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Temporal variation of Mexiconema cichlasomae (Nematoda: Daniconematidae) in the Mayan cichlid fish Cichlasoma urophthalmus and its intermediate host Argulus yucatanus from a tropical coastal lagoon

  • A. L. MAY-TEC (a1), D. PECH (a2), M. L. AGUIRRE-MACEDO (a1), J. W. LEWIS (a3) and V. M. VIDAL-MARTÍNEZ (a1)...

The aim of the present investigation was to determine whether temporal variation in environmental factors such as rainfall or temperature influence long-term fluctuations in the prevalence and mean abundance of the nematode Mexiconema cichlasomae in the cichlid fish Cichlasoma uropthalmus and its crustacean intermediate host, Argulus yucatanus. The study was undertaken in a tropical coastal lagoon in the Yucatan Peninsula (south-eastern Mexico) over an 8-year period. Variations in temperature, rainfall and monthly infection levels for both hosts were analysed using time series and cross-correlations to detect possible recurrent patterns. Infections of M. cichlasomae in A. yucatanus showed annual peaks, while in C. urophthalmus peaks were bi-annual. The latter appear to be related to the accumulation of several generations of this nematode in C. urophthalmus. Rainfall and temperature appear to be key environmental factors in influencing temporal variation in the infection of M. cichlasomae over periods longer than a year together with the accumulation of larval stages throughout time.

