Hostname: page-component-848d4c4894-pjpqr Total loading time: 0 Render date: 2024-06-18T06:20:48.501Z Has data issue: false hasContentIssue false

Population growth of Gyrodactylus kobayashii in goldfish (Carassius auratus) associated with host density

Published online by Cambridge University Press:  21 April 2022

Xiao Jin
Affiliation:
Key Laboratory of Aquaculture Disease Control, Ministry of Agriculture, and State Key Laboratory of Freshwater Ecology and Biotechnology, Institute of Hydrobiology, Chinese Academy of Sciences, Wuhan 430072, People's Republic of China University of Chinese Academy of Sciences, Beijing 100049, People's Republic of China
Hong Zou
Affiliation:
Key Laboratory of Aquaculture Disease Control, Ministry of Agriculture, and State Key Laboratory of Freshwater Ecology and Biotechnology, Institute of Hydrobiology, Chinese Academy of Sciences, Wuhan 430072, People's Republic of China
Ming Li
Affiliation:
Key Laboratory of Aquaculture Disease Control, Ministry of Agriculture, and State Key Laboratory of Freshwater Ecology and Biotechnology, Institute of Hydrobiology, Chinese Academy of Sciences, Wuhan 430072, People's Republic of China
Shangong Wu
Affiliation:
Key Laboratory of Aquaculture Disease Control, Ministry of Agriculture, and State Key Laboratory of Freshwater Ecology and Biotechnology, Institute of Hydrobiology, Chinese Academy of Sciences, Wuhan 430072, People's Republic of China
Guitang Wang
Affiliation:
Key Laboratory of Aquaculture Disease Control, Ministry of Agriculture, and State Key Laboratory of Freshwater Ecology and Biotechnology, Institute of Hydrobiology, Chinese Academy of Sciences, Wuhan 430072, People's Republic of China
David J. Marcogliese
Affiliation:
Aquatic Contaminants Research Division, Water Science and Technology Directorate, Science and Technology Branch, Environment and Climate Change Canada, St. Lawrence Centre, 105 McGill, 7th floor, Montreal, Quebec H2Y 2E7, Canada St. Andrews Biological Station, Fisheries and Oceans Canada, 125 Marine Science Drive, St. Andrews, New Brunswick E5B 0E4, Canada
Wenxiang Li*
Affiliation:
Key Laboratory of Aquaculture Disease Control, Ministry of Agriculture, and State Key Laboratory of Freshwater Ecology and Biotechnology, Institute of Hydrobiology, Chinese Academy of Sciences, Wuhan 430072, People's Republic of China University of Chinese Academy of Sciences, Beijing 100049, People's Republic of China
*
Author for correspondence: Wenxiang Li, E-mail: liwx@ihb.ac.cn

Abstract

Host density is a key regulatory factor in parasite transmission. The goldfish (Carassius auratus)-Gyrodactylus kobayashii model was used to investigate effects of host density on population growth of gyrodactylids. A donor fish infected by five gravid gyrodactylids was mixed with 11 parasite-free goldfish at five host densities. There was a significant positive correlation between host density and mean abundance of G. kobayashii throughout the 58-day experiment. During early infection (days 15–24), mean abundance in medium high (0.5 fish L−1) and high host density groups (1 and 2 fish L−1) was significantly higher than that in the low host density groups (0.125 and 0.25 fish L−1). At high host density, prevalence increased more rapidly, and the peak prevalence was higher. Fitting of an exponential growth model showed that the population growth rate of the parasite increased with host density. A hypothesis was proposed that higher host density contributed to increased reinfection of detached gyrodactylids. A reinfection experiment was designed to test this hypothesis. Both mean abundance and prevalence at a host density of 1 fish L−1 were significantly higher than those at 0.25 fish L−1 on days 1 and 3, which suggested that more reinfections of G. kobyashii occurred at the higher host density. Density-dependent transmission during the early infection was an important contributor of population growth of G. kobayashii, as well as density-dependent reinfection of the detached gyrodactylids.

