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Transmission dynamics of ectoparasitic gyrodactylids (Platyhelminthes, Monogenea): An integrative review

Published online by Cambridge University Press:  19 April 2022

Natalia Tepox-Vivar ,
Jessica F. Stephenson  and
Palestina Guevara-Fiore Open the ORCID record for Palestina Guevara-Fiore [Opens in a new window]
Natalia Tepox-Vivar
Affiliation:
Maestría en Ciencias Biológicas, Benemérita Universidad Autónoma de Puebla (BUAP), Puebla 72592, Mexico
Jessica F. Stephenson
Affiliation:
Department of Biological Sciences, University of Pittsburgh, Pittsburgh, PA 15260, USA
Palestina Guevara-Fiore*
Affiliation:
Facultad de Ciencias Biológicas, Benemérita Universidad Autónoma de Puebla (BUAP), Puebla 72592, Mexico
*
Author for correspondence: Palestina Guevara-Fiore, E-mail: palestina.guevara@correo.buap.mx
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Abstract

Parasite transmission is the ability of pathogens to move between hosts. As a key component of the interaction between hosts and parasites, it has crucial implications for the fitness of both. Here, we review the transmission dynamics of Gyrodactylus species, which are monogenean ectoparasites of teleost fishes and a prominent model for studies of parasite transmission. Particularly, we focus on the most studied host–parasite system within this genus: guppies, Poecilia reticulata, and G. turnbulli/G. bullatarudis. Through an integrative literature examination, we identify the main variables affecting Gyrodactylus spread between hosts, and the potential factors that enhance their transmission. Previous research indicates that Gyrodactylids spread when their current conditions are unsuitable. Transmission depends on abiotic factors like temperature, and biotic variables such as gyrodactylid biology, host heterogeneity, and their interaction. Variation in the degree of social contact between hosts and sexes might also result in distinct dynamics. Our review highlights a lack of mathematical models that could help predict the dynamics of gyrodactylids, and there is also a bias to study only a few species. Future research may usefully focus on how gyrodactylid reproductive traits and host heterogeneity promote transmission and should incorporate the feedbacks between host behaviour and parasite transmission.

Keywords

Host behaviourparatenic hostpoeciliidaeR0salmonidssex-biased parasitism
Type
Review Article
Information
Parasitology , Volume 149 , Issue 7 , June 2022 , pp. 865 - 877
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Copyright
Copyright © The Author(s), 2022. Published by Cambridge University Press

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References

Altizer, S, Nunn, CL, Thrall, PH, Gittleman, JL, Antonovics, J, Cunningham, AA, Dobson, AP, Ezenwa, V, Jones, KE, Pedersen, AB, Mary, P and Pulliam, JRC (2003) Social organization and parasite risk in mammals: integrating theory and empirical studies. Annual Review of Ecology, Evolution, and Systematics 34, 517–547. doi: 10.1146/annurev.ecolsys.34.030102.151725.CrossRefGoogle Scholar
Anderson, RM and May, RM (1992) Infectious Diseases of Humans: Dynamics and Control, 1st Edn. New York, United States: Oxford University Press.Google Scholar
Anderson, TK and Sukhdeo, MV (2010) Abiotic versus biotic hierarchies in the assembly of parasite populations. Parasitology 137, 743–754. doi: 10.1017/S0031182009991430CrossRefGoogle ScholarPubMed
Antolin, MF (2008) Unpacking β: within-host dynamics and the evolutionary ecology of pathogen transmission. Annual Review of Ecology, Evolution, and Systematics 39, 415–437. doi: 10.1146/annurev.ecolsys.37.091305.110119CrossRefGoogle Scholar
Appleby, C (1996) Seasonal occurrence, topographical distribution and transmission of Gyrodactylus callanatis (Monogenea) infecting juvenile Atlantic cod in the Oslo Fjord, Norway. Journal of Fish Biology 48, 1266–1274.Google Scholar
Araujo, SB, Braga, MP, Brooks, DR, Agosta, SJ, Hoberg, EP, Von-Hartenthal, FW and Boeger, WA (2015) Understanding host-switching by ecological fitting. Plos One 10, e0139225.CrossRefGoogle ScholarPubMed
Arnold, ML (2004) Natural hybridization and the evolution of domesticated, pest and disease organisms. Molecular Ecology 13, 997–1007.CrossRefGoogle ScholarPubMed
Bakke, TA and Sharp, LA (1990) Susceptibility and resistance of minnows Phoxinus phoxinus (L.) to Gyrodactylus salaris Malmberg 1957 (Monogenea) under laboratory condition. Fauna Norvegica Ser. A 11, 51–55.Google Scholar
Bakke, TA, Jansen, PA and Brabrand, A (1990) Susceptibility and resistance of brook lamprey Lampetra planeri (Bloch), roach Rutilus rutilus (L.) and perch, Perca fluviatilis L. to Gyrodactylus salaris Malmberg (Monogenea). Fauna Norvegica Ser. A 11, 23–26.Google Scholar
Bakke, TA, Jansen, PA and Hansen, LP (1991) Experimental transmission of Gyrodactylus salaris Malmberg, 1957 (Platyhelminthes, Monogenea) from the Atlantic salmon (Salmo salar) to the European eel (Anguilla anguilla). Canadian Journal of Zoology 69, 733–737.CrossRefGoogle Scholar
