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

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

doi:10.1111/oik.08450

Cited by 9 publications

(4 citation statements)

References 82 publications

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“…Finally, size‐dependent diet preference or ontogenetic diet shift, which are known to alter TP, especially those of carnivorous species (Sánchez‐Hernández et al., 2017), and other species interactions that drive trophic transfer of energy, such as host–parasite relationships (Lafferty et al., 2006), were partially but not fully considered in our study. These unexplored research areas could be addressed using cutting‐edge toolboxes such as CSIA‐AA (Riekenberg et al., 2021).…”

Section: Discussionmentioning

confidence: 99%

Integrated trophic position as a proxy for food‐web complexity

Ishikawa,

Takashima,

Maruoka

et al. 2023

Methods Ecol Evol

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There are two distinct approaches to describing the distributions of biomass and species in food webs: one to consider them as discrete trophic levels (TLs); and the other to consider them as continuous trophic positions (TPs). Bridging the gap between these two perspectives presents a nontrivial challenge in integrating biodiversity and food‐web structure. Food network unfolding (FNU) is a technique used to bridge this gap by partitioning the biomass of species into integer TLs to compute three complexity indices, namely vertical (DV), horizontal (DH) and range (DR) diversity (D indices), through decomposition of Shannon's index H′. Using FNU, the food web (a network of species with unique TPs) is converted to a linear food chain (a biomass distribution at discrete TLs). This enables us to expect that the unfolded biomass within species decreases exponentially as the TL increases. Under this condition, the mean TL value in unfolded food chains is hypothesized to have an exponential relationship with the vertical diversity, DV. To explore this, we implemented FNU and calculated D indices for food webs publicly available at EcoBase (n = 158) and calculated the integrated TP (iTP), defined as the biomass‐weighted average TP of a given food web. The iTP corresponds to the mean TL in unfolded food chains and can be empirically measured through compound‐specific isotope analysis of amino acids (CSIA‐AA). Although our analysis is biased towards marine ecosystems, we revealed an exponential relationship between iTP and DV, suggesting that iTP can serve as a measurable proxy for DV. Furthermore, we found a positive correlation between the iTP observed in the total communities (total iTP) and the iTPs of partial communities consisting only of species with 2.0 ≤ TP < 3.0 (partial iTP; r2 = 0.48), suggesting that DV can be predicted using partial iTP. Our findings suggest that the net effect of species diversity, excluding the effect of biomass (corresponding to H′ − DV), on food‐web complexity can be revealed by combining CSIA‐AA with biodiversity analysis (e.g. environmental DNA).

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Section: Discussionmentioning

confidence: 99%

Integrated trophic position as a proxy for food‐web complexity

Ishikawa,

Takashima,

Maruoka

et al. 2023

Methods Ecol Evol

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“…This would allow confirming that protein and lipid demands – and subsequent host-to-parasite nutrient fluxes – do change with growth or reproduction status of the barnacle. In addition, compound-specific stable isotopic analysis (CSIA) of amino acids could also be powerful to ascertain the effect of metabolism on parasite's isotopic ratio and could help tease apart enzymatic activities (Sabadel et al ., 2019 ; Riekenberg et al ., 2021 b ), while CSIA of fatty acid (e.g. polysaturated long-chain fatty acids) could shed light on the routing of lipid from host to parasite (Twining et al ., 2020 ).…”

Section: Discussionmentioning

confidence: 99%

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

Sabadel

Cresson²,

Finucci³

et al. 2022

Parasitology

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The parasitic barnacle, Anelasma squalicola, is a rare and evolutionary fascinating organism. Unlike most other filter-feeding barnacles, A. squalicola has evolved the capability to uptake nutrient from its host, exclusively parasitizing deepwater sharks of the families Etmopteridae and Pentanchidae. The physiological mechanisms involved in the uptake of nutrients from its host are not yet known. Using stable isotopes and elemental compositions, we followed the fate of nitrogen, carbon and sulphur through various tissues of A. squalicola and its host, the Southern lanternshark Etmopterus granulosus, to better understand the trophic relationship between parasite and host. Like most marine parasites, A. squalicola is lipid-rich and clear differences were found in the stable isotope ratios between barnacle organs. It is evident that the deployment of a system of ‘rootlets’, which merge with host tissues, allows A. squalicola to draw nutrients from its host. Through this system, proteins are then rerouted to the exterior structural tissues of A. squalicola while lipids are used for maintenance and egg synthesis. The nutrient requirement of A. squalicola was found to change from protein-rich to lipid-rich between its early development stage and its definitive size.

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“…Consequently, stable isotopes could provide insight into parasite‐related effects on the ecology of their host. Yet few studies have assessed the effects of macroparasite infections on the isotopic signature and niche structure of definitive hosts as well as its functional significance (Britton and Andreou 2016; Gilbert et al ., 2020; Riekenberg et al ., 2021).…”

Section: Introductionmentioning

confidence: 99%

Narrower isotopic niche size in fish infected by the intestinal parasitePomphorhynchussp. compared to uninfected ones

Molbert

Goutte

2022

Journal of Fish Biology

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Examples of parasite-related effects on intermediate crustacean hosts are numerous but their ecological consequences on their vertebrate hosts are scarce. Here, we address the role of macroparasite infections on the trophic niche structure of definitive hosts and its potential physiological consequences using wild fish populations infected with an acantochephalan parasite Pomphorhynchus sp., a trophically-transmitted intestinal worm. Infected and uninfected fish were sampled from six populations on the Marne River, France and the prevalence of intestinal parasites in the host populations ranged from 50% to 90%. Although the isotopic ratios (δ 13 C and δ 15 N) did not differ between infected and uninfected fish, we found a consistent pattern of isotopic niche size being considerably smaller in infected hosts when compared with non-infected ones. This was not explained by interindividual differences in intrinsic factors such as length/age or body condition between infected and uninfected fish.These results suggest a potential niche specialization of infected fish, which did not impair their energetic status.

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

Cited by 9 publications

References 82 publications

Integrated trophic position as a proxy for food‐web complexity

Integrated trophic position as a proxy for food‐web complexity

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

Narrower isotopic niche size in fish infected by the intestinal parasitePomphorhynchussp. compared to uninfected ones

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