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

David W Thieltges,Tsukushi Kamiya,M Anouk Goedknegt,Katie O'Dwyer,Alistair M Senior

doi:10.1111/oik.06086

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.

Highlights

Trophic interactions are pivotal in driving population dynamics, community structure and the functioning of food webs (McCann 2011, Hanley and La Pierre 2015)
Our analysis provides a quantitative framework for identifying patterns in stable isotope discrimination factors of parasites and broadens our general understanding of trophic interactions
Our analyses revealed large variation in δ13C between consumers and their diet (Δ13C) and Δ15N isotope discrimination factors among the parasite species

Summary

Introduction

Trophic interactions are pivotal in driving population dynamics, community structure and the functioning of food webs (McCann 2011, Hanley and La Pierre 2015). Underlying an understanding of the manifold effects of trophic interactions on ecological processes is the knowledge of who eats whom In this respect, the analysis of naturally occurring stable isotopes has gained increasing popularity (Layman et al 2012, Traugott et al 2013). The difference in δ13C between consumers and their diet (Δ13C) is used to identify the diet source of carbon (e.g. terrestrial versus marine primary producers; Hobson 1986), and the difference in δ15N (trophic enrichment, Δ15N) is used to determine a consumer’s trophic position (Vander Zanden et al 1997) The latter is calculated based on the empirically derived average difference between consumers and their resources known as the trophic discrimination factor, or Δ15N. In predator– prey and herbivore–plant trophic interactions, the difference between one trophic level and the is assumed to be equivalent, on average, to a Δ15N of about 3.4‰ (Minagawa and Wada 1984, Vander Zanden et al 1997, Post 2002)

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