High parasite diversity in the amphipod Gammarus lacustris in a subarctic lake
Status PubMed-not-MEDLINE Jazyk angličtina Země Velká Británie, Anglie Médium electronic-ecollection
Typ dokumentu časopisecké články
PubMed
33209296
PubMed Central
PMC7663964
DOI
10.1002/ece3.6869
PII: ECE36869
Knihovny.cz E-zdroje
- Klíčová slova
- Amphipod, Cestoda, Trematoda, food web, trophically transmitted parasites,
- Publikační typ
- časopisecké články MeSH
Amphipods are often key species in aquatic food webs due to their functional roles in the ecosystem and as intermediate hosts for trophically transmitted parasites. Amphipods can also host many parasite species, yet few studies address the entire parasite community of a gammarid population, precluding a more dynamic understanding of the food web. We set out to identify and quantify the parasite community of Gammarus lacustris to understand the contributions of the amphipod and its parasites to the Takvatn food web. We identified seven parasite taxa: a direct life cycle gregarine, Rotundula sp., and larval stages of two digenean trematode genera, two cestodes, one nematode, and one acanthocephalan. The larval parasites use either birds or fishes as final hosts. Bird parasites predominated, with trematode Plagiorchis sp. having the highest prevalence (69%) and mean abundance (2.7). Fish parasites were also common, including trematodes Crepidostomum spp., nematode Cystidicola farionis, and cestode Cyathocephalus truncatus (prevalences 13, 6, and 3%, respectively). Five parasites depend entirely on G. lacustris to complete their life cycle. At least 11.4% of the overall parasite diversity in the lake was dependent on G. lacustris, and 16% of the helminth diversity required or used the amphipod in their life cycles. These dependencies reveal that in addition to being a key prey item in subarctic lakes, G. lacustris is also an important host for maintaining parasite diversity in such ecosystems.
Department of Ecology Evolution and Marine Biology University of California Santa Barbara CA USA
Institute of Marine Research Ecosystem Processes Research Group Tromsø Norway
Institute of Parasitology Biology Centre Czech Academy of Sciences České Budějovice Czech Republic
Marine Science Institute University of California Santa Barbara Santa Barbara CA USA
Western Ecological Research U S Geological Survey Santa Barbara CA USA
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Amundsen, P. A. , Knudsen, R. , Kuris, A. M. , & Kristoffersen, R. (2003). Seasonal and ontogenetic dynamics in trophic transmission of parasites. Oikos, 102, 285–293. 10.1034/j.1600-0706.2003.12182.x DOI
Amundsen, P.‐A. , Lafferty, K. D. , Knudsen, R. , Primicerio, R. , Klemetsen, A. , & Kuris, A. M. (2009). Food web topology and parasites in the pelagic zone of a subarctic lake. Journal of Animal Ecology, 78, 563–572. 10.1111/j.1365-2656.2008.01518.x PubMed DOI
Amundsen, P.‐A. , Lafferty, K. D. , Knudsen, R. , Primicerio, R. , Kristoffersen, R. , Klemetsen, A. , & Kuris, A. M. (2013). New parasites and predators follow the introduction of two fish species to a subarctic lake: Implications for food‐web structure and functioning. Oecologia, 171, 993–1002. 10.1007/s00442-012-2461-2 PubMed DOI PMC
Amundsen, P.‐A. , Primicerio, R. , Smalås, A. , Henriksen, E. H. , Knudsen, R. , Kristoffersen, R. , & Klemetsen, A. (2019). Long‐term ecological studies in northern lakes—challenges, experiences, and accomplishments. Limnology and Oceanography, 64, S11–21. 10.1002/lno.10951 DOI
Awachie, J. B. (1966). Observations on Cyathocephalus truncatus Pallas, 1781 (Cestoda:Spathebothriidea) in its intermediate and definitive hosts in a trout stream, North Wales. Journal of Helminthology, 40, 1–10. 10.1017/s0022149x00034039 PubMed DOI
Awachie, J. B. E. (1968). On the bionomics of Crepidostomum metoecus (Braun, 1900) and Crepidostomum farionis (Müller, 1784) (Trematoda: Allocreadiidae). Parasitology, 58, 307–324. 10.1017/S0031182000069341 DOI
Awachie, J. B. E. (1973). Ecological observations on Metabronema truttae and Cystidicola farionis Nematoda Spiruroidea in their intermediate and definitive hosts in Afon Terrig northern Wales Unitid Kingdom. Acta Parasitologica Polonica, 21, 661–670.