Bakke, TA, Harris, PD, Jansen, PA and Hansen, LP (1992) Host specificity and dispersal strategy in gyrodactylid monogeneans, with particular reference to Gyrodactylus salaris (Platyhelminthes, Monogenea). Diseases of Aquatic Organisms 13, 63–74.CrossRefGoogle Scholar
Bakke, TA, Jansen, PA and Harris, PD (1996) Differences in susceptibility of anadromous and resident stocks of Arctic charr to infections of Gyrodactylus salaris, under experimental conditions. Journal of Fish Biology 49, 341–351.Google Scholar
Bakke, TA, Harris, PD and Cable, J (2002) Host specificity dynamics: observations on gyrodactylid monogeneans. International Journal for Parasitology 32, 281–308.CrossRefGoogle ScholarPubMed
Bakke, TA, Cable, J and Harris, PD (2007) The biology of gyrodactylid monogeneans: the “Russian-doll killers. Advances in Parasitology 64, 161–460.CrossRefGoogle ScholarPubMed
Beel, J and Gipp, B (2009) Google Scholar's ranking algorithm: an introductory overview. Presented at the Proceedings of the 12th International Conference on Scientometrics and Informetrics (ISSI’09), Rio de Janeiro, Brazil, 230–241.Google Scholar
Begon, M, Bennett, M, Bowers, RG, French, NP, Hazel, SM and Turner, J (2002) A clarification of transmission terms in host-microparasite models: numbers, densities and areas. Epidemiology & Infection 129, 147–153.CrossRefGoogle ScholarPubMed
Beldomenico, PM and Begon, M (2010) Disease spread, susceptibility and infection intensity: vicious circles? Trends in Ecology & Evolution 25, 21–27.CrossRefGoogle ScholarPubMed
Bikhovski, BE (1961) Monogenetic trematodes. Their Classification and Phylogeny. Monogenetic Trematodes, 1st Edn. Washington, USA: MBLWHOI Library.Google Scholar
Boeger, WA, Kritsky, DC, Pie, MR and Engers, KB (2005) Mode of transmission, host switching, and escape from the Red Queen by viviparous gyrodactylids (Monogenoidea). Journal of Parasitology 91, 1000–1007.CrossRefGoogle Scholar
Bonwitt, J, Dawson, M, Kandeh, M, Ansumana, R, Sahr, F, Brown, H and Kelly, AH (2018) Unintended consequences of the ‘bushmeat ban’ in West Africa during the 2013–2016 Ebola virus disease epidemic. Social Science & Medicine 200, 166–173.CrossRefGoogle ScholarPubMed
Briard, L and Ezenwa, VO (2021) Parasitism and host social behaviour: a meta-analysis of insights derived from social network analysis. Animal Behaviour 172, 171–182.CrossRefGoogle Scholar
Brooker, AJ, Grano-Maldonado, MI, Irving, S, Bron, JE, Longshaw, M and Shinn, AP (2011) The effect of octopaminergic compounds on the behaviour and transmission of Gyrodactylus. Parasites & Vectors 4, 207.CrossRefGoogle ScholarPubMed
Buchmann, K and Lindenstrøm, T (2002) Interactions between monogenean parasites and their fish hosts. International Journal for Parasitology 32, 309–319.CrossRefGoogle ScholarPubMed
Buchmann, K and Uldal, A (1997) Gyrodactylus derjavini infections in four salmonids: comparative host susceptibility and site selection of parasites. Diseases of Aquatic Organisms 28, 201–209.CrossRefGoogle Scholar
Buchmann, K, Lindenstrøm, T, Sigh, J, Dalgaard, JMB and Larsen, TB (2005) Susceptibility of Atlantic salmon to Gyrodactylus salaris infection is associated with unregulated cytokine expression. Bulletin-Scandinavian Society for Parasitology 14, 14–38.Google Scholar
Cable, J and Harris, PD (2002) Gyrodactylid developmental biology: historical review, current status and future trends. International Journal for Parasitology 32, 255–280.CrossRefGoogle ScholarPubMed
Cable, J and Van Oosterhout, C (2007a) The impact of parasites on the life history evolution of guppies (Poecilia reticulata): the effects of host size on parasite virulence. International Journal for Parasitology 37, 1449–1458.CrossRefGoogle Scholar
Cable, J and van Oosterhout, C (2007b) The role of innate and acquired resistance in two natural populations of guppies (Poecilia reticulata) infected with the ectoparasite Gyrodactylus turnbulli. Biological Journal of the Linnean Society 90, 647–655.CrossRefGoogle Scholar
Cable, J, Harris, PD, Tinsley, RC and Lazarus, CM (1999) Phylogenetic analysis of Gyrodactylus spp. (Platyhelminthes: Monogenea) using ribosomal DNA sequences. Canadian Journal of Zoology 77, 1439–1449.CrossRefGoogle Scholar
Cable, J, Harris, PD and Bakke, TA (2000) Population growth of Gyrodactylus salaris (Monogenea) on Norwegian and Baltic Atlantic salmon (Salmo salar) stocks. Parasitology 121, 621–629.CrossRefGoogle ScholarPubMed
Cable, J, Scott, EC, Tinsley, RC and Harris, PD (2002) Behavior favoring transmission in the viviparous monogenean Gyrodactylus turnbulli. Journal of Parasitology 88, 183–184.CrossRefGoogle ScholarPubMed
Cable, J, Archard, GA, Mohammed, RS, McMullan, M, Stephenson, JF, Hansen, H and Van Oosterhout, C (2013) Can parasites use predators to spread between primary hosts? Parasitology 140, 1138–1143.CrossRefGoogle ScholarPubMed
Callicott, B and Vaughn, D (2005) Google scholar vs library scholar: testing the performance of schoogle. Internet Reference Services Quarterly 10, 71–88.CrossRefGoogle Scholar
