Stable isotopes unravel the feeding mode–trophic position relationship in trematode parasites

Abstract

1. Stable isotopes have been sporadically used over the last two decades to characterise host-parasite trophic relationships. The main reason for this scarcity is the lack of an obvious pattern in the ratio of nitrogen stable isotope values (δ 15 N) of parasites in comparison to their host tissues, which would be key to understand any host-parasite system dynamics.2. To circumvent this, we focused on a single snail host, Zeacumantus subcarinatus, and three of its trematode parasites.3. We used stable isotopes to investigate each host-trematode trophic relationship and shed light on the mechanisms utilised by the parasite to reroute its hosts' biomass.4. All our trematodes were found to be 15 N-enriched compared to their host, with their δ 15 N values strongly related to their feeding behaviours: passive versus active. It was possible to 'rank' these parasite species and assess their 'relative' trophic position using δ 15 N values. We also demonstrated that including a broader range of samples (e.g. host food and faeces, multiple parasite life stages) helped understand the metabolic mechanisms used by the various participants, and that using carbon stable isotope values and C:N ratios allowed to identify an important lipid requirement of these trematode parasites. Finally, we show how critical it is to not ignore parasitic infections as they can have a great influence on their host's trophic position.5. We have shown that by focussing on a single host species and a single taxonomic group of parasites, we can remove a certain amount of variation recorded by broader isotope studies. We hope that these data will ultimately improve our ability to place parasites in food webs, and thus improve our understanding of the connections and interactions that dictate food web dynamics.

Unravelling the trophic interaction between a parasitic barnacle (Anelasma squalicola) and its host Southern lanternshark (Etmopterus granulosus) using stable isotopes

“…Nevertheless, these results are aligned with other studies looking at 'absorptive' parasites such as acanthocephalan (Nachev et al, 2017) or cestodes (Power and Klein, 2004;Finn et al, 2022), challenging the classic framework of predator-prey relationships (i.e. δ 15 N enrichment from prey to predator) (Thieltges et al, 2019;Kamiya et al, 2020;Sabadel and MacLeod, 2022). The correlations of each measured variable (stable isotope values and elemental compositions) with barnacle sizes could be indicative of a metabolic shift leading to different nutrient requirements between developing and fully grown organisms.…”

“…Nevertheless, these results are aligned with other studies looking at ‘absorptive’ parasites such as acanthocephalan (Nachev et al ., 2017 ) or cestodes (Power and Klein, 2004 ; Finn et al ., 2022 ), challenging the classic framework of predator–prey relationships (i.e. δ 15 N enrichment from prey to predator) (Thieltges et al ., 2019 ; Kamiya et al ., 2020 ; Sabadel and MacLeod, 2022 ).…”

“…Indeed, carbon isotopic ratios do not vary considerably with each trophic level (~1‰), allowing the use of this element as a tracer of organic matter source (Post, 2002 ; Fry, 2006 ). Moreover, the relative depletion in δ 13 C values is correlated with the presence of lipids, an important food resource for marine parasites (Sabadel and MacLeod, 2022 ). Similarly, δ 34 S values, mainly represented by 2 amino acids, cysteine and methionine, in organic tissues show little change with trophic transfer (Peterson et al ., 1985 ; Krouse, 1991 ).…”

Deciphering the complex trophic relationship of the black-spotted croaker (Teleostei: Sciaenidae) and its parasites using stable isotope analysis

“…The analysis of parasite carbon isotope signatures can also be effective in food web studies, allowing researchers to identify the specific diet source of carbon that the parasite has consumed (Fry 2006;Sabadel et al 2019;Gilbert et al 2020b;Sabadel and MacLeod 2022). The isotopic turnover rates, and subsequent signatures of carbon (δ 13 C) are used as tracers of diet sources within an organism, or its host (Vander Zanden et al 1997;Guillemin et al 2022).…”

“…Trophic discrimination factors for nitrogen and carbon are used in ecological studies to characterise trophic relationships and determine pathways of nutrient assimilation. Specifically, the trophic discrimination factor of nitrogen (TDFN) is used to determine trophic levels, while the trophic discrimination factor of carbon (TDFC) is used to identify the dietary source of carbon that an organism consumes, based on stable isotope data (Riekenberg et al 2021;Sabadel and MacLeod 2022).…”