Bakker, T. C. M. , Frommen, J. G. , & Thünken, T. (2017). Adaptive parasitic manipulation as exemplified by acanthocephalans. Ethology, 123, 779–784. 10.1111/eth.12660 DOI
Bakker, T. C. , Mazzi, D. , & Zala, S. (1997). Parasite‐induced changes in behavior and color make Gammarus pulex more prone to fish predation. Ecology, 78, 1098–1104.
Blasco‐Costa, I. , Faltýnková, A. , Georgieva, S. , Skírnisson, K. , Scholz, T. , & Kostadinova, A. (2014). Fish pathogens near the Arctic Circle: Molecular, morphological and ecological evidence for unexpected diversity of diplostomum (Digenea: Diplostomidae) in Iceland. International Journal for Parasitology, 44, 703–715. 10.1016/j.ijpara.2014.04.009 PubMed DOI
Bojko, J. , Bącela‐Spychalska, K. , Stebbing, P. D. , Dunn, A. M. , Grabowski, M. , Rachalewski, M. , & Stentiford, G. D. (2017). Parasites, pathogens and commensals in the “low‐impact” non‐native amphipod host Gammarus roeselii. Parasit Vectors, 10, 193 10.1186/s13071-017-2108-6 PubMed DOI PMC
Bojko, J. , & Ovcharenko, M. (2019). Pathogens and other symbionts of the Amphipoda: Taxonomic diversity and pathological significance. Diseases of Aquatic Organisms, 136, 3–36. 10.3354/dao03321 PubMed DOI
Bousfield, E. L. (1958). Fresh‐water amphipod crustaceans of glaciated North America. Canadian Field Naturalist, 72, 55–113.
Bush, A. O. , Lafferty, K. D. , Lotz, J. M. , Shostak, A. W. (1997). Parasitology meets ecology on its own terms: Margolis et al Revisited.. Journal of Parasitology, 83, 575–583. 10.2307/3284227 PubMed DOI
Cezilly, F. , Perrot‐Minnot, M.‐J. , & Rigaud, T. (2014). Cooperation and conflict in host manipulation: Interactions among macro‐parasites and micro‐organisms. Frontiers in Microbiology, 5, 248 10.3389/fmicb.2014.00248 PubMed DOI PMC
Denny, M. (1969). Life‐cycles of helminth parasites using Gammarus lacustris as an intermediate host in a Canadian lake. Parasitology, 59, 795–827. PubMed
Dezfuli, B. S. , Capuano, S. , & Congiu, L. (2002). Identification of life cycle stages of Cyathocephalus truncatus (Cestoda: Spathebothriidea) using molecular techniques. Journal of Parasitology, 632–634. 10.1645/0022-3395(2002)088[0632:IOLCSO]2.0.CO;2 PubMed DOI
Dezfuli, B. S. , Giari, L. , & Poulin, R. (2000). Species associations among larval helminths in an amphipod intermediate host. International Journal for Parasitology, 30, 1143–1146. 10.1016/S0020-7519(00)00093-X PubMed DOI
Dianne, L. , Perrot‐Minnot, M.‐J. , Bauer, A. , Guvenatam, A. , & Rigaud, T. (2014). Parasite‐induced alteration of plastic response to predation threat: Increased refuge use but lower food intake in Gammarus pulex infected with the acanothocephalan Pomphorhynchus laevis. International Journal for Parasitology, 44, 211–216. https://cran.r-project.org/web/packages/venn/index.html PubMed
Dusa, A. (2020). venn: Draw Venn Diagrams. 10.1016/j.ijpara.2013.11.001 DOI
Frainer, A. , Johansen, K. S. , Siwertsson, A. , Mousavi, S. K. , Brittain, J. E. , Klemetsen, A. , Knudsen, R. , & Amundsen, P.‐A. (2016). Variation in functional trait composition of benthic invertebrates across depths and seasons in a subarctic lake. Fundamental and Applied Limnology / Archiv Für Hydrobiologie, 188, 103–112. 10.1127/fal/2016/0839 DOI
