Stable Isotope Dynamics of Herbivorous Reef Fishes and Their Ectoparasites

Abstract

Acanthurids (surgeonfishes) are an abundant and diverse group of herbivorous fishes on coral reefs. While their contribution to trophic linkages and dynamics in coral reef systems has received considerable attention, the role of linkages involving their parasites has not. As both consumers of fish tissue and prey to microcarnivores, external parasites may play a significant role in trophic transfer between primary consumers (and hence their predominantly algae-based diet) and the broader coral reef community. Stable isotope analysis is a common tool for studying trophic linkages which can be used for studies involving parasites. We examined the stable isotope ecology (13C and 15N) of copepod (Caligus atromaculatus) and monogenean (Neobenedenia sp.) ectoparasites collected from two species of Caribbean acanthurids (Acanthurus coeruleus and Acanthurus bahianus). There were significant intraspecific differences in isotope discrimination factors between parasites collected from the two different host species as well as interspecific differences between parasites collected from the same host species. Discrimination factors for 15N were consistently positive but varied in magnitude depending on host and parasite species and were slightly lower than what would be expected for consumers. The 13C discrimination factors for both monogeneans and copepods collected from A. coeruleus were consistently positive but were negative for copepods collected from A. bahianus. These findings emphasize the complexity of the stable isotope trophic interactions occurring between parasites and their hosts, highlighting the value of these types of host-parasite isotopic studies.

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

“…This process, known as pinocytosis, has been described in the tegument plerocercoids (Barrett 1981), and hinders the absorption of certain compounds and nutrients, including stable isotopes, ultimately leading to isotopic depletion against host tissues (Maule and Marks 2006;Behrmann-Godel and Yohannes 2015) The copepods, which are blood-feeding ectoparasites attached to the gill filaments of the host, were 15 N-enriched relative to host gill tissue. This finding correlates with the feeding pattern of the parasite and corroborates stable 15 N fractionation patterns in other blood-feeding ectoparasites (Table 2) (Deudero et al 2002;Sures et al 2019;Jenkins et al 2020). In contrast to our a priori expectations that any parasite feeding directly from host tissues should be enriched in 15 N compared to the hostas would be the case in a classic predator-prey relationship -copepods and many other blood-feeding ectoparasites infecting marine fish, have been reported to exhibit variable isotopic patterns (Deudero et al 2002;Demopoulos and Sikkel 2015;Gilbert et al 2020a ).…”

“…Parasites feeding on these lipid-rich tissues are therefore expected to be depleted in 13 C. Patterns in this study are consistent with other blood-feeding parasites in marine systems, including the copepod Lernaeocera branchialis which has been shown to cause significant reductions in fat content of infected marine hosts (Table 2) (Khan 1988;Deudero et al 2002). Patterns of both carbon depletion and enrichment have been observed between the copepod Caligus atromaculatus and its two marine hosts, however these findings are not comparable as signatures were compared with host blood rather than tissues (Table 2) (Jenkins et al 2020). The copepods in our study, with the isotopic enrichment observed, and blood-feeding strategy, reside at a higher trophic level than the host.…”

“…This pattern was also reported from the copepod Caligus atromaculatus (Jenkins et al 2020). Clavella adunca, a copepod which embeds into host musculature, highlighted the variable isotopic relationships possible between ectoparasites and hosts reporting an isotopic depletion compared to hosts (Table 2) (Deudero et al 2002).…”

“…This biochemical process, and the absence of fish whole blood available for analysis in this study, would explain why some ectoparasites are enriched in 15 N with respect to their host (Table 2) (Jenkins et al 2020). However, enrichment patterns can be dissimilar and can, in fact, be adjusted according to nutrient availability and time of extraction, as the isotopic values of progressing parasite life stages and long-term residents' approach those of their hosts (Deudero et al 2002;Dean et al 2011;Hernández-Arciga et al 2016).…”

Parasitic Copepods as Biochemical Tracers of Foraging Patterns and Dietary Shifts in Whale Sharks (Rhincodon typus Smith, 1828)

“…It has also been argued that differences from standard trophic discrimination factors in parasite-host parings might be due to a mismatch between the host tissue selected by researchers for analysis and the tissue actually consumed by the parasite [55,72]. It was assumed that copepods fed on whale shark blood because removal of the parasite from the shark typically revealed an area of inflamed scar tissue where dermal denticles were not present that released small amounts of blood.…”