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The trophic level of Mytilicola intestinalis Steuer (Copepoda: Poecilostomatidae) in Mytilus edulis L., determined from Stable Isotope Analysis.
Abstract
Special volume (1991): Proceedings of the Fourth International Conference on Copepoda, in the Bulletin of the Plankton Society of Japan.
Mytilicola intestinalis inhabits the digestive tract of the commercially important European blue mussel Mytilus edulis. Early researchers believed that Mytilicola damaged the host by feeding directly upon the epithelial lining of the host intestine, whilst more recent work indicated that it does not seriously affect the host and feeds upon excess food (phytoplankton and detritus) which passes through the mussel intestine. Comparative analysis of the stable isotope 15N shows that it is 2.8 ppt higher in whole Mytilicola than in mussel intestine, suggesting that Mytilicola occupies a higher a trophic level than Mytilus and therefore is unlikely to use the same food source. Whilst the limitations and pitfalls of this method are recognised and discussed, it is concluded from these observations (and from evidence provided by other techniques) that Mytilicola utilizes mussel breakdown products such as mucus and sloughed-off cells as its major food source and thus feeds indirectly upon the host.
... However, Shotter [51] indicated that the mandibles of Clavella uncinata, a similar species to C. adunca, were too weak to tear tissue but instead function in gathering material by scraping superficial tissue toward the mouth, with little blood comprising the diet and intestinal contents. In some instances, studies have indicated adult female copepods are significantly enriched in 15 N relative to the host organism [52][53][54]. Gretsy and Qyarmby [52] found that adult Mytilicola intestinalis were enriched by 3‰ relative to the intestine of European blue mussel host (Mytilus edulis). Goedknegt et al. [54] similarly found that adult Mytilicola orientalis were enriched in 15 N stable isotope relative to the adductor muscle of the host mussel, M. According to predictions of stable isotope fractionation between consumers and prey items, geographic variation in the ratios of stable isotopes of carbon and nitrogen should be reflected in a predictable manner in relation to the isotope signatures of the host [6,47,55]. ...
... In some instances, studies have indicated adult female copepods are significantly enriched in 15 N relative to the host organism [52][53][54]. Gretsy and Qyarmby [52] found that adult Mytilicola intestinalis were enriched by 3‰ relative to the intestine of European blue mussel host (Mytilus edulis). Goedknegt et al. [54] similarly found that adult Mytilicola orientalis were enriched in 15 N stable isotope relative to the adductor muscle of the host mussel, M. According to predictions of stable isotope fractionation between consumers and prey items, geographic variation in the ratios of stable isotopes of carbon and nitrogen should be reflected in a predictable manner in relation to the isotope signatures of the host [6,47,55]. ...
Background
Stable 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.
Methods
Sharptooth 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.
Results
Stable 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.
Conclusion
Differences 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.
... Our findings differ from the results of a SIA of a congeneric species of M. orientalis, the copepod M. intestinalis, which also lives in the intestine of M. edulis. Gresty and Quarmby (1991) found δ 15 N values of the parasite that were, on average, 2·8‰ higher than for the blue mussel and suggested a parasitic trophic relationship between the parasite and its host. In their study, infected mussels (collection season unknown) were kept in aquaria that were filled with estuarine water and mussels were fed with the diatom Phaeodactilym trycornutum 2-3 weeks prior to dissection, after which the mussel intestine was used in the SIA analysis. ...
... Methodological differences may underlie the diverging trophic fractionation factors in the two parasite species but it is also possible that the feeding behaviour of both congeneric copepods is different. Although M. intestinalis may not directly feed on host tissue but rather on sloughed-off cells of the intestine or on mucus produced by the host (Gresty and Quarmby, 1991), it may still mainly feed (indirectly) on its mussel host. In contrast, the much lower trophic enrichment (Δ 15 N) of 1·2‰ observed in M. orientalis in our study might suggest a more complex mix of a parasitic and commensal relationship between this parasite and its new host. ...