Frainer, A. , McKie, B. G. , Amundsen, P.‐A. , Knudsen, R. , & Lafferty, K. D. (2018). Parasitism and the biodiversity‐functioning relationship. Trends in Ecology & Evolution, 33, 260–268. 10.1016/j.tree.2018.01.011 PubMed DOI
Franceschi, N. , Rigaud, T. , Moret, Y. , Hervant, F. , & Bollache, L. (2007). Behavioural and physiological effects of the trophically transmitted cestode parasite, Cyathocephalus truncatus, on its intermediate host, Gammarus pulex . Parasitology, 134, 1839–1847. 10.1017/S0031182007003228 PubMed DOI
Goodrich, H. P. (1949). Heliospora n.g. and Rotundula n.g., Gregarines of Gammarus pulex . Journal of Cell Science, 3, 27–35. PubMed
Gordy, M. A. , & Hanington, P. C. (2019). A fine‐scale phylogenetic assessment of digenean trematodes in central Alberta reveals we have yet to uncover their total diversity. Ecology and Evolution, 9, 3153–3238. 10.1002/ece3.4939 PubMed DOI PMC
Grunberg, R. L. , & Sukhdeo, M. V. K. (2017). Temporal community structure in two gregarines (Rotundula gammari and Heliospora longissima) co‐infecting the Amphipod Gammarus fasciatus . Journal of Parasitology, 103, 6–13. 10.1645/16-47 PubMed DOI
Haine, E. R. , Boucansaud, K. , & Rigaud, T. (2005). Conflict between parasites with different transmission strategies infecting an amphipod host. Proceedings of the Royal Society B: Biological Sciences, 272, 2505–2510. 10.1098/rspb.2005.3244 PubMed DOI PMC
Hechinger, R. F. , & Lafferty, K. D. (2005). Host diversity begets parasite diversity: Bird final hosts and trematodes in snail intermediate hosts. Proceedings of the Royal Society of London. Series B Biological Sciences, 272, 1059–1066. PubMed PMC
Helluy, S. , & Thomas, F. (2003). Effects of Microphallus papillorobustus (Platyhelminthes : Trematoda) on serotonergic immunoreactivity and neuronal architecture in the brain of Gammarus insensibilis (Crustacea : Amphipoda). Proceedings of the Royal Society of London. Series B Biological Sciences, 270, 563–568. PubMed PMC
Helluy, S. , & Thomas, F. (2010). Parasitic manipulation and neuroinflammation: Evidence from the system Microphallus papillorobustus (Trematoda) ‐ Gammarus (Crustacea). Parasit Vectors, 3 10.1186/1756-3305-3-38 PubMed DOI PMC
Hindsbo, O. L. E. (1972). Effects of Polymorphus (Acanthocephala) on colour and behaviour of Gammarus lacustris . Nature, 238, 333 10.1038/238333a0 PubMed DOI
Hoberg, E. P. , Galbreath, K. E. , Cook, J. A. , Kutz, S. J. , & Polley, L. (2012). Northern host‐parasite assemblages. History and biogeography on the borderlands of episodic climate and environmental transition In Rollinson D. & Hay S. I. (Eds.), Advances in Parasitology. vol. 79, (1–97). Amsterdam, Netherlands: Elsevier. PubMed
Holmes, J. C. , & Price, P. W. (1986). Communities of parasites In Holmes J. C. & Kikkawa J. (Eds.), Community Ecology: Patterns and Processes, (187–213). Oxford: Blackwell Scientific Publications.