Type
Research Article
Copyright
Copyright © The Author(s), 2022. Published by Cambridge University Press

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Anderson, RM and May, RM (1979) Population biology of infectious diseases: Part I. Nature 280, 361367.CrossRefGoogle ScholarPubMed
Anderson, MR and May, RM (1991) Infectious Diseases of Humans: Dynamics and Control. New York: Oxford University Press.Google Scholar
Arneberg, P, Skorping, A, Grenfell, B and Read, AF (1998) Host densities as determinants of abundance in parasite communities. Proceedings of the Royal Society of London, Series B: Biological Sciences 265, 12831289.CrossRefGoogle Scholar
Bakke, TA, Harris, PD, Jansen, P 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, 6374.CrossRefGoogle Scholar
Bakke, TA, Cable, J and Harris, PD (2007) The biology of gyrodactylid monogeneans: the “Russian-doll killers”. Advances in Parasitology 64, 161460.CrossRefGoogle Scholar
Barlow, ND (1996) The ecology of wildlife disease control: simple models revisited. Journal of Applied Ecology 33, 303314.CrossRefGoogle Scholar
Begon, M, Feore, SM, Brown, K, Chantrey, J, Jones, T and Bennett, M (1998) Population and transmission dynamics of cowpox in bank voles: testing fundamental assumptions. Ecology Letters 1, 8286.CrossRefGoogle Scholar
Bush, AO, Lafferty, KD, Lotz, JM, Shostak, AW (1997) Parasitology meets ecology on its own terms: Margolis, et al. revisited. Journal of Parasitology 83, 575583.CrossRefGoogle ScholarPubMed
Cable, J and Harris, PD (2002) Gyrodactylid developmental biology: historical review, current status and future trends. International Journal for Parasitology 32, 255280.CrossRefGoogle ScholarPubMed
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, 621629.CrossRefGoogle ScholarPubMed
Cable, J, Scott, ECG, Tinsley, RC and Harris, PD (2002a) Behavior favoring transmission in the viviparous monogenean Gyrodactylus turnbulli. Journal of Parasitology 88, 183184.CrossRefGoogle Scholar
Cable, J, Tinsley, RC and Harris, PD (2002b) Survival, feeding and embryo development of Gyrodactylus gasterostei (Monogenea: Gyrodactylidae). Parasitology 124, 5368.CrossRefGoogle Scholar
Earn, DJD, Rohani, P, Bolker, BM and Grenfell, BT (2000) A simple model for complex dynamical transitions in epidemics. Science 287, 667670.CrossRefGoogle ScholarPubMed
Gheorgiu, C, Marcogliese, DJ and Scott, M (2006) Concentration-dependent effects of waterborne zinc on population dynamics of Gyrodactylus turnbulli (Monogenea) on isolated guppies (Poecilia reticulata). Parasitology 132, 225232.CrossRefGoogle Scholar
Harris, PD (1982) Studies of the Gyrodactyloldea (Monogenea) (PhD). 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, 28542857.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, 245251.CrossRefGoogle Scholar
Jansen, PA and Bakke, TA (1991) Temperature-dependent reproduction and survival of Gyrodactylus salaris Malmberg, 1957 (Platyhelminthes: Monogenea) on Atlantic salmon (Salmo salar). Parasitology 102, 105112.CrossRefGoogle Scholar
Jansen, PA, Kristoffersen, AB, Viljugrein, H, Jimenez, D, Aldrin, M and Stien, A (2012) Sea lice as a density-dependent constraint to salmonid farming. Proceedings of the Royal Society B-Biological Sciences 279, 23302338.CrossRefGoogle ScholarPubMed
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
Krkošek, M (2010) Host density thresholds and disease control for fisheries and aquaculture. Aquaculture Environment Interactions 1, 2132.CrossRefGoogle Scholar