Cornet, S, Bichet, C, Larcombe, S, Faivre, B and Sorci, G (2014) Impact of host nutritional status on infection dynamics and parasite virulence in a bird-malaria system. Journal of Animal Ecology 83, 256–265.CrossRefGoogle Scholar
Croft, DP, Arrowsmith, J, Bielby, K, Skinnern, E, White, ID, Couzin, AE, Magurran, IR and Krause, J (2003) Mechanisms underlying shoal composition in the Trinidadian guppy, Poecilia reticulata. Oikos 100, 429–438.CrossRefGoogle Scholar
Croft, DP, Edenbrow, M, Darden, SK, Ramnarine, IW, Van Oosterhout, C and Cable, J (2011) Effect of gyrodactylid ectoparasites on host behaviour and social network structure in guppies Poecilia reticulata. Behavioral Ecology and Sociobiology 65, 2219–2227.CrossRefGoogle Scholar
Dargent F, , Torres-Dowdall J, Scott ME Ramnarine I, Fussmann GF (2013) Can mixed-species groups reduce individual parasite load? A field test with two closely related poeciliid fishes (Poecilia reticulata and Poecilia picta). Plos one 2, e56789. doi: 10.1371/journal.pone.0056789CrossRefGoogle Scholar
de Roij, J, Harris, PD and MacColl, ADC (2010) Divergent resistance to a monogenean flatworm among three-spined stickleback populations. Functional Ecology 25, 217–226.CrossRefGoogle Scholar
Detwiler, JT and Criscione, CD (2010) An infectious topic in reticulate evolution: introgression and hybridization in animal parasites. Genes (Basel) 1, 102–123.CrossRefGoogle ScholarPubMed
Dmitrieva, EV (2003) Transmission triggers and pathways in Gyrodactylus sphinx (Monogenea, Gyrodactylidae). Vestnik zoologii 37, 67–72.Google Scholar
Ezenwa, VO, Archie EA, ME, Hawley DM, C, Martin, LB, Moore, J and White, L (2016) Host behaviour-parasite feedback: an essential link between animal behaviour and disease ecology. Proceedings of the Royal Society B: Biological Sciences 283, 20153078. doi: 10.1098/rspb.2015.3078CrossRefGoogle ScholarPubMed
Frank, SA (1996) Models of parasite virulence. The Quarterly Review of Biology 71, 37–78.CrossRefGoogle ScholarPubMed
Funk, S, Bansal, S, Bauch, CT, Eames, KT, Edmunds, WJ, Galvani, AP and Klepac, P (2015) Nine challenges in incorporating the dynamics of behaviour in infectious diseases models. Epidemics 10, 21–25.CrossRefGoogle ScholarPubMed
García-Vásquez, A, Hansen, H, Christison, K, Rubio-Godoy, M, Bron, J and Shinn, A (2010) Gyrodactylids (Gyrodactylidae, Monogenea) infecting Oreochromis niloticus niloticus (L.) and O. mossambicus (Peters) (Cichlidae): A pan-global survey. Acta Parasitologica 55, 215–229. doi: 10.2478/s11686-010-0042-2CrossRefGoogle Scholar
García-Vásquez, A, Razo-Mendivil, U and Rubio-Godoy, M. (2017). Triple trouble? Invasive poeciliid fishes carry the introduced tilapia pathogen Gyrodactylus cichlidarum in the Mexican highlands. Veterinary Parasitology 235, 37–40. https://doi.org/10.1016/j.vetpar.2017.01.014CrossRefGoogle ScholarPubMed
García-Vásquez, A, Pinacho-Pinacho, CD, Guzmán-Valdivieso, I, Calixto-Rojas, M and Rubio-Godoy, M (2021) Morpho-molecular characterization of Gyrodactylus parasites of farmed tilapia and their spillover to native fishes in Mexico. Scientific Reports 11, 13957. doi: 10.1038/s41598-021-93472-6CrossRefGoogle ScholarPubMed
Getz, WM and Pickering, J (1983) Epidemic models: thresholds and population regulation. The American Naturalist 121, 892–898.CrossRefGoogle Scholar
Gilbey, J, Verspoor, E, Mo, TA, Sterud, E, Olstad, K, Hytterod, S, Jones, C and Noble, L (2006) Identification of genetic markers associated with Gyrodactylus salaris resistance in Atlantic salmon Salmo salar. Diseases of Aquatic Organisms 71, 119–129.CrossRefGoogle ScholarPubMed
Gotanda, KM, Delaire, LC, Raeymaekers, JA, Perez-Jvostov, F, Dargent, F, Bentzen, P, Scott, ME, Fussmann, GF and Hendry, AP (2013) Adding parasites to the guppy-predation story: insights from field surveys. Oecologia 172, 155–166.CrossRefGoogle Scholar
Grano-Maldonado, M, Moreno-Navas, J and Rodriguez-Santiago, MA (2018) Transmission strategies used by Gyrodactylus gasterostei (Monogenea) on its host, the three-spined stickleback Gasterosteus aculeatus. Fishes 3(20), 2–11. doi: 10.3390/fishes3020020CrossRefGoogle Scholar
Grether GF, , Kasahara S, Kolluru GR and Cooper EL, (2004) Sex–specific effects of carotenoid intake on the immunological response to allografts in guppies (Poecilia reticulata). Proceedings of the Royal Society B: Biological Sciences 271, 45–49. doi: doi:10.1098/rspb.2003.2526CrossRefGoogle Scholar
Harris, PD (1980) The effect of temperature upon population growth in the viviparous monogeneans Gyrodactylus. Parasitology 81, R26.Google Scholar
Harris, PD (1982). Studies on the biology of the Gyrodactyloidea (Monogenea) (PhD Thesis). Mary University of London.Google Scholar
Harris, PD (1988) Changes in the site specificity of Gyrodactylus turnbulli Harris, 1986 (Monogenea) during infections of individual guppies (Poecilia reticulata Peters, 1859). Canadian Journal of Zoology 66, 2854–2857.CrossRefGoogle Scholar