Hsieh, T. C. , Ma, K. H. , & Chao, A. (2016). iNEXT: An R package for rarefaction and extrapolation of species diversity (Hill numbers). Methods in Ecology and Evolution, 7, 1451–1456. 10.1111/2041-210X.12613 DOI
Jacquin, L. , Mori, Q. , Pause, M. , Steffen, M. , & Medoc, V. (2014). Non‐specific manipulation of Gammarid behaviour by P. minutus parasite enhances their predation by definitive bird hosts. PLoS One, 9(7), e101684 10.1371/journal.pone.0101684 PubMed DOI PMC
Karaman, G. S. , & Pinkster, S. (1977). Freshwater Gammarus species from Europe, North Africa and adjacent regions of Asia (Crustacea ‐ Amphipoda). Bijdr Tot Dierkd, 47, 1–86. 10.1163/26660644-04701001 DOI
Kelly, D. W. , Dick, J. T. , & Montgomery, W. I. (2002). The functional role of Gammarus (Crustacea, Amphipoda): Shredders, predators, or both? Hydrobiologia, 485, 199–203.
Klemetsen, A. , & Elliott, J. M. (2010). Spatial distribution and diversity of macroinvertebrates on the stony shore of a subarctic lake. International Review of Hydrobiology, 95, 190–206. 10.1002/iroh.200911199 DOI
Klemetsen, A. , & Knudsen, R. (2013). Diversity and abundance of water birds in a subarctic lake during three decades. Fauna Norvegica, 33, 21–27. 10.5324/fn.v33i0.1584 DOI
Knudsen, R. (1995). Relationships between habitat, prey selection and parasite infection in Arctic charr (Salvelinus alpinus). Nordic Journal of Freshwater Research, 71, 333–344.
Knudsen, R. , Amundsen, P.‐A. , & Klemetsen, A. (2002). Parasite‐induced host mortality: Indirect evidence from a long‐term study. Environmental Biology of Fishes, 64, 257–265.
Knudsen, R. , Amundsen, P.‐A. , Nilsen, R. , Kristoffersen, R. , & Klemetsen, A. (2008). Food borne parasites as indicators of trophic segregation between Arctic charr and brown trout. Environmental Biology of Fishes, 83, 107–116. 10.1007/s10641-007-9216-7 DOI
Knudsen, R. , Curtis, M. A. , & Kristoffersen, R. (2004). Aggregation of helminths: The role of feeding behavior of fish hosts. Journal of Parasitology, 90, 1–7. 10.1645/GE-3184 PubMed DOI
Knudsen, R. , Gabler, H. M. , Kuris, A. M. , & Amundsen, P. A. (2001). Selective predation on parasitized prey ‐ A comparison between two helminth species with different life‐history strategies. Journal of Parasitology, 87, 941–945. PubMed
Knudsen, R. , Kristoffersen, R. , & Amundsen, P.‐A. (1999). The long‐term dynamics of the interactions between Arctic charr and the nematode parasite Cystidicola farionis after fish stock reduction in Lake Takvatn, northern Norway. ISACF Inf Ser, 7, 135–140.
