyptus Forest Exposed to 5 Years of Elevated CO2

“…However, N-limitation can occur more frequently than P-limitation in geologically young soils (LeBauer and Treseder, 2008); whereas P-limitation tends to be more prevalent in old, highly weathered soils (Walker and Syers, 1976; Vitousek et al, 2004; Turner et al, 2013). In green leaves, N and P concentrations are important not only because of their functional relationships to photosynthetic assimilation rates and growth (Aerts and Chapin, 2000; Wright et al, 2004; Ågren, 2008), but also because they may regulate carbon (C) and nutrient cycles and food webs in terrestrial ecosystems (Chapin et al, 2011).…”

“…The decrease in N:P in response to elevated CO 2 has been explained by the observation that N concentrations may be more sensitive to elevated CO 2 than P-concentrations, something that has primarily been observed in N-limiting ecosystems (Feng et al, 2015; Huang et al, 2015). However, the importance of P dynamics in elevated CO 2 is less clear, and the assumption of a homeostatic N:P ratio in elevated CO 2 due to similar proportional N and P responses needs to be tested (Ågren, 2008; Goll et al, 2012; Zhang et al, 2014). Given the potential for elevated CO 2 to change stoichiometric ratios (Sardans et al, 2012; Deng et al, 2015; Yuan and Chen, 2015), it is critical to understand how elevated CO 2 affects plant N:P ratios to evaluate nutrient limitations in terrestrial ecosystems in the future.…”

Reviewing the role of plant litter inputs to forested wetland ecosystems: leafing through the literature

“…However, those same leachates might also slow host development, increase the duration of parasite exposure, and subsequently increase parasite loads (Stephens et al. , Dodd and Buchholz ). Research indicates that the composition and chemistry of leaf litter inputs to a forested wetland might act as an environmental filter that selects for specific species and ecological interactions (Earl et al.…”

Bottom‐up trait‐mediated indirect effects decrease pathogen transmission in a tritrophic system

“…, Stephens et al. ). For instance, insect host–pathogen interactions may be dictated by the resource quality of the plant on which the insect feeds such that resource quality determines whether the insect becomes infected or not (Hunter and Schultz , Cory and Hoover , Elderd et al.…”

“…While for generalists, changes in resource quality due to induction may decrease herbivore performance, induced plant defenses can have important indirect effects on upper trophic levels and may change the interaction between a predator and its prey (Ohgushi 2012, Kersch-Becker andThaler 2015) as well as between a host and its pathogen (Hall et al 2009. Thus, changes in plant resource quality can have cascading consequences for other actors in the system via TMIEs (Werner and Peacor 2003, Stephens et al 2017. For instance, insect hostpathogen interactions may be dictated by the resource quality of the plant on which the insect feeds such that resource quality determines whether the insect becomes infected or not (Hunter and Schultz 1993, Cory and Hoover 2006.…”