Harris, PD (1989) Interactions between population growth and sexual reproduction in the viviparous monogenean Gyrodactylus turnbulli Harris, 1986 from the guppy Poecilia reticulata Peters. Parasitology 98, 245–251.CrossRefGoogle Scholar
Harris, PD and Lyles, AM (1992) Infections of Gyrodactylus bullatarudis and Gyrodactylus turnbulli on guppies (Poecilia reticulata) in Trinidad. The Journal of Parasitology, 912–914. doi: 10.2307/3283329CrossRefGoogle Scholar
Harris, PD, Shinn, AP, Cable, J and Bakke, TA (2004) Nominal species of the genus Gyrodactylus von Nordmann 1832 (Monogenea: Gyrodactylidae), with a list of principal host species. Systematic Parasitology 59, 1–27.CrossRefGoogle Scholar
Hawley, DM, Etienne, RS, Ezenwa, VO and Jolles, AE (2011) Does animal behavior underlie covariation between hosts’ exposure to infectious agents and susceptibility to infection? Implications for disease dynamics. Integrative and Comparative Biology 51, 528–539.CrossRefGoogle ScholarPubMed
Hawley, DM, Gibson, AK, Townsend, AK, Craft, ME and Stephenson, JF (2021) Bidirectional interactions between host social behaviour and parasites arise through ecological and evolutionary processes. Parasitology 148, 274–288.CrossRefGoogle ScholarPubMed
Heesterbeek, JA (2002) A brief history of R0 and a recipe for its calculation. Acta Biotheoretica 50, 189–204.CrossRefGoogle Scholar
Heggberget, TG and Johnsen, BO (1982) Infestations by Gyrodactylus sp. of Atlantic salmon, Salmo salar L., in Norwegian rivers. Journal of Fish Biology 21, 15–26.CrossRefGoogle Scholar
Hendrichsen DK, , Kristoffersen R, Gjelland KØ, Knudsen R, Kusterle S, Rikardsen AH, Henriksen EH, Smalås A, Olstad K (2015) Sex–specific effects of carotenoid intake on the immunological response to allografts in guppies (Poecilia reticulata). Proceedings of the Royal Society B: Biological Sciences 271, 45–49. doi: 10.1098/rspb.2003.2526Google Scholar
Hockley FA, , Wilson CA, Brew A and Cable J, (2014) Fish responses to flow velocity and turbulence in relation to size, sex and parasite load. Journal of The Royal Society Interface 11, 20130814. doi: 10.1098/rsif.2013.0814CrossRefGoogle ScholarPubMed
Hoffman, GL and Putz, RE (1964) Studies on Gyrodactylus macrochiri n.sp. (Trematoda: Monogenea) from Lepomis macrochirus. Proceedings of the Helminthological Society of Washington 31, 76–82.Google Scholar
Houde, A (1998) Sex, Color, and Mate Choice in Guppies, 1st Edn. Princeton, EUA: Princeton University Press.CrossRefGoogle Scholar
Houde, AE and Torio, AJ (1992) Effect of parasitic infection on male color pattern and female choice in guppies. Behavioral Ecology 3, 346–351.CrossRefGoogle Scholar
Huyse, T, Audenaert, V and Volckaert, FA (2003) Speciation and host-parasite relationships in the parasite genus Gyrodactylus (Monogenea, Platyhelminthes) infecting gobies of the genus Pomatoschistus (Gobiidae, Teleostei). International Journal for Parasitology 33, 1679–1689.CrossRefGoogle Scholar
Janecka, MJ, Rovenolt, F and Stephenson, JF (2021) How does host social behavior drive parasite non-selective evolution from the within-host to the landscape-scale? Behavioral Ecology and Sociobiology 75. doi: doi:10.1007/s00265-021-03089-yCrossRefGoogle Scholar
Janeway, CA, Travers, P and Walport, M (2001) Immunobiology: The Immune System in Health and Disease, 5th Edn. New York: Garland Science. Principles of innate and adaptive immunity. Available at https://www.ncbi.nlm.nih.gov/books/NBK27090/Google Scholar
Jansen, PA and Bakke, TA (1991) Temperature-dependent reproduction and survival of Gyrodactylus salaris Malmberg, 1957 (Platyhelminthes: Monogenea) on Atlantic salmon (Salmo salar L.). Parasitology 102, 105–112.CrossRefGoogle Scholar
Johnsen, BO and Jensen, AJ (1986) Infestations of Atlantic salmon, Salmo salar, by Gyrodactylus salaris in Norwegian rivers. Journal of Fish Biology 29, 233–241.CrossRefGoogle Scholar
Johnsen, BO and Jensen, AJ (1992) Infection of Atlantic salmon, Salmo salar L., by Gyrodactylus salaris, Malmberg 1957, in the River Lakselva, Misvaer in northern Norway. Journal of Fish Biology 40, 433–444.CrossRefGoogle Scholar
Johnson, MB, Lafferty, KD, Van Oosterhout, C and Cable, J (2011) Parasite transmission in social interacting hosts: monogenean epidemics in guppies. PLoS One 6, e22634.CrossRefGoogle ScholarPubMed
Kamiso, HN and Olson, RE (1986) Host-parasite relationships between Gyrodactylus stellatus (Monogenea: Gyrodactylidae) and Parophrys vetulus (Pleuronectidae: English Sole) from coastal waters of Oregon. The Journal of Parasitology 72, 125–129. doi: 10.2307/3281804CrossRefGoogle Scholar
Kennedy, CEJ, Endler, JA, Poynton, SL and McMinn, H (1987) Parasite load predicts mate choice in guppies. Behavioral Ecology and Sociobiology 21, 291–295.CrossRefGoogle Scholar
King, TA and Cable, J (2007) Experimental infections of the monogenean Gyrodactylus turnbulli indicate that it is not a strict specialist. International Journal for Parasitology 37, 663–672.CrossRefGoogle Scholar
King, TA, van Oosterhout, C and Cable, J (2009) Experimental infections with the tropical monogenean, Gyrodactylus bullatarudis: potential invader or experimental fluke? Parasitology International 58, 249–254.CrossRefGoogle ScholarPubMed