Kuhn, J. A. , Knudsen, R. , Kristoffersen, R. , Primicerio, R. , & Amundsen, P. A. (2016). Temporal changes and between‐host variation in the intestinal parasite community of Arctic charr in a subarctic lake. Hydrobiologia, 783, 79–91. 10.1007/s10750-016-2731-9 DOI
Kuhn, J. A. , Kristoffersen, R. , Knudsen, R. , Jakobsen, J. , Marcogliese, D. J. , Locke, S. A. , Primicerio, R. , & Amundsen, P.‐A. (2015). Parasite communities of two three‐spined stickleback populations in subarctic Norway–effects of a small spatial‐scale host introduction. Parasitology Research, 114, 1327–1339. 10.1007/s00436-015-4309-2 PubMed DOI
Labaude, S. , Rigaud, T. , & Cézilly, F. (2017). Additive effects of temperature and infection with an acanthocephalan parasite on the shredding activity of Gammarus fossarum (Crustacea: Amphipoda): The importance of aggregative behavior. Global Change Biology, 23, 1415–1424. 10.1111/gcb.13490 PubMed DOI
Lafferty, K. D. (1999). The evolution of trophic transmission. Parasitol Today, 15, 111–115. 10.1016/S0169-4758(99)01397-6 PubMed DOI
Lafferty, K. D. , Dobson, A. P. , & Kuris, A. M. (2006). Parasites dominate food web links. Proceedings of the National Academy of Sciences, 103, 11211–11216. 10.1073/pnas.0604755103 PubMed DOI PMC
Lafferty, K. D. , & Kuris, A. M. (2009). Parasites reduce food web robustness because they are sensitive to secondary extinction as illustrated by an invasive estuarine snail Philosophical Transactions of the Royal Society B: Biological Sciences, 364, 1659–1663. 10.1098/rstb.2008.0220 PubMed DOI PMC
Lafferty, K. D. , & Shaw, J. C. (2013). Comparing mechanisms of host manipulation across host and parasite taxa. Journal of Experimental Biology, 216, 56–66. 10.1242/jeb.073668 PubMed DOI
Lagrue, C. , Güvenatam, A. , & Bollache, L. (2013). Manipulative parasites may not alter intermediate host distribution but still enhance their transmission: Field evidence for increased vulnerability to definitive hosts and non‐host predator avoidance. Parasitology, 140, 258–265. 10.1017/S0031182012001552 PubMed DOI
Lagrue, C. , & Poulin, R. (2009). Life cycle abbreviation in trematode parasites and the developmental time hypothesis: Is the clock ticking? Journal of Evolutionary Biology, 22, 1727–1738. 10.1111/j.1420-9101.2009.01787.x PubMed DOI
Locke, S. A. , Marcogliese, D. J. , & Tellervo, V. E. (2014). Vulnerability and diet breadth predict larval and adult parasite diversity in fish of the Bothnian Bay. Oecologia, 174, 253–262. 10.1007/s00442-013-2757-x PubMed DOI
MacNeil, C. , Dick, J. T. , & Elwood, R. W. (1997). The trophic ecology of freshwater Gammarus spp. (Crustacea: Amphipoda): Problems and perspectives concerning the functional feeding group concept. Biological Reviews, 72, 349–364. 10.1017/S0006323196005038 DOI
MacNeil, C. , Dick, J. T. , & Elwood, R. W. (1999). The dynamics of predation on Gammarus spp. (Crustacea: Amphipoda). Biological Reviews, 74, 375–395. 10.1017/S0006323199005368 DOI
Medoc, V. , & Beisel, J. N. (2011). When trophically‐transmitted parasites combine predation enhancement with predation suppression to optimize their transmission. Oikos, 120, 1452–1458. 10.1111/j.1600-0706.2011.19585.x DOI
Moravec, F. , & (1994). Parasitic Nematodes of freshwater fishes of Europe, (1–470). Dordrecht, Netherlands: Springer Netherlands.
