Parasites and stable isotopes: a comparative analysis of isotopic discrimination in parasitic trophic interactions

Abstract

Stable isotopes are widely used to identify trophic interactions and to determine trophic positions of organisms in food webs. Comparative studies have provided general insights into the variation in isotopic composition between consumers and their diet (discrimination factors) in predator–prey and herbivore–plant relationships while other major components of food webs such as host–parasite interactions have been largely overlooked. In this study, we conducted a literature‐based comparative analysis using phylogenetically‐controlled mixed effects models, accounting for both parasite and host phylogenies, to investigate patterns and potential drivers in Δ13C and Δ15N discrimination factors in metazoan parasitic trophic interactions. Our analysis of 101 parasite–host pairs revealed a large range in Δ13C (–8.2 to 6.5) and Δ15N (–6.7 to 9.0) among parasite species, with no significant overall depletion or enrichment of 13C and 15N in parasites. As previously found in other trophic interactions, we identified a scaling relationship between the host isotopic value and both discrimination factors with Δ13C and Δ15N decreasing with increasing host δ13C and δ15N, respectively. Furthermore, parasite phylogenetic history explained a large fraction (>60%) of the observed variation in the Δ15N discrimination factor. Our findings suggest that the traditional isotope ecology framework (using an average Δ15N of 3.4‰) applies poorly to parasitic trophic interactions. They further indicate the need for a scaled rather than a fixed trophic discrimination factor framework along gradients of host δ15N. We also identified several conceptual and methodological issues which should to be considered in future research to help integrate parasitic interactions into a holistic isotope ecology framework across diverse trophic interactions.

Impacts of host phylogeny, feeding styles, and parasite attachment site on isotopic discrimination in helminths infecting coral reef fish hosts

“…4), while no statistically significant within-pairings relationships were found for carbon (Supplementary Table 2). Negative scaling of trophic discrimination factors with increased host carbon and nitrogen values has previously been observed for parasite-host, predator-prey and herbivore-plant relationships 12,14,31 and may be associated with dietary quality. In this study, there appears to be an increased spread in the fractionation (Δ 15 N values) observed within the herbivore S. lineatus , with the lowest δ 15 N values occurring with the highest Δ 15 N values and a distinct grouping of individuals with lower Δ 15 N values corresponding with the highest δ 15 N values (Fig.…”

“…The relatively uniform neutral or negative relationships for Δ 13 C values across the pairings located from both the dietary tract and the general cavity indicate that lipid carbon is likely utilized to support tissue growth beyond species closely associated with fatty tissues (e.g. blood and liver) 13,14 . This relationship should be examined further with methods that incorporate metabolic pathway techniques for target species beyond model organisms targeted for pathogenicity 21,22 .…”

“…Stable isotope techniques are routinely utilized to study trophic relationships within food webs 8,9 by using trophic discrimination factors for carbon and nitrogen (Δ 13 C and Δ 15 N) to account for the stepwise increase in δ 13 C and δ 15 N (‰) that occurs between diet and consumer during metabolism 10–12 . However, parasites do not generally follow this relationship with parasite-host discrimination factors (Δ 13 C or Δ 15 N) observed ranging from considerably higher than typical trophic discrimination between predator and prey to negative values for Δ 13 C or Δ 15 N across a variety of taxa 1,13,14 .…”

“…Amongst helminths in fish hosts, cestodes and nematodes are usually depleted in δ 15 N values versus their hosts 13,15–17 and vary in Δ 13 C, while trematodes have been found to vary in both Δ 13 C and Δ 15 N 18,19 . However, there can also be considerable variation within these helminth groups 14,20 . Distinct differences for trophic discrimination in parasitic relationships are potentially caused by the combined effects of unique feeding ecologies, often reduced metabolic capabilities of the parasitic taxa being investigated 21,22 , and host metabolic effects due to parasitism 23 .…”

“…prey items, detritus, mucus, or blood 24 ). In addition, it has been suggested that trophic discrimination factors of parasites may not be fixed but scale with the isotopic signature of their hosts, both within 25 and among parasite species 14 .…”