Knell, RJ and Webberley, KM (2004) Sexually transmitted diseases of insects: distribution, evolution, ecology and host behaviour. Biological Reviews 79, 557–581.CrossRefGoogle ScholarPubMed
Kolluru, GR, Grether, GF, Dunlop, E and South, SH (2009) Food availability and parasite infection influence mating tactics in guppies (Poecilia reticulata). Behavioral Ecology 20, 131–137.CrossRefGoogle Scholar
Kolluru GR, , Grether GF, South SH, Dunlop E, Cardinali A, Liu L, Carapiet A (2006) The effects of carotenoid and food availability on resistance to a naturally occurring parasite (Gyrodactylus turnbulli) in guppies (Poecilia reticulata). Biological Journal of the Linnean Society 40, 433–444. doi: 10.1111/j.1095-8649.1992.tb02588.xGoogle Scholar
Konczal, M, Ellison, AR, Phillips, KP, Radwan, J, Mohammed, RS, Cable, J and Chadzinska, M (2020a) RNA-Seq analysis of the guppy immune response against Gyrodactylus bullatarudis infection. Parasite Immunology 42, e12782.CrossRefGoogle Scholar
Konczal, M, Przesmycka, KJ, Mohammed, RS, Phillips, KP, Camara, F, Chmielewski, S, Hahn, C, Guigo, R, Cable, J and Radwan, J (2020b) Gene duplications, divergence and recombination shape adaptive evolution of the fish ectoparasite Gyrodactylus bullatarudis. Molecular Ecology 29, 1494–1507.CrossRefGoogle Scholar
Konczal, M, Przesmycka, KJ, Mohammed, RS, Hahn, C, Cable, J and Radwan, J (2021) Expansion of frozen hybrids in the guppy ectoparasite, Gyrodactylus turnbulli. Molecular Ecology 30, 1005–1016.CrossRefGoogle ScholarPubMed
Koski, P, Anttila, P and Kuusela, J (2015) Killing of Gyrodactylus salaris by heat and chemical disinfection. Acta Veterinaria Scandinavica 58, 1–6. doi: 10.1186/s13028-016-0202-yCrossRefGoogle Scholar
Kuusela, J, Zietara, MS and Lumme, J (2007) Hybrid origin of Baltic salmon-specific parasite Gyrodactylus salaris: a model for speciation by host switch for hemiclonal organisms. Molecular Ecology 16, 5234–5245.CrossRefGoogle Scholar
Lambrechts, L, Scott, TW and Gubler, DJ (2010) Consequences of the expanding global distribution of Aedes albopictus for dengue virus transmission. PLoS Neglected Tropical Diseases 4, e646.CrossRefGoogle ScholarPubMed
Lindenstrøm, T and Buchmann, K (2000) Acquired resistance in rainbow trout against Gyrodactylus derjavini. Journal of Helminthology 74, 155–166.CrossRefGoogle ScholarPubMed
Lindenstrøm, T, Secombes, CJ and Buchmann, K (2004) Expression of immune response genes in rainbow trout skin induced by Gyrodactylus derjavini infections. Veterinary Immunology and Immunopathology 97, 137–148.CrossRefGoogle ScholarPubMed
Lipsitch, M and Moxon, E (1997) Virulence and transmissibility of pathogens: what is the relationship? Trends in Microbiology 5, 31–37.CrossRefGoogle ScholarPubMed
Llewellyn, J (1984) The biology of Isancistrum subulatae n. sp., a monogenean parasitic on the squid, Alloteuthis subulata, at Plymouth. Journal of the Marine Biological Association of the United Kingdom 64, 285–302.CrossRefGoogle Scholar
Lloyd-Smith, JO, Cross, PC, Briggs, CJ, Daugherty, M, Getz, WM, Latto, J, Sanchez, MS, Smith, AB and Swei, A (2005a) Should we expect population thresholds for wildlife disease? Trends in Ecology & Evolution 20, 511–519.CrossRefGoogle Scholar
Lloyd-Smith, JO, Schreiber, SJ, Kopp, PE and Getz, WM (2005b) Superspreading and the effect of individual variation on disease emergence. Nature 438, 355–359.CrossRefGoogle Scholar
López, S (1999) Parasitized female guppies do not prefer showy males. Animal Behaviour 57, 1129–1134.CrossRefGoogle Scholar
Lumme J, and Ziętara MS, (2018) Horizontal transmission of the ectoparasite Gyrodactylus arcuatus (Monogenea: Gyrodactylidae) to the next generation of the three-spined stickleback Gasterosteus aculeatus. Folia parasitologica 65, 1–8. doi: 10.14411/fp.2018.006CrossRefGoogle Scholar
Maceda-Veiga, A and Cable, J (2019) Diseased fish in the freshwater trade: from retailers to private aquarists. Diseases of Aquatic Organisms 132, 157–162.CrossRefGoogle ScholarPubMed
Madhavi, R and Anderson, RM (1985) Variability in the susceptibility of the fish host, Poecilia reticulata, to infection with Gyrodactylus bullatarudis (Monogenea). Parasitology 91, 531–544.CrossRefGoogle Scholar
Magurran, AE and Seghers, BH (1994) A cost of sexual harassment in the guppy, Poecilia reticulata. Proceedings of the Royal Society of London. Series B: Biological Sciences 258, 89–92.Google Scholar
Mahmud, MA, Bradley, JE and MacColl, AD (2017) Abiotic environmental variation drives virulence evolution in a fish host–parasite geographic mosaic. Functional Ecology 31, 2138–2146.CrossRefGoogle Scholar
Malmberg, G (1970) The excretory systems and marginal hooks as a basis for the systematics of Gyrodactylus (Trematoda, Monogenea). Arkiv for Zoologi 23, 1–235.Google Scholar
Marcogliese, DJ (1995) The role of zooplankton in the transmission of helminth parasites to fish. Reviews in Fish Biology and Fisheries 5, 336–371.CrossRefGoogle Scholar
