Does infection tilt the scales? Disease effects on the mass balance of an invertebrate nutrient recycler

Abstract

While parasites are increasingly recognized as important components of ecosystems, we currently know little about how they alter ecosystem nutrient availability via host-mediated nutrient cycling. We examined whether infection alters the flow of nutrients through hosts and whether such effects depend upon host diet quality. To do so, we compared the mass specific nutrient (i.e., nitrogen and phosphorus) release rates, ingestion rates, and elemental composition of uninfected Daphnia to those infected with a bacterial parasite, P. ramosa. N and P release rates were increased by infection when Daphnia were fed P-poor diets, but we found no effect of infection on the nutrient release of individuals fed P-rich diets. Calculations based on the first law of thermodynamics indicated that infection should increase the nutrient release rates of Daphnia by decreasing nutrient accumulation rates in host tissues. Although we found reduced nutrient accumulation rates in infected Daphnia fed all diets, this reduction did not increase the nutrient release rates of Daphnia fed the P-rich diet because infected Daphnia fed this diet ingested nutrients more slowly than uninfected hosts. Our results thus indicate that parasites can significantly alter the nutrient use of animal consumers, which could affect the availability of nutrients in heavily parasitized environments.

Exploited and excreting: parasite type affects host nutrient recycling

“…In diseased metazoans, it is difficult to separate the physiological origins of infection-induced reductions in ingestion and fecundity as just activating the immune system of the host can reduce host fecundity, alter feeding, and increase metabolism (Ahmed et al 2002, Bashir-Tanoli andTinsley 2014). Consistent with previous work in the same system (Frost et al 2008a, Narr andFrost 2015), P. ramosa-infected individuals possessed lower P content than their uninfected conspecifics in both the P-rich and intermediate P diets. Indeed, anorexia has been associated with increased survival of Trendlines are shown for diet treatments in which fecundity was considered a top predictor of nutrient release (delta AICc < 4) using second order Akaike's information criteria.…”

“…One reason for this may be that uninfected Daphnia fed the low quality diet produced fewer offspring than those fed higher quality diets, so that the effect of parasitism on the fecundity of poorly fed Daphnia was too small to alter their nutrient release rates (Fig. This explanation is consistent with a previous experiment, where diet-specific effects of parasitism on ingestion rate counteracted changes in body nutrient content and reduced differences in nutrient release between infected and uninfected individuals (Narr and Frost 2015). Nevertheless, we observed a positive relationship between fecundity and ingestion rate for Daphnia fed the low P diet.…”

“…To account for these differences, we adjusted the volume of media (and availability of algae) in our excretion (and ingestion) trials so that each mg of Daphnia (approximated from previous experiments; Narr and Frost 2015) was held in 11.5 mL of COMBO during the excretion experiment and so that each individual Daphnia was held in a standardized volume of COMBO (and amount of food) during the ingestion experiment. To do this, we held animals without food for 60 min and measured the increase in dissolved nutrient concentrations in their chambers over that time.…”

“…For example, in infected and uninfected mosquitos, fecundity and ingestion rates are often positively correlated (Hogg and Hurd, 1995). Given the strong effects of ingestion on nutrient release (Narr and Frost 2015), full resolution of parasite-driven changes in host nutrient use will require a better mechanistic understanding of the physiological connections between fecundity and ingestion rate. All three of these effects may simply be by-products of immune function or could also offer a selective advantage to diseased hosts in the face of parasitism.…”

“…In the latter case, the functional role of a parasite within an ecosystem is defined by its prevalence, the symptoms of its host, and the ecological role of host populations. Indeed, recent evidence indicates that parasitism can affect the rate at which consumers recycle nutrients (Bernot 2013, Narr andFrost 2015). Indeed, recent evidence indicates that parasitism can affect the rate at which consumers recycle nutrients (Bernot 2013, Narr andFrost 2015).…”