Stable nitrogen isotope analysis of amino acids as a new tool to clarify complex parasite–host interactions within food webs

Tijs Joling,Andreas M. Waser,Marcel T. J. van der Meer,David W. Thieltges,Lonneke L. IJsseldijk,Philip M. Riekenberg

doi:10.1111/oik.08450

Abstract

Traditional bulk isotopic analysis is a pivotal tool for mapping consumer–resource interactions in food webs but has largely failed to adequately describe parasite–host relationships. Thus, parasite–host interactions remain undescribed in food web frameworks despite these relationships increasing linkage density, connectance and ecosystem biomass. Compound‐specific stable isotopes from amino acids provides a promising novel approach that may aid in mapping parasite–host relationships in food webs. Here we apply a combination of traditional bulk stable isotope analyses and compound‐specific isotopic analysis of nitrogen in amino acids to examine resource use and trophic interactions of five parasites from three hosts from a marine coastal food web (Wadden Sea, European Atlantic). By comparing isotopic compositions of bulk and amino acid nitrogen, we aimed to characterize isotopic fractionation occurring between parasites and their hosts and to clarify parasite trophic positions. Our results indicate that parasitic trophic interactions were more accurately identified using compound‐specific stable isotope analysis due to removal of underlying source isotopic variation for both parasites and hosts. The compound‐specific method provided clearer trophic discrimination factors in comparison to bulk isotope methods. Amino acid compound specific isotope analysis has widely been applied to examine trophic position within food webs, but our analyses suggest that the method is particularly useful for clarifying the feeding strategies for parasitic species. Baseline isotopic information provided by source amino acids allows clear identification of the fractionation from parasite metabolism by integrating underlying isotopic variations from the host tissues. However, like for bulk isotope analysis, the application of a universal trophic discrimination factor to parasite–host relationships remains inappropriate for compound‐specific stable isotope analysis. Despite this limitation, compound‐specific stable isotope analysis is and will continue to be a valuable tool to increase our understanding of parasitic interactions in marine food webs.

Highlights

Bulk tissue stable isotope analysis is routinely applied to identify resource utilization and trophic interactions within food webs (Minagawa and Wada 1984, Fry 2006)
Pairwise t-tests and Wilcoxon tests describe δ13C and δ15N comparisons between parasites and host tissues as appropriate following Shapiro–Wilk tests for normality
This study identified considerable differences between Δ15N values determined for parasite–host pairings using bulk-SIA (Fig. 1) and AA-CSIA (Fig. 2–4) causing different Trophic positions (TP) estimates for parasites between techniques

Summary

Introduction

Bulk tissue stable isotope analysis (hereafter δ13Cbulk or δ15Nbulk and bulk-SIA) is routinely applied to identify resource utilization and trophic interactions within food webs (Minagawa and Wada 1984, Fry 2006). Application of system-wide or group-specific TDFs do not reliably account for parasite–host relationships, which have TDFs varying from −6.7‰ to 9.0‰ (Thieltges et al 2019) for δ15Nbulk These values fall well outside of the ranges typically observed for δ15Nbulk TDFs for consumers (McCutchan et al 2003, Mill et al 2007, Caut et al 2009) and span across parasitic species (Pinnegar et al 2001, Dubois et al 2009), feeding styles and host tissue specificity, indicating that TDFs for parasites may be specific to each relationship (Lafferty et al 2008, Thieltges et al 2019). Despite widespread occurrence of parasites throughout ecosystems, these relationships have been neglected during construction of food webs since they are often incompletely understood and/or described (Marcogliese and Cone 1997, Lafferty et al 2008). Incomplete characterizations of parasite–host relationships are due to the cryptic nature of interactions resulting from the difficulty of reliable sampling during the complex life-cycles of many parasite (Goater et al 2014)

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