Martin-Martin, A, Orduna-Malea, E, Harzing, A-W and López-Cózar, D (2017) Can we use Google Scholar to identify highly-cited documents? Journal of Informetrics 11, 163.CrossRefGoogle Scholar
Martin, CH and Johnsen, S (2007) A field test of the Hamilton–Zuk hypothesis in the Trinidadian guppy (Poecilia reticulata). Behavioral Ecology and Sociobiology 61, 1897–1909.CrossRefGoogle Scholar
Matejusova, I, Felix, B, Sorsa-Leslie, T, Gilbey, J, Noble, LR, Jones, CS and Cunningham, CO (2006) Gene expression profiles of some immune relevant genes from skin of susceptible and responding Atlantic salmon (Salmo salar L.) infected with Gyrodactylus salaris (Monogenea) revealed by suppressive subtractive hybridisation. International Journal for Parasitology 36, 1175–1183.CrossRefGoogle ScholarPubMed
McCallum, H (2001) How should pathogen transmission be modelled? Trends in Ecology & Evolution 16, 295–300.CrossRefGoogle ScholarPubMed
McCallum, H, Fenton, A, Hudson, PJ, Lee, B, Levick, B, Norman, R, Perkins, SE, Viney, M, Wilson, AJ and Lello, J (2017) Breaking beta: deconstructing the parasite transmission function. Philosophical Transactions of the Royal Society B: Biological Sciences 372, 20160084.CrossRefGoogle ScholarPubMed
Meinilä, M, Kuusela, J, Ziętara, MS and Lumme, J (2004) Initial steps of speciation by geographic isolation and host switch in salmonid pathogen Gyrodactylus salaris (Monogenea: Gyrodactylidae). International Journal for Parasitology 34, 515–526.CrossRefGoogle Scholar
Milei, J, Guerri-Guttenberg, RA, Grana, DR and Storino, R (2009) Prognostic impact of Chagas disease in the United States. American Heart Journal 157, 22–29.CrossRefGoogle ScholarPubMed
Mo, TA (1992) Seasonal variations in the prevalence and infestation intensity of Gyrodactylus salaris Malmberg, 1957 (Monogenea, Gyrodactylidae) on Atlantic Salmon parr, Salmo-Salar L., in the River Batnfjordselva, Norway. Journal of Fish Biology 41, 697–707. https://doi.org/10.1111/j.1095-8649.1992.tb02699.xCrossRefGoogle Scholar
Mo, TA (1997) Seasonal occurrence of Gyrodactylus derjavini (Monogenea) on brown trout, Salmo trutta, and Atlantic salmon, S. salar, in the Sandvikselva river, Norway. The Journal of Parasitology 83, 1025–1029. doi: 10.2307/3284356CrossRefGoogle ScholarPubMed
Mohammed, RS, King, SD, Bentzen, P, Marcogliese, D, van Oosterhout, C and Lighten, J (2020) Parasite diversity and ecology in a model species, the guppy (Poecilia reticulata) in Trinidad. Royal Society Open Science 7, 191112.CrossRefGoogle Scholar
Moher, D, Liberati, A, Tetzlaff, J and Altman, DG and PRISMA Group (2015) Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. Open Medicine 3, 123–130. doi: 10.1186/2046-4053-4-1Google Scholar
Moore, J (2002) Parasites and the Behavior of Animals, 2nd Edn. Colorado, USA: Oxford University Press on Demand.Google Scholar
Olstad, K, Cable, J, Robertsen, G and Bakke, TA (2006) Unpredicted transmission strategy of Gyrodactylus salaris (Monogenea: Gyrodactylidae): survival and infectivity of parasites on dead hosts. Parasitology 133, 33–41.CrossRefGoogle ScholarPubMed
Paladini, G, Shinn, AP, Taylor, NG, Bron, JE and Hansen, H (2021) Geographical distribution of Gyrodactylus salaris Malmberg, 1957 (Monogenea, Gyrodactylidae). Parasites & Vectors 14, 1–20. doi: 10.1186/s13071-020-04504-5CrossRefGoogle Scholar
Parker, JD (1965). Seasonal Occurence, Transmission, and Host Specificity of the Monogenetic Trematode Gyrodactylus elegans from the Golden Shiner (Notemigonus crysoleucas) (PhD thesis). Southern Illinois.Google Scholar
Peeler EJ, , Gardiner R, Thrush MA (2004) Qualitative risk assessment of routes of transmission of the exotic fish parasite Gyrodactylus salaris between river catchments in England and Wales. Preventive veterinary medicine 65, 1–8. doi: 10.1016/j.prevetmed.2004.05.005Google Scholar
Poleo, AB, Schjolden, J, Hansen, H, Bakke, TA, Mo, TA, Rosseland, BO and Lydersen, E (2004) The effect of various metals on Gyrodactylus salaris (Platyhelminthes, Monogenea) infections in Atlantic salmon (Salmo salar). Parasitology 128, 169–177.CrossRefGoogle Scholar
Poulin, R (2020) Meta-analysis of seasonal dynamics of parasite infections in aquatic ecosystems. International Journal for Parasitology 50, 501–510.CrossRefGoogle ScholarPubMed
Råberg, L, Graham, AL and Read, AF (2009) Decomposing health: tolerance and resistance to parasites in animals. Philosophical Transactions of the Royal Society B: Biological Sciences 364, 37–49.CrossRefGoogle ScholarPubMed
Rahn, AK, Hammer, DA and Bakker, TC (2015) Experimental infection with the directly transmitted parasite Gyrodactylus influences shoaling behaviour in sticklebacks. Animal Behaviour 107, 253–261.CrossRefGoogle Scholar
Ravel C, , Cortes S, Pratlong F, Dedet JP, Campino L (2006) First report of genetic hybrids between two very divergent Leishmania species: Leishmania infantum and Leishmania major. International Journal for Parasitology 36, 1383–1388. doi: 10.1016/j.ijpara.2006.06.019CrossRefGoogle ScholarPubMed
