Stable-isotope analysis: a neglected tool for placing parasites in food webs

Sabadel, Amandine; Stumbo, Anthony D.; MacLeod, Colin D.

doi:10.1017/s0022149x17001201

Cited by 25 publications

(25 citation statements)

References 52 publications

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“…The decrease in the number of nematode taxa with invasion, with lower richness in invaded (no-removal treatment) compared to uninvaded (seedling-removal treatment) plots, is consistent with the decrease in diversity of nematodes and other invertebrates caused by other invasive species [47,48], including other pine species [24], although the opposite pattern has also been observed [49]. In addition, nematode communities from invaded plots differed in taxa composition, suggesting that P. contorta exerts a selective pressure over the soil nematode taxa that can inhabit the soil.…”

Section: Discussionsupporting

confidence: 61%

Community- and trophic-level responses of soil nematodes to removal of a non-native tree at different stages of invasion

et al. 2020

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Success of invasive non-native plant species management is usually measured as changes in the abundance of the invasive plant species or native plant species following invader management, but more complex trophic responses to invader removal are often ignored or assumed. Moreover, the effects of invader removal at different stages of the invasion process is rarely evaluated, despite a growing recognition that invader impacts are density or stage-dependent. Therefore, the effectiveness of invasive species management for restoring community structure and function across trophic levels remains poorly understood. We determined how soil nematode diversity and community composition respond to removal of the globally invasive tree species Pinus contorta at different stages of invasion by reanalysing and expanding an earlier study including uninvaded vegetation (seedlings removed continuously), early invader removal (saplings removed), late removal (trees removed), and no removal (invaded). These treatments allowed us to evaluate the stage-dependent belowground trophic responses to biological invasion and removal. We found that invaded plots had half the nematode taxa richness compared to uninvaded plots, and that tree invasion altered the overall composition of the nematode community. Differences in nematode community composition between uninvaded nematode communities and those under the tree removal strategy tended to dilute higher up the food chain, whereas the composition of uninvaded vs. sapling removal strategies did not differ significantly. Conversely, the composition of invaded compared to uninvaded nematode communities differed across all trophic levels, altering the community structure and function. Specifically, invaded communities were structurally simplified compared to uninvaded communities, and had a higher proportion of short life cycle nematodes, characteristic of disturbed environments. We demonstrate that a shift in management strategies for a globally invasive tree species from removing trees to earlier removal of saplings is needed for maintaining the composition and structure of soil nematode communities to resemble uninvaded conditions.

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Section: Discussionsupporting

confidence: 61%

Community- and trophic-level responses of soil nematodes to removal of a non-native tree at different stages of invasion

et al. 2020

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“…Hence, whether this mechanism is really the driving force behind the negative scaling pattern observed in parasitic trophic interactions remains to be investigated. Compound-specific isotope analysis of amino acids (CSIA-AA) may be a promising tool in this respect, as it may help to not only reveal the exact trophic position of hosts but also of parasites (Steffan et al 2013, Sabadel et al 2019. In any case, the existence of a negative scaling of Δ 15 N of parasite species with the δ 15 N of their hosts suggests that a scaled rather than a fixed, discrimination factor framework may be needed to be able to include parasites in traditional isotopic food web studies.…”

Section: Modelmentioning

confidence: 99%

“…This calls for more experimental work on parasitic trophic interactions and the potentially mediating environmental factors, similar to what has been increasingly applied in studies on other consumer-resource interactions (Gannes et al 1997, Martínez del Rio et al 2009, Wolf et al 2009). Using compound-specific isotope analysis of amino acids (CSIA-AA) rather than the traditional bulk isotope analysis may provide further insights into the trophic position of parasites (Steffan et al 2013, Sabadel et al 2019. A better understanding of potential methodological issues and of the ecological drivers mediating discrimination factors in parasitic trophic interactions will allow for stronger inference in respect to feeding relationships of parasites and their trophic positions in food webs.…”

Section: Modelmentioning

confidence: 99%

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

Thieltges

Goedknegt

O’Dwyer³

et al. 2019

Oikos

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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.

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“…Since the late 1970's analysis of natural levels of stable isotopes of nitrogen ( 15 N/ 14 N) and carbon ( 13 C/ 12 C) have been used as a unique fingerprint for studying trophic relationships of organisms [1][2][3].…”

Section: Introductionmentioning

confidence: 99%

“…In ecosystems, parasites are functionally important in shaping and stabilising the structure of food webs [8,[10][11][12]. Parasites are in turn also affected by the structure of food webs [13] as many parasites rely on trophic interactions between organisms for their transmission [14].…”

Section: Introductionmentioning

confidence: 99%

Stable isotope analysis spills the beans about spatial variance in trophic structure in a fish host – parasite system from the Vaal River System, South Africa

Gilbert

Nachev

Jochmann

et al. 2019

Preprint

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BackgroundStable isotope analysis offers a unique tool for comparing trophic interactions and food web architecture in ecosystems. This approach is based on analysis of the stable isotope ratios of carbon (13 C/ 12 C) and nitrogen (15 N/ 14 N) in organisms. Studies comparing stable isotope enrichment in hosts and parasites have shown that parasites are variably enriched in stable isotopes relative to the host.MethodsSharptooth catfish (Clarias gariepinus) were collected from six sites along the Vaal River, South Africa and were assessed for ectoparasites and endoparasites. Lamproglena clariae (Copepoda), Tetracampus ciliotheca and Proteocephalus glanduligerus (Cestoda), and larval Contracaecum sp. (Nematoda) were collected from the gills, intestine and mesenteries, respectively. Signatures of δ 13 C and δ 15 N were analysed in host muscle tissue and parasites using bulk stable isotope analysis.ResultsStable isotope enrichment was variable between parasites and the host fish, with L. clariae and the host sharing similar δ 15 N signatures and the endoparasites being depleted in both δ 13 C and δ 15 N relative to the host. Spatial differences in enrichment of stable isotopes were also identified. Fish and parasites collected from below the Vaal River Barrage were more enriched in the 15 N isotope than hosts and parasites collected from other sites. The opposite was identified for 13 C isotope fractionation.ConclusionDifferences in stable isotope enrichment in parasites infecting C. gariepinus could be related to the feeding strategy of each parasite species collected. Enrichment of δ 15 N in L. clariae would relate to the micropredatory nature of this parasite, which feeds on whole blood of the host fish. Depleted isotope levels in endoparasites could relate to their absorptive feeding strategy on metabolic by-products of the host. Spatial differences in both host and parasite tissues identified likely resulted from differences in the diet of the host and related with availability of prey items for the host fish.

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Stable-isotope analysis: a neglected tool for placing parasites in food webs

Cited by 25 publications

References 52 publications

Community- and trophic-level responses of soil nematodes to removal of a non-native tree at different stages of invasion

Community- and trophic-level responses of soil nematodes to removal of a non-native tree at different stages of invasion

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

Stable isotope analysis spills the beans about spatial variance in trophic structure in a fish host – parasite system from the Vaal River System, South Africa

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