Hostname: page-component-6766d58669-kn6lq Total loading time: 0 Render date: 2026-05-20T21:53:17.737Z Has data issue: false hasContentIssue false
  • English
  • Français

Temporal variation in the dispersion patterns of metazoan parasites of a coastal fish species from the Gulf of Mexico

Published online by Cambridge University Press:  09 January 2013

V.M. Vidal-Martínez ,
P. Pal ,
M.L. Aguirre-Macedo ,
A.L. May-Tec  and
J.W. Lewis
V.M. Vidal-Martínez*
Affiliation:
Laboratorio de Parasitología, Departamento de Recursos del Mar, Cinvestav-IPN Unidad Mérida, Carretera antigua a Progreso km 6, Apdo. Postal 73 – Cordemex, 97310Mérida, Yucatán, México
P. Pal
Affiliation:
School of Biological Sciences, Royal Holloway University of London, Egham, SurreyTW20 0EX, UK
M.L. Aguirre-Macedo
Affiliation:
Laboratorio de Parasitología, Departamento de Recursos del Mar, Cinvestav-IPN Unidad Mérida, Carretera antigua a Progreso km 6, Apdo. Postal 73 – Cordemex, 97310Mérida, Yucatán, México
A.L. May-Tec
Affiliation:
Laboratorio de Parasitología, Departamento de Recursos del Mar, Cinvestav-IPN Unidad Mérida, Carretera antigua a Progreso km 6, Apdo. Postal 73 – Cordemex, 97310Mérida, Yucatán, México
J.W. Lewis
Affiliation:
School of Biological Sciences, Royal Holloway University of London, Egham, SurreyTW20 0EX, UK
*
*E-mail: vvidal@mda.cinvestav.mx
Get access Rights & Permissions [Opens in a new window]

Abstract

Global climate change (GCC) is expected to affect key environmental variables such as temperature and rainfall, which in turn influence the infection dynamics of metazoan parasites in tropical aquatic hosts. Thus, our aim was to determine how temporal patterns of temperature and rainfall influence the mean abundance and aggregation of three parasite species of the fish Cichlasoma urophthalmus from Yucatán, México. We calculated mean abundance and the aggregation parameter of the negative binomial distribution k for the larval digeneans Oligogonotylus manteri and Ascocotyle (Phagicola) nana and the ectoparasite Argulus yucatanus monthly from April 2005 to December 2010. Fourier analysis of time series and cross-correlations were used to determine potential associations between mean abundance and k for the three parasite species with water temperature and rainfall. Both O. manteri and A. (Ph.) nana exhibited their highest frequency peaks in mean abundance at 6 and 12 months, respectively, while their peak in k occurred every 24 months. For A. yucatanus the frequency peaks in mean abundance and k occurred every 12 months. We suggest that the level of aggregation at 24 months of O. manteri increases the likelihood of fish mortality. Such a scenario is less likely for A. (Ph.) nana and A. yucatanus, due to their low infection levels. Our findings suggest that under the conditions of GCC it would be reasonable to expect higher levels of parasite aggregation in tropical aquatic hosts, in turn leading to a potential increase in parasite-induced host mortality.

Information

Type
Research Papers
Information
Journal of Helminthology , Volume 88 , Issue 1 , March 2014 , pp. 112 - 122
Copyright
Copyright © Cambridge University Press 2013 

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.)