Lester, RJG (1972) Attachment of Gyrodactylus to Gasterosteus and host response. Journal of Parasitology 58, 717722.CrossRefGoogle ScholarPubMed
Li, RR, Li, WX, Wu, XD and Wang, GT (2014) Identification of Gyrodactylus species in goldfish (Carassius auratus) through morphological study and the analysis of the rDNA ITS sequence. Acta Hydrobiologica Sinica 38, 903909.Google Scholar
McCallum, H, Barlow, N and Hone, J (2001) How should pathogen transmission be modelled? Trends in Ecology & Evolution 16, 295300.CrossRefGoogle ScholarPubMed
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, 3341.CrossRefGoogle ScholarPubMed
Poulin, R (2007) Evolutionary Ecology of Parasites, 2nd Edn. Princeton: Princeton University Press.CrossRefGoogle Scholar
R Core Team (2017) R: A Language and Environment for Statistical Computing. Vienna, Austria: R Foundation for Statistical Computing.Google Scholar
Ramsey, D, Spencer, N, Caley, P, Efford, M, Hansen, K, Lam, M and Cooper, D (2002) The effects of reducing population density on contact rates between brushtail possums: implications for transmission of bovine tuberculosis. Journal of Applied Ecology 39, 806818.CrossRefGoogle Scholar
Richards, EL, van Oosterhout, C and Cable, J (2010) Sex-specific differences in shoaling affect the rate of parasite transmission in guppies. PLoS ONE 5, e13285.CrossRefGoogle Scholar
Richards, EL, van Oosterhout, C and Cable, J (2012) Interactions between male guppies facilitates the transmission of the monogenean ectoparasite Gyrodactylus turnbulli. Experimental Parasitology 132, 483486.CrossRefGoogle ScholarPubMed
Scott, ME (1982) Reproductive potential of Gyrodactylus bullatarudis (Monogenea) on guppies (Poecilia reticulata). Parasitology 85, 217236.CrossRefGoogle Scholar
Scott, ME (1985a) Dynamics of challenge infections of Gyrodactylus bullatarudis Turnbull (Monogenea) on guppies, Poecilia reticulata (Peters). Journal of Fish Diseases 8, 495503.CrossRefGoogle Scholar
Scott, ME (1985b) Experimental epidemiology of Gyrodactylus bullatarudis (Monogenea) on guppies (Poecilia reticulata): short-and long-term studies. In Rollinson, D and Anderson, RM (eds), Ecology and Genetics of Host-Parasite Interactions. New York: Academic Press, pp. 2138.Google 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, 159194.CrossRefGoogle ScholarPubMed
Scott, ME and Nokes, DJ (1984) Temperature-dependent reproduction and survival of Gyrodactylus bullatarudis (Monogenea) on guppies (Poecilia reticulata). Parasitology 89, 221228.CrossRefGoogle Scholar
Scott, ME and Robinson, MA (1984) Challenge infections of Gyrodactylus bullatarudis (Monogenea) on guppies, Poecilia reticulata (Peters), following treatment. Journal of Fish Biology 24, 581586.CrossRefGoogle Scholar
Smith, KF, Acevedo-Whitehouse, K and Pedersen, A (2009) The role of infectious diseases in biological conservation. Animal Conservation 12, 112.CrossRefGoogle Scholar
Soleng, A, Jansen, PA and Bakke, TA (1999) Transmission of the monogenean Gyrodactylus salaris. Folia Parasitologica 46, 179184.Google Scholar
Stringer, AP and Linklater, WL (2015) Host density drives macroparasite abundance across populations of a critically endangered megaherbivore. Oecologia 179, 201207.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.CrossRefGoogle Scholar
Zhou, S (2018) Ecology of Gyrodactylus kobayashii on goldfish (Carassius auratus) and the screening of anthelmintic drugs (PhD). University of Chinese Academy of Sciences.Google Scholar
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, 12211228.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, 4045.CrossRefGoogle ScholarPubMed