Reynolds, M, Arapi, EA and Cable, J (2018) Parasite-mediated host behavioural modifications: Gyrodactylus turnbulli infected Trinidadian guppies increase contact rates with uninfected conspecifics. Parasitology 145, 920–926.CrossRefGoogle ScholarPubMed
Reynolds, M, Hockley, FA, Wilson, C and Cable, J (2019) Assessing the effects of water flow rate on parasite transmission amongst a social host. Hydrobiologia 830, 201–212.CrossRefGoogle Scholar
Reznick, D (1995) Life history evolution in guppies: a model system for the empirical study of adaptation. Netherlands Journal of Zoology 46, 172–190.CrossRefGoogle Scholar
Richards, GR and Chubb, JC (1996) Host response to initial and challenge infections, following treatment, of Gyrodactylus bullatarudis and G. turnbulli (Monogenea) on the guppy (Poecilia reticulata). Parasitology Research 82, 242–247.CrossRefGoogle Scholar
Richards, GR and Chubb, JC (1998) Longer-term population dynamics of Gyrodactylus bullatarudis and G. turnbulli (Monogenea) on adult guppies (Poecilia reticulata) in 50-I experimental arenas. Parasitology Research 84, 753–756.CrossRefGoogle Scholar
Richards, EL, Van Oosterhout, C and Cable, J (2010) Sex-specific differences in shoaling affect parasite transmission in guppies. PLoS One 5, e13285.CrossRefGoogle ScholarPubMed
Richards, EL, Van Oosterhout, C and Cable, J (2012) Interactions between males guppies facilitates the transmission of the monogenean ectoparasite Gyrodactylus turnbulli. Experimental Parasitology 132, 483–486.CrossRefGoogle ScholarPubMed
Roberts, MG (2007) The pluses and minuses of R0. Journal of the Royal Society Interface 4, 949–961.CrossRefGoogle ScholarPubMed
Robertson, S, Bradley, JE and MacColl, ADC (2017) No evidence of local adaptation of immune responses to Gyrodactylus in three-spined stickleback (Gasterosteus aculeatus). Fish & Shellfish Immunology 60, 275–281.CrossRefGoogle Scholar
Rubio-Godoy, M, Muñoz-Córdova, G, Garduño-Lugo, M, Salazar-Ulloa, M and Mercado-Vidal, G (2012) Microhabitat use, not temperature, regulates intensity of Gyrodactylus cichlidarum long-term infection on farmed tilapia—Are parasites evading competition or immunity? Veterinary Parasitology 183, 305–316.CrossRefGoogle ScholarPubMed
Ryder, JJ, Miller, MR, White, A, Knell, RJ and Boots, M (2007) Host-parasite population dynamics under combined frequency- and density-dependent transmission. Oikos 116, 2017–2026.CrossRefGoogle Scholar
Schelkle, B, Faria, PJ, Johnson, MB, Van Oosterhout, C and Cable, J (2012) Mixed infections and hybridisation in monogenean parasites. PLoS One 7, e39506.CrossRefGoogle ScholarPubMed
Scott, ME (1982) Reproductive potential of Gyrodactylus bullatarudis (Monogenea) on guppies (Poecilia reticulata). Parasitology 85, 217–236.CrossRefGoogle Scholar
Scott, ME and Anderson, RM (1984) The population dynamics of Gyrodactylus bullatarudis (Monogenea) within laboratory populations of the fish host Poecilia reticulata. Parasitology 89, 159–194.CrossRefGoogle ScholarPubMed
Scott, ME and Nokes, DJ (1984) Temperature-dependent reproduction and survival of Gyrodactylus bullatarudis (Monogenea) on guppies (Poecilia reticulata). Parasitology 89, 221–228.CrossRefGoogle Scholar
Seghers, BH (1974) Schooling behavior in the guppy (Poecilia reticulata): an evolutionary response to predation. Evolution 28, 486–489.Google ScholarPubMed
Smith, KF, Acevedo-Whitehouse, K and Pedersen, AB (2009) The role of infectious diseases in biological conservation. Animal Conservation 12, 1–12.CrossRefGoogle Scholar
Soleng, A and Bakke, T (1998) The susceptibility of three-spined strickleback (Gasterosteus aculeatus), nine-spined stickleback (Pungitius pungitius) and flounder (Platichthys flesus) to the monogenean Gyrodactylus salaris. Parasitology International 47, 270–274. doi: 10.1016/s1383-5769(98)80928-8CrossRefGoogle Scholar
Soleng, A, Bakke, TA and Hansen, LP (1998) Potential for dispersal of Gyrodactylus salaris (Platyhelminthes, Monogenea) by sea-running stages of the Atlantic salmon (Salmo salar): field and laboratory studies. Canadian Journal of Fisheries and Aquatic Sciences 55, 507–514. doi: 10.1016/S1383-5769(98)80928-8CrossRefGoogle Scholar
Soleng, A, Jansen, PA and Bakke, TA (1999) Transmission of the monogenean Gyrodactylus salaris. Folia Parasitologica 4, 179–184.Google Scholar
Soleng, A, Poleo Antonio, BS and Bakke, TA (2005) Toxicity of aqueous aluminium to the ectoparasitic monogenean Gyrodactylus salaris. Aquaculture 250, 616–620.CrossRefGoogle Scholar
Soler-Jiménez, LC, Paredes-Trujillo, AI and Vidal-Martínez, VM (2017) Helminth parasites of finfish commercial aquaculture in Latin America. Journal of Helminthology 91, 110–136.CrossRefGoogle ScholarPubMed
Stephenson, JF (2019) Parasite-induced plasticity in host social behaviour depends on sex and susceptibility. Biology Letters 15, 20190557.CrossRefGoogle ScholarPubMed
Stephenson, JF and Reynolds, M (2016) Imprinting can cause a maladaptive preference for infectious conspecifics. Biology Letters 12, 20160020. doi: 10.1098/rsbl.2016.0020CrossRefGoogle Scholar