Article purchase

Temporarily unavailable

References

Aguirre-Macedo, M.L., Vidal-Martínez, V.M. & Lafferty, K.D. (2011) Trematode communities in snails can indicate impact and recovery from hurricanes in a tropical coastal lagoon. International Journal for Parasitology 41, 1403–1408.Google Scholar
Anderson, R.M. (1993) Epidemiology. pp. 75–116in Cox, F.E.G. (Ed.) Modern parasitology. Oxford, Blackwell Scientific Publications.Google Scholar
Anderson, R.M. & Gordon, D.M. (1982) Processes influencing the distribution of parasite numbers within host populations with special emphasis on parasite-induced host mortalities. Parasitology 85, 373–398.Google Scholar
Bliss, C.A. & Fisher, R.A. (1953) Fitting the negative binomial to biological data and a note on the efficient fitting of the negative binomial. Biometrics 9, 176–200.Google Scholar
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.Google Scholar
Chubb, J.C. (1979) Seasonal occurrence of helminths in freshwater fish. Part II. Trematoda. Advances in Parasitology 17, 141–313.Google Scholar
Ditrich, O., Scholz, T., Aguirre-Macedo, M.L. & Vargas-Vazquez, J. (1997) Larval stages of trematodes from freshwater molluscs of the Yucatan Peninsula, Mexico. Folia Parasitologica 44, 109–127.Google Scholar
Fellis, K.J. & Esch, G.W. (2004) Community structure and seasonal dynamics of helminth parasites in Lepomis cyanellus and L. macrochirus from Charlie's Pond, North Carolina: Host size and species as determinants of community structure. Journal of Parasitology 90, 41–49.Google Scholar
Fingerut, J.T., Zimmer, C.A. & Zimmer, R.K. (2003) Larval swimming overpowers turbulent mixing and facilitates transmission of a marine parasite. Ecology 84, 2502–2515.Google Scholar
Fiorillo, R.A. & Font, W.F. (1999) Seasonal dynamics and community structure of helminths of spotted sunfish, Lepomis miniatus (Osteichthyes: Centrarchidae) from an oligohaline estuary in southeastern Louisiana, USA. Journal of the Helminthological Society of Washington 66, 101–110.Google Scholar
Gitay, H., Suárez, A.R., Watson, T. & Dokken, D.J. (2002) Climate change and biodiversity. 86 pp. Geneva, Intergovernmental Panel on Climate Change.Google Scholar
Hernández-Guevara, N.A., Pech, D. & Ardisson, P.L. (2008) Temporal trends in benthic macrofauna composition in response to seasonal variation in a tropical coastal lagoon, Celestun, Gulf of Mexico. Marine and Freshwater Research 59, 772–779.Google Scholar
Herrera-Silveira, J.A. (1994) Spatial heterogeneity and seasonal patterns in a tropical coastal lagoon. Journal of Coastal Research 10, 738–746.Google Scholar
Jiménez-García, M.I. & Vidal-Martínez, V.M. (2005) Temporal variation in the infection dynamics and maturation cycle of Oligogonotylus manteri (Digenea) in the cichlid fish, ‘Cichlasoma’ urophthalmus, from Yucatan, Mexico. Journal of Parasitology 91, 1008–1014.Google Scholar
Kennedy, C.R. (1993) The dynamics of intestinal helminth communities in eels Anguilla anguilla in a small stream – long-term changes in richness and structure. Parasitology 107, 71–78.Google Scholar
Klimpel, S., Seehagen, A. & Palm, H.W. (2003) Metazoan parasites and feeding behaviour of four small-sized fish species from the central North Sea. Parasitology Research 91, 290–297.CrossRefGoogle ScholarPubMed
Koprivnikar, J. & Poulin, R. (2009a) Effects of temperature, salinity, and water level on the emergence of marine cercariae. Parasitology Research 105, 957–965.Google Scholar
Koprivnikar, J. & Poulin, R. (2009b) Interspecific and intraspecific variation in cercariae release. Journal of Parasitology 95, 14–19.Google Scholar
Koprivnikar, J., Lim, D., Fu, C. & Brack, S.H.M. (2010) Effects of temperature, salinity, and pH on the survival and activity of marine cercariae. Parasitology Research 106, 1167–1177.Google Scholar