Invasive parasites can spill over to new hosts in invaded ecosystems with often unpredictable trophic relationships in the newly arising parasite-host interactions. In European seas, the intestinal copepod Mytilicola orientalis was co-introduced with Pacific oysters ( Magallana gigas ) and spilled over to native blue mussels ( Mytilus edulis ), with negative impacts on the condition of infected mussels. However, whether the parasite feeds on host tissue and/or stomach contents is yet unknown. To answer this question, we performed a stable isotope analysis in which we included mussel host tissue and the primary food sources of the mussels, microphytobenthos (MPB) and particulate organic matter (POM). The copepods were slightly enriched in δ¹⁵ N (mean Δ ¹⁵ N ± s.d. ; 1·22 ± 0·58‰) and δ¹³ C (Δ ¹³ C 0·25 ± 0·32‰) with respect to their host. Stable isotope mixing models using a range of trophic fractionation factors indicated that host tissue was the main food resource with consistent additional contributions of MPB and POM. These results suggest that the trophic relationship of the invasive copepod with its mussel host is parasitic as well as commensalistic. Stable isotope studies such as this one may be a useful tool to unravel trophic relationships in new parasite-host associations in the course of invasions.
... Indirect feeding on metabolic byproducts such as mucus or blood (e.g. Gresty & Quarmby, 1991) should also result in isotopic enrichment of the parasite. ...
... Triaenophorus nodulosus should be able to utilize a variety of metabolic resources in both locations. Therefore, one could expect that, irrespective of location, T. nodulosus will absorb nutrients (mainly glucose) directly across its tegument (Kuperman, 1973;Barrett, 1981), resulting in an enriched isotopic signature (Gresty & Quarmby, 1991). We found variability in isotopic discrimination and thus conclude that plerocercoids and adult worms of T. nodulosus may feed on nutritional resources other than Table 2. Mean^SE values of carbon, nitrogen and sulphur isotopes of Triaenophorus nodulosus in pike and discrimination factors. ...
Previous studies of dietary isotope discrimination have led to the general expectation that a consumer will exhibit enriched stable isotope levels relative to its diet. Parasite-host systems are specific consumer-diet pairs in which the consumer (parasite) feeds exclusively on one dietary source: host tissue. However, the small numbers of studies previously carried out on isotopic discrimination in parasite-host (ΔXP-HT) systems have yielded controversial results, showing some parasites to be isotopically depleted relative to their food source, while others are enriched or in equilibrium with their hosts. Although the mechanism for these deviations from expectations remains to be understood, possible influences of specific feeding niche or selection for only a few nutritional components by the parasite are discussed. ΔXP-HT for multiple isotopes (δ13C, δ15N, δ34S) were measured in the pike tapeworm Triaenophorus nodulosus and two of its life-cycle fish hosts, perch Perca fluviatilis and pike Esox lucius, within which T. nodulosus occupies different feeding locations. Variability in the value of ΔXP-HT calculated for the parasite and its different hosts indicates an influence of feeding location on isotopic discrimination. In perch liver ΔXP-HT was relatively more negative for all three stable isotopes. In pike gut ΔXP-HT was more positive for δ13C, as expected in conventional consumer-diet systems. For parasites feeding on pike gut, however, the δ15N and δ34S isotope values were comparable with those of the host. We discuss potential causes of these deviations from expectations, including the effect of specific parasite feeding niches, and conclude that ΔXP-HT should be critically evaluated for trophic interactions between parasite and host before general patterns are assumed.
... However, Shotter (1971) indicated that the mandibles of Clavella uncinata, a similar species to C. adunca, were too weak to tear tissue but instead function in gathering material by scraping superficial tissue toward the mouth, with little blood comprising the diet and intestinal contents. In some instances, studies have indicated adult female copepods are significantly enriched in 15 N relative to the host organism (Baud et al., 2004;Goedknegt et al., 2018;Gretsy and Quarmby, 1991). Gretsy and Qyarmby (1991) found that adult Mytilicola intestinalis were enriched by 3 ‰ relative to the intestine of European blue mussel host (Mytilus edulis). ...