Nikolov, P. N. , Georgiev, B. B. , & Dezfuli, B. S. (2008). Cyclophyllidean cysticercoids from Echinogammarus tibaldii (Amphipoda, Gammaridae) from Lake Piediluco, Italy. Acta Parasitol, 53, 215–218. 10.2478/s11686-008-0017-8 DOI
Poulin, R. (2014). Parasite biodiversity revisited: Frontiers and constraints. International Journal for Parasitology, 44, 581–589. 10.1016/j.ijpara.2014.02.003 PubMed DOI
Prati, S. , Henriksen, E. H. , Knudsen, R. , & Amundsen, P.‐A. (2020). Seasonal dietary shifts enhance parasite transmission to lake salmonids during ice cover. Ecology and Evolution, 10, 4031–4043. 10.1002/ece3.6173 PubMed DOI PMC
R Core Team . (2018). R: The R Project for Statistical Computing. https://www.r‐project.org/
Rauque, C. A. , & Semenas, L. (2013). Interactions among four parasite species in an amphipod population from Patagonia. Journal of Helminthology, 87, 97–101. 10.1017/S0022149X12000107 PubMed DOI
Siwertsson, A. , Refsnes, B. , Frainer, A. , Amundsen, P.‐A. , & Knudsen, R. (2016). Divergence and parallelism of parasite infections in Arctic charr morphs from deep and shallow lake habitats. Hydrobiologia, 783, 131–143. 10.1007/s10750-015-2563-z DOI
Sokolov, S. G. , & Gordeev, I. I. (2014). Occurrence of helminths in amphipods Gammarus lacustris Sars, 1863 (Amphipoda: Gammaridae) from Kronotskoe Lake (Kamchatka). Parazitologiia, 48, 325–332. PubMed
Soldánová, M. , Georgieva, S. , Roháčová, J. , Knudsen, R. , Kuhn, J. A. , Henriksen, E. H. , Siwertsson, A. , Shaw, J. C. , Kuris, A. M. , Amundsen, P.‐A. , Scholz, T. , Lafferty, K. D. , & Kostadinova, A. (2017). Molecular analyses reveal high species diversity of trematodes in a sub‐Arctic lake. International Journal for Parasitology, 47, 327–345. 10.1016/j.ijpara.2016.12.008 PubMed DOI
Song, Z. , & Proctor, H. (2020). Parasite prevalence in intermediate hosts increases with waterbody age and abundance of final hosts. Oecologia, 192, 311–321. 10.1007/s00442-020-04600-4 PubMed DOI
Sorcetti, C. C. , & Di Giovanni, M. V. (1984). Gregarines (Protozoa‐Sporozoa) in Italian freshwater arthropods. A Preliminary Contribution. Italian Journal of Zoology, 51, 313–327.
Sures, B. , Nachev, M. , Pahl, M. , Grabner, D. , & Selbach, C. (2017). Parasites as drivers of key processes in aquatic ecosystems: Facts and future directions. Experimental Parasitology, 180, 141–147. 10.1016/j.exppara.2017.03.011 PubMed DOI
Thomas, F. , Poulin, R. , de Meeüs, T. , Guégan, J.‐F. , Renaud, F. , Thomas, F. , de Meeus, T. , Guegan, J.‐F. , & Renaud, F. (1999). Parasites and ecosystem engineering: What roles could they play? Oikos, 84, 167–171. 10.2307/3546879 DOI
Ubeda, C. , Trejo, A. S. O. , & Semenas, L. (1994). Status of three different fish hosts of Pomphorhynchus patagonicus in Lake Rosario. Research and Reviews in Parasitology, 54, 87–92.
Väinölä, R. , Witt, J. D. S. , Grabowski, M. , Bradbury, J. H. , Jazdzewski, K. , & Sket, B. (2008). Global diversity of amphipods (Amphipoda; Crustacea) in freshwater. Hydrobiologia, 595, 241–255. 10.1007/s10750-007-9020-6 DOI
Zuur, A. , Ieno, E. N. , Walker, N. , Saveliev, A. A. , & Smith, G. M. (2009). Mixed effects models and extensions in ecology with R, (1–574). New York, NY: Springer‐Verlag New York.