Lei, F. & Poulin, R. (2011) Effects of salinity on multiplication and transmission of an intertidal trematode parasite. Marine Biology 158, 995–1003.Google Scholar
Leong, T.S. (1986) Seasonal occurrence of metazoan parasites of Puntius binotatus in an irrigation canal, Pulau-Pinang, Malaysia. Journal of Fish Biology 28, 9–16.Google Scholar
Lo, C.T. & Lee, K.M. (1996) Pattern of emergence and the effects of temperature and light on the emergence and survival of heterophyid cercariae (Centrocestus formosanus and Haplorchis pumilio). Journal of Parasitology 82, 347–350.Google Scholar
Lysne, D.A., Hemmingsen, W. & Skorping, A. (1997) Regulation of infrapopulations of Cryptocotyle lingua on cod. Parasitology 114, 145–150.Google Scholar
Marcogliese, D.J. (2001) Implications of climate change for parasitism of animals in the aquatic environment. Canadian Journal of Zoology 79, 1331–1352.Google Scholar
Martínez, J. & Merino, S. (2011) Host–parasite interactions under extreme climatic conditions. Current Zoology 57, 390–405.Google Scholar
Martínez-Palacios, C.A. & Ross, L.G. (1992) The reproductive biology and growth of the Central American cichlid Cichlasoma urophthalmus (Gunther). Journal of Applied Ichthyology 8, 99–109.Google Scholar
Olden, J.D. & Neff, B.D. (2001) Cross correlation bias in lag analysis of aquatic time series. Marine Biology 138, 1063–1070.Google Scholar
Pal, P. & Lewis, J.W. (2004) Parasite aggregations in host populations using a reformulated negative binomial model. Journal of Helminthology 78, 57–61.Google Scholar
Pal, P., Abu-Madi, M.A. & Lewis, J.W. (2008) Applying an aggregative dispersive dichotomy (ADD) model to parasitic infections in host populations. Journal of Helminthology 82, 187–192.Google Scholar
Parmesan, C. (2006) Ecological and evolutionary responses to recent climate change. Annual Review of Ecology Evolution and Systematics 37, 637–669.CrossRefGoogle Scholar
Pech, D., Aguirre-Macedo, M.L., Lewis, J.W. & Vidal-Martínez, V.M. (2010) Rainfall induces time-lagged changes in the proportion of tropical aquatic hosts infected with metazoan parasites. International Journal for Parasitology 40, 937–944.Google Scholar
Platt, T. & Denman, K.L. (1975) Spectral analysis in ecology. Annual Review of Ecology and Systematics 6, 189–210.Google Scholar
Poulin, R. (2006) Global warming and temperature-mediated increases in cercarial emergence in trematode parasites. Parasitology 132, 143–151.Google Scholar
Poulin, R. & FitzGerald, G.J. (1989) Possible explanation for the aggregate distribution of Argulus canadensis Wilson, 1916 on juvenile sticklebacks (Crustacea: Branchiura) (Gasterosteidae). Journal of Parasitology 75, 58–60.Google Scholar
Poulin, R. & Mouritsen, K.N. (2006) Climate change, parasitism and the structure of intertidal ecosystems. Journal of Helminthology 80, 183–191.Google Scholar
Press, W.H., Teukolsky, S.A., Vatterling, W.T. & Flannery, B.P. (1996) Numerical recipes in Fortran 77: The art of scientific computing. 963 pp. Cambridge, Cambridge University Press.Google Scholar
Robar, N., Burness, G. & Murray, D.L. (2010) Tropics, trophics and taxonomy: the determinants of parasite-associated host mortality. Oikos 119, 1273–1280.Google Scholar
Salgado-Maldonado, G. & Kennedy, C.R. (1997) Richness and similarity of helminth communities in the tropical cichlid fish Cichlasoma urophthalmus from the Yucatan Peninsula, Mexico. Parasitology 114, 581–590.Google Scholar
Sandoval-Gio, J., Rodríguez-Canul, R. & Vidal-Martínez, V.M. (2008) Humoral antibody response of the tilapia Oreochromis niloticus against Cichlidogyrus spp. (Monogenea). Journal of Parasitology 94, 404–409.CrossRefGoogle ScholarPubMed
Scharlemann, J.P.W., Benz, D., Hay, S.I., Purse, B.V., Tatem, A.J., Wint, G.R.W. & Rogers, D.J. (2008) Global data for ecology and epidemiology: a novel algorithm for temporal Fourier processing MODIS data. PLoS ONE 3, e1408.Google Scholar