Stable isotope analysis offers a unique tool for comparing trophic interactions and food web architecture in ecosystems based on analysis of stable isotope ratios of carbon (¹³C/¹²C) and nitrogen (¹⁵N/¹⁴N) in organisms. Clarias gariepinus were collected from six sites along the Vaal River, South Africa and were assessed for ectoparasites and endoparasites. Lamproglena clariae (Copepoda), Tetracampos ciliotheca and Proteocephalus glanduligerus (Cestoda), and larval Contracaecum sp. (Nematoda) were collected from the gills, intestine and mesenteries, respectively. Signatures of δ¹³C and δ¹⁵N were analysed in host muscle tissue and parasites using bulk stable isotope analysis. Variable stable isotope enrichment between parasites and host were observed; L. clariae and the host shared similar δ¹⁵N signatures and endoparasites being depleted in δ¹³C and δ¹⁵N relative to the host. Differences in stable isotope enrichment between parasites could be related to the feeding strategy of each parasite species collected. Geographic and spatial differences in enrichment of stable isotopes observed in hosts were mirrored by parasites. As parasites rely on a single host for meeting their nutritional demands, stable isotope variability in parasites relates to the dietary differences of host organisms and therefore variations in baseline stable isotope signatures of food items consumed by hosts.
... The constant wounding causes metaplastic changes of the gut epithelium that could further limit gut function (Moore, Lowe, & Gee, 1978). Reduced filtration rates coupled to increased metabolic demands caused by M. intestinalis' feeding on host tissue (Gresty & Quarmby, 1991) lead to lower mussel condition and could in cases of high parasite load kill the host (Theisen, 1987). ...
Parasite spillover from invasive aliens to native species increases the risk of disease emergence within native biota—either by direct harm to the new host or by indirect effects like increased risks of secondary infection.
One example for such a detrimental effect is the parasitic copepod Mytilicola intestinalis that infected blue mussels Mytilus edulis after being introduced into the North Sea in the early 20th century. Since 1949, the parasite was blamed for multiple mass mortalities of infested blue mussels but evidence for a direct causal involvement of M. intestinalis remained circumstantial.
Here, we now examine the potential effects of primary infections by the invasive parasite on the susceptibility to secondary infections with virulent bacteria (Vibrio spp.) in a full factorial infection experiment combining parasite infection (control vs. infected) with different Vibrio infection treatments (control, bath challenge, injection) in environmental conditions that either favoured the host (ambient temperature) or the bacterium (elevated temperature). The influence of primary and secondary infections on cellular immunity (phagocytosis) and Vibrio load in the haemolymph was used to correlate these results to host survival.
Our results suggest that the rate of secondary Vibrio infection is increased due to lower efficiency of the cellular immune response. As a consequence, the failure of clearing Vibrio from the haemolymph might increase mortality of mussels infected by M. intestinalis.
This demonstrates that indirect effects of parasite invasions can outweigh direct effects of the infection highlighting the need for a more integrative approach to understand and predict the consequences of parasite invasions.
... This is the digestive organ in molluscs, and infections may compromise its functioning. As stable isotope analyses suggest that Mytilicola feeds on host tissue (Gresty and Quarmby 1991;Goedknegt et al. 2017b), the energy demand of the growing copepods can be expected to lead to a significant loss of tissue, ultimately resulting in a potential lower host condition (11-13% reduction in our experiments). Moreover, when Mytilicola feeds on host tissue, the resulting metaplasia of the host gut epithelium (Moore et al. 1977) needs to be repaired, which is an energetically demanding process for the host and likely to reduce host condition. ...
Invasive species can indirectly affect native species by modifying parasite–host dynamics and disease occurrence. This scenario applies to European coastal waters where the invasive Pacific oyster (Magallana gigas) co-introduced the parasitic copepod Mytilicola orientalis that spills over to native blue mussels (Mytilus edulis) and other native bivalves. In this study, we investigated the impact of M. orientalis infections on blue mussels by conducting laboratory experiments using controlled infections with larval stages of the parasitic copepod. As the impact of infections is likely to depend on the mussels’ food availability, we also tested whether potential adverse effects of infection on mussels intensify under low food conditions. Blue mussels that were experimentally infected with juvenile M. orientalis had a significantly lower body condition (11–13%) compared with uninfected mussels after nine weeks of infection. However, naturally infected mussels from a mixed mussel and oyster bed did not significantly differ in body condition compared with uninfected mussels. Contrary to effects on mussel condition, we did not find an effect of experimental infections on clearance rates, shell growth or survival of blue mussels and no clear sign of exacerbating effects of food limitation. Our study illustrates that invasive species can indirectly affect native species via parasite co-introductions and parasite spillover. The results of this study call for the integration of such parasite-mediated indirect effects of invasions in impact assessments of invasive species.