Stephenson, JF, Van Oosterhout, C, Mohammed, RS and Cable, J (2015) Parasites of Trinidadian guppies: evidence for sex- and age-specific trait-mediated indirect effects of predators. Ecology 96, 489–498.CrossRefGoogle ScholarPubMed
Stephenson, JF, Kinsella, C, Cable, J and Van Oosterhout, C (2016) A further cost for the sicker sex? Evidence for male-biased parasite-induced vulnerability to predation. Ecology and Evolution 6, 2506–2515.CrossRefGoogle ScholarPubMed
Stephenson, JF, Young, KA, Fox, J, Jokela, J, Cable, J and Perkins, SE (2017) Host heterogeneity affects both parasite transmission to and fitness on subsequent hosts. Philosophical Transactions of the Royal Society B: Biological Sciences 372, 20160093. doi: 10.1098/rstb.2016.0093CrossRefGoogle ScholarPubMed
Stephenson JF, , Perkins SE, Cable J (2018) Transmission risk predicts avoidance of infected conspecifics in Trinidadian guppies. Journal of Animal Ecology 87, 1525–1533. doi: 10.1111/1365-2656.12885CrossRefGoogle ScholarPubMed
Tadiri, CP, Dargent, F and Scott, ME (2013) Relative host body condition and food availability influence epidemic dynamics: a Poecilia reticulata-Gyrodactylus turnbulli host-parasite model. Parasitology 140, 343–351.CrossRefGoogle ScholarPubMed
Tadiri, CP, Scott, ME and Fussmann, GF (2016) Impact of host sex and group composition on parasite dynamics in experimental populations. Parasitology 143, 523–531.CrossRefGoogle ScholarPubMed
Tadiri, CP, Scott, ME and Fussmann, GF (2018) Microparasite dispersal in metapopulations: a boon or bane to the host population? Proceedings of the Royal Society B: Biological Sciences 285, 20181519.CrossRefGoogle ScholarPubMed
Tadiri, CP, Kong, JD, Fussmann, GF, Scott, ME and Wang, H (2019) A data-validated host-parasite model for infectious disease outbreaks. Frontiers in Ecology and Evolution 7, 307. doi: 10.3389/fevo.2019.00307CrossRefGoogle Scholar
Tang JA, , Templeton TJ, Cao J and Culleton R, (2020) The consequences of mixed-species malaria parasite co-infections in mice and mosquitoes for disease severity, parasite fitness, and transmission success. Frontiers in Immunology 10. doi: 10.3389/fimmu.2019.03072Google Scholar
Thrall, PH, Antonovics, J and Dobson, AP (2000) Sexually transmitted diseases in polygynous mating systems: prevalence and impact on reproductive success. Proceedings of the Royal Society of London. Series B: Biological Sciences 267, 1555–1563.CrossRefGoogle ScholarPubMed
Trujillo-González, A, Becker, JA, Vaughan, DB and Hutson, KS (2018) Monogenean parasites infect ornamental fish imported to Australia. Parasitology Research 117, 995–1011.CrossRefGoogle ScholarPubMed
VanderWaal, KL and Ezenwa, VO (2016) Heterogeneity in pathogen transmission: mechanisms and methodology. Functional Ecology 30, 1606–1622.CrossRefGoogle Scholar
van Oosterhout, C, Potter, R, Wright, H and Cable, J (2008) Gyro-scope: an individual-based computer model to forecast gyrodactylid infections on fish hosts. International Journal for Parasitology 38, 541–548.CrossRefGoogle ScholarPubMed
van Oosterhout C, , Harris PD, Cable J (2003) Marked variation in parasite resistance between two wild populations of the Trinidadian guppy, Poecilia reticulata (Pisces: Poeciliidae). Biological Journal of the Linnean Society 79, 645–651. doi: 10.1046/j.1095-8312.2003.00203.xCrossRefGoogle Scholar
White, LA, Forester, JD and Craft, ME (2018) Covariation between the physiological and behavioral components of pathogen transmission: host heterogeneity determines epidemic outcomes. Oikos 127, 538–552.CrossRefGoogle Scholar
Winger, AC, Kanck, M, Kristoffersen R, and Knudsen R, (2007) Seasonal dynamics and persistence of Gyrodactylus salaris in two riverine anadromous Arctic charr populations. Environmental Biology of Fishes 83, 117–123. doi: 10.1007/s10641-007-9274-xCrossRefGoogle Scholar
World Health Organization (2020) Covid-19 SPRP Monitoring Framework-Global Overview. Geneva, Switzerland: World Health Organization.Google Scholar
Zhang, S, Zhi, T, Xu, X, Zheng, Y, Bilong Bilong, CF, Pariselle, A and Yang, T (2019) Monogenean fauna of alien tilapias (Cichlidae) in south China. Parasite 26, 4.CrossRefGoogle ScholarPubMed
Zhou, S, Zou, H, Wu, SG, Wang, GT, Marcogliese, DJ and Li, WX (2017) Effects of goldfish (Carassius auratus) population size and body condition on the transmission of Gyrodactylus kobayashii (Monogenea). Parasitology 144, 1221–1228.CrossRefGoogle Scholar
Zhou, S, Li, WX, Zou, H, Zhang, J, Wu, SG, Li, M and Wang, GT (2018) Expression analysis of immune genes in goldfish (Carassius auratus) infected with the monogenean parasite Gyrodactylus kobayashii. Fish and Shellfish Immunology 77, 40–45.CrossRefGoogle ScholarPubMed
Zhou, S, Liu, Y, Dong, J, Yang, Q, Xu, N, Yang, Y, Gu, Z and Ai, X (2021) Transcriptome analysis of goldfish (Carassius auratus) in response to Gyrodactylus kobayashii infection. Parasitology Research 120, 161–171.CrossRefGoogle ScholarPubMed
Ziętara, MS and Lumme, J (2002) Speciation by host switch and adaptive radiation in a fish parasite genus Gyrodactylus (Monogenea, Gyrodactylidae). Evolution 56, 2445–2458.CrossRefGoogle Scholar