Scholz, T., Lavadores, I.P., Vargas, J., Mendoza, E.F., Rodriguez, R. & Vivas, C. (1994) Life-cycle of Oligogonotylus manteri (Digenea, Cryptogonimidae), a parasite of cichlid fishes in Southern Mexico. Journal of the Helminthological Society of Washington 61, 190–199.Google Scholar
Scholz, T., Vargas-Vázquez, J., Aguirre-Macedo, M.L. & Vidal-Martínez, V.M. (1997) Species of Ascocotyle Looss, 1899 (Digenea: Heterophyidae) of the Yucatan Peninsula, Mexico, and notes on their life-cycles. Systematic Parasitology 36, 161–181.Google Scholar
Simá-Álvarez, A., Aguirre, M.L., Scholz, T. & Güemez, R.J. (1994) Histopathology of the intestine of Cichlasoma urophthalmus (Gunther) infected with metacercariae of Oligogonotylus manteri Watson, 1976 (Digenea, Cryptogonimidae). Journal of Fish Diseases 17, 523–526.Google Scholar
Simková, A., Jarkovský, J., Koubková, B., Barus, V. & Prokes, M. (2005) Associations between fish reproductive cycle and the dynamics of metazoan parasite infection. Parasitology Research 95, 65–72.Google Scholar
Stanko, M., Krasnov, B.R. & Morand, S. (2006) Relationship between host abundance and parasite distribution: inferring regulating mechanisms from census data. Journal of Animal Ecology 75, 575–583.Google Scholar
Steinauer, M.L. & Font, W.F. (2003) Seasonal dynamics of the helminths of bluegill (Lepomis macrochirus) in a subtropical region. Journal of Parasitology 89, 324–328.Google Scholar
Studer, A. & Poulin, R. (2012) Effects of salinity on an intertidal host–parasite system: Is the parasite more sensitive than its host? Journal of Experimental Marine Biology and Ecology 412, 110–116.Google Scholar
Thiel, M., Romano, M.C., Schwarz, U., Kurths, J. & Timmer, J. (2004) Surrogate-based hypothesis test without surrogates. International Journal of Bifurcation and Chaos 14, 2107–2114.Google Scholar
Vidal-Martínez, V. & Poulin, R. (2003) Spatial and temporal repeatability in parasite community structure of tropical fish hosts. Parasitology 127, 387–398.Google Scholar
Vidal-Martínez, V.M., Aguirre-Macedo, M.L., Scholz, T., González-Solís, D. & Mendoza-Franco, E. (2001) Atlas of the helminth parasites of cichlid fishes of Mexico. 164 pp. Prague, Academia.Google Scholar
Vincent, A.G. & Font, W.F. (2003) Seasonal and yearly population dynamics of two exotic helminths, Camallanus cotti (Nematoda) and Bothriocephalus acheilognathi (Cestoda), parasitizing exotic fishes in Waianu Stream, O'ahu, Hawaii. Journal of Parasitology 89, 756–760.CrossRefGoogle ScholarPubMed
Violante-González, J., Aguirre-Macedo, M.L. & Vidal-Martínez, V.M. (2008) Temporal variation in the helminth parasite communities of the Pacific fat sleeper, Dormitator latifrons, from Tres Palos Lagoon, Guerrero, Mexico. Journal of Parasitology 94, 326–334.Google Scholar
Voutilainen, A., Huuskonen, H. & Taskinen, J. (2010) Penetration and migration success of Diplostomum spp. cercariae in arctic charr. Journal of Parasitology 96, 232–235.Google Scholar
Webb, A.C. (2008) Spatial and temporal influences on population dynamics of a branchiuran ectoparasite, Argulus sp. A, in fresh waters of tropical northern Queensland, Australia. Crustaceana 81, 1055–1067.Google Scholar
Wei, W.W.S. (1990) Time series analysis: Univariate and multivariate methods. 478 pp. New York, Adisson–Wesley.Google Scholar
Zander, C.D. (2003) Four-year monitoring of parasite communities in gobiid fishes of the south-western Baltic-I. Guild and component community. Parasitology Research 90, 502–511.Google Scholar
Zander, C.D. (2004) Four-year monitoring of parasite communities in gobiid fishes of the south-western Baltic-II. Infracommunity. Parasitology Research 93, 543–555.Google Scholar
Zander, C.D. (2005) Four-year monitoring of parasite communities in gobiid fishes of the southwest Baltic-III. Parasite species diversity and applicability of monitoring. Parasitology Research 95, 136–144.Google Scholar