... Coral mucus uptake (as illustrated by Strathmann et al. 1984) and utilization by S. giganteus, resulting in nitrogen secretion (Rotjan & Lewis 2006, reviewed by Rowley 2008, subsequent use by the host coral and zooxanthellae with a possible increase in mucus Ca 2+ concentration further utilized by the worm may be occurring. To test this hypothesis, the use of 45 Ca and 14 C (as used by Marshall & Wright 1998) and 15 N (as used by Gresty & Quarmby 1991) may ascertain any trophic recycling and/or niche partitioning (Tapanila 2004) occurring between S. giganteus, host coral and its zooxanthellae. Furthermore, juvenile tube construction, via rapid carbonate (calcite or aragonite, Smith 1985, Rouse & Pleijel 2001 deposition, only proceeds in the presence of live coral (Smith 1984a). ...
Ecological and taxonomic study of the coral associate serpulid polychaetes within the genus Spirobranchus, on coral reefs within the Wakatobi Marine National Park, SE Sulawesi, Indonesia.
... Coral mucus uptake (as illustrated by Strathmann et al. 1984; Figure 2) and utilization by S. giganteus, resulting in nitrogen secretion, subsequent use by the host coral and zooxanthellae with a possible increase in mucus Ca 2+ concentration further utilized by the worm may be occuring. To test this hypothesis, the use of 45 Ca and 14 C (as used by Marshall & Wright, 1998) and 15 N (as used by Gresty & Quarmby, 1991) may ascertain any trophic recycling &/or niche partitioning (Tapanila, 2004) occurring between S. giganteus, host coral and its zooxanthellae. ...
Coral reefs are high in species diversity with a low effective population size for most species and a high incidence of specific co-evolved relationships. Hermatypic corals are associated with, and attract a variety of, symbionts and commensals which helps to maintain coral reef biodiversity. However, little is known about such associations. Tropical tube-dwelling polychaetes provide an interesting surrogate in the enhancement of current understanding of such associations posing the question: what is the nature of the symbiotic association between tropical tube-dwelling polychaetes and their hermatypic coral hosts? This question is addressed by reviewing the life history and ecology of the conspicuous serpulid Spirobranchus giganteus (Pallas, 1766), an obligate associate of living hermatypic corals showing host species specificity. The distribution, life history and behavioural patterns of this taxon are suggestive of more than the currently perceived commensal association between its coral hosts. Most notably, recent studies have suggested the up regulation of Spirobranchus giganteus symbiotic association from commensalism to mutualism, with Spirobranchus giganteus protecting the coral host from predation, and increased water circulation to adjacent polyps facilitating coral recovery in algal dominated coral colonies. Such recent evidence illustrates the importance of associate organisms on coral reefs.
During a histopathological survey of Mytilus galloprovincialis in Galicia (NW Spain), microcells were observed infecting several organs of the symbiont copepod Mytilicola intestinalis. Positive results of PCR assay with specific primers for genus Mikrocytos and a clear signal of in situ hybridization with MACKINI-1 digoxigenin- labelled DNA probe (DIG-ISH) indicated a protozoan parasite of Mikrocytos genus. The ultrastructural study revealed intra and extracellular locations, polymorphic nuclei, intracellular round vesicles in the cytoplasm and absence of mitochondria. The present paper reports the characterization of the Mikrocytos sp. infecting M. intestinalis and proposes a novel species in the genus: Mikrocytos mytilicoli n. sp. A sequence of 18S-28S rDNA was obtained with 95.6% maximum identity (query cover 100%) with Mikrocytos mackini. Phylogenetic analysis showed that M. mytilicoli n. sp. and M. mackini share a common ancestor. However, comparison of the ITS1 rDNA region showed low similarity (75.8%) with M. mackini, which, combined with differences in ultrastructural details, host and geographic location, support the designation of a new species. This is the first description of microcytid parasite of the genus Mikrocytos from a non-bivalve host.
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