Corresponding author
*Corresponding author: Laboratorio de Parasitología, Departamento de Recursos del Mar, Cinvestav, Carretera antigua a Progreso km 6, Apdo. Postal 73 – Cordemex, 97310 Mérida, Yucatán, Mexico. Tel.: +52 999 942 9400. Fax: +52 999 981 23 34. E-mail:
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Abell, S., Gadeka, P., Pearceb, C. and Congdon, B. (2006). Seasonal resource availability and use by an endangered tropical mycophagous marsupial. Biological Conservation 132, 533540.
Aguirre-Macedo, M. L., Vidal-Martínez, V. M. and 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, 14031408.
Avenant-Oldewage, A., Swanepoel, J. H. and Knight, E. (1994). Histomorphology of the digestive tract of Chonopeltis australis (Crustacea: Branchiura). The South African Journal of Zoology 29, 7481.
Benedetti-Cecchi, L., Acunto, S., Bulleri, F. and Cinelli, F. (2000). Population ecology of the barnacle Chtliamalus stellatus in the northwest Mediterranean. Marine Ecological Progress Series 198, 157170.
Bush, A. O., Lafferty, K. D., Lotz, J. M. and Shostak, A. W. (1997). Parasitology meets ecology on this own terms: Margolis et., al. revisited. Journal of Parasitology 83, 575583.
Caspeta-Mandujano, J. M. and Mejía-Mojica, H. (2004). Seasonal dynamics of the ocurrence and maduration of Rhabdochona Canadensis in its definitive host, Notropics boucardi of the Chalma River, State of Morelos, México. Helminthologia 41, 121123.
Coley, P. D. and Aide, T.M. (1991). Comparisons of herbivory and plant defenses in temperate and tropical broad-leaved forest. In Plant-Animal Interactions: Evolutionary Ecology in Tropical and Temperate Regions (ed. Price, P. W., Lewinshom, T. M., Fernades, G. W. and Benson, W. W.), pp. 2549. Wiley and Sons, New York, USA.
Colón-González, F., Lake, I. and Bentham, G. (2011). Climate variability and dengue fever in warm and humid Mexico. The American Journal of Tropical Medicine and Hygiene 84, 757763.
Des Clers, S. (1994). Sampling to Detect Infections and Estimate Prevalence in Aquaculture. Pisces Press, Stirling, Scotland.
Easterling, D. R., Evans, P., Groisman, T. R., Kunkel, K. E. and Ambenje, P. (2000). Observed variability and trends in extreme climate events: A brief review. American Meteorological Society 81, 417425.
Faunce, C. H., Patterson, H. M. and Lorenz, J. J. (2002). Age, growth, and mortality of the Mayan cichlid (Cichlasoma urophthalmus) from the southeastern Everglades. Fishery Bulletin 100, 4250.
Fiorillo, R. A. and 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, U.S.A. Journal of the Helminthological Society of Washington 66, 101110.
Ghil, M. (2002). Natural climate variability. In Encyclopedia of Global Environmental Change (ed. MacCracken, M. C. and Perry, J. S.), pp. 544549. John Wiley & Sons, Ltd, Chichester, UK.
Githeko, A. K., Lindsay, S. W., Confalonieri, U. E. and Patz, J. A. (2000). Climate change and vector-borne diseases: a regional analysis. Bulletin of the World Health Organization, N. 78 (9).
Greenfield, D. W. and Thomerson, J. E. (1997). Fishes of the Continental Waters of Belize. University of Florida Press, Gainsville, FL, USA.
Hay, S. I., Myers, M. F., Burke, D. S., Vaughn, D. W., Endy, T., Ananda, N., Shanks, G. D., Snow, R. W. and Rogers, D. J. (2000). Etiology of interepidemic periods of mosquito-bornedisease. Proceedings of the National Academy of Sciences, USA 97, 93359339.
Herrera-Silveira, J. A., Martín, M. B. and Díaz-Arce, V. (1999). Variaciones del fitoplanton en cuatro lagunas costeras del estado de Yucatán, México. Revista de Biología Tropical 47, 4756.
Hernández-Guevara, N. A., Pech, D. and 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, 772779.
Hubálek, Z. (2005). North Atlantic weather oscillation and human infectious diseases in the Czech Republic, 1951–2003. European Journal of Epidemiology 20, 263270. doi 10.1007/s10654-004-6518-3.
Hubálek, Z., Halouzka, J. and Juricová, Z. (2003). Longitudinal surveillance of the tick Ixodes ricinius for borreliae. Medical and Veterinary Entomology 17, 4651.
Jiménez-García, M. I. and 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 Yucatán, México. Journal of Parasitology 91, 10081014.
Kennedy, C. R. (1993). The dynamics of helminth communities in eels Anguilla anguilla in a small stream: long term changes in richness and structure. Parasitology 107, 7178.
Kerans, B. L., Stevens, R. I. and Lemmon, J. C. (2005). Water temperature affects a host–parasite interaction: Tubifex tubifex and Myxobolus cerebralis. Journal of Aquatic Animal Health 17, 216221.
Knipes, A. K. and Janovy, J. Jr. (2009). Community structure and seasonal dynamics of Dactylogyrus SPP. (Monogenea) on the fathead minnow (Pimephales promelas) from the Salt Valley Watershed, Lancaster County, Nebraska. Journal of Parasitology 95, 12951305.
Krasnov, B. R., Korallo-Vinarskaya, N. P., Vinarski, M. V., Shenbrot, G. I., Moullot, D. and Poulin, R. (2008). Searching for general patterns in parasite ecology: host identity versus environmental influence on gamasid mite assemblages in small mammals. Parasitology 135, 229242. doi:10.1017/S003118200700368X.
Lafferty, K. (2009). The ecology of climate change and infectious diseases. Ecology 90, 888900.
Leong, T. S. (1986). Seasonal occurrence of metazoan parasites of Puntius binotaus in an irrigation canal, Pulau Pinang, Malaysia. Journal of Fish Biology 28, 916.
Legendre, P. and Legendre, L. (1998). Numerical Ecology. 2nd English Edn. Elsevier Science BV, Amsterdam, The Netherlands.
Luque, J. L. and Poulin, R. (2008). Linking ecology with parasite diversity in Neotropical fishes. Journal of Fish Biology 72, 189204. doi: 10.1111/j.1095-8649.2007.01695.x.
Mas-Coma, S., Valero, M. A. and Bargues, M. D. (2009). Climate change effects on trematodiases, with emphasis on zoonotic fascioliasis and schistosomiasis. Veterinary Parasitology 163, 264280. doi: 10.1016/j.vetpar.2009.03.024.
Marcogliese, D. J. (2008). The impact of climate change on the parasites and infectious diseases of aquatic animals. Scientific and Technical Review of the Office International des Epizooties 27, 467484.
Martin, L. B., Pless, M., Svoboda, J. and Wikelski, M. (2004). Immune activity in temperate and tropical house sparrows: A common-garden experiment. Ecology 85, 23232331.
Martinez, J. and Merino, S. (2011). Host-parasite interactions under extreme climatic conditions. Current Zoology 57, 390405.
Martínez-Palacios, C. A. (1987). Aspects of the biology of Cichlasoma urophthalmus (Günther) with particular reference to its culture in Celestún Lagoon, Yucatan, Mexico. Ph.D. Thesis, University of Stirling, Stirling, UK.
Martínez-Palacios, C. A. and Ross, L. G. (1988). The feeding ecology of the Central American cichlid Cichlasoma urophthalmus (Gunther). Journal of Fish Biology 33, 665670.
Martinez-Palacios, C. A. and Ross, L. G. (1992). The reproductive biology and growth of the Central American cichlid Cichlasoma urophthalmus Günther. Journal Applied Ichthyology 8, 99109.
May-Tec, A. L. (2007). Aspectos biológicos del ciclo de vida de Mexiconema cichlasomae (Nematoda: Daniconematidae) en Cichlasoma urophthalmus y en su hospedero intermediario Argulus sp. en Celestún, Yucatán. Tesis Licenciatura en Biología. Instituto Tecnológico Agropecuario N° 2.
Mejia-Madrid, H. H. and Aguirre-Macedo, M. L. (2011). Systematics of Mexiconema cichlasomae (Nematoda: Daniconematidae) Based on Sequences of SSU rDN. Journal of Parasitology 97, 160162. doi: 10.1645/GE-2569.1.
Miller, R. R., Winckley, W. L. and Norris, M. S. (2005). Freshwater Fishes of Mexico. The University of Chigago Press, Chicago, ILL, USA.
Molnár, K. and Székely, C. (1998). Ocurrence of Skrajabillanid nematodes in fishes of Hungary and in the intermediate host. Argulus foliaceus L. Acta Veterinaria Hungarica 46, 451463.
Moravec, F. (1994). Parasitic nematodes of freshwater fishes of Europe. Academia and Kluwer Academy Publishers, Praha, Czech Republic.
Moravec, F. (2004). Some aspects of the taxonomy and biology of dracunculoid nematodes parasitic in fishes: A review. Folia Parasitologica 51, 113.
Moravec, F. (2006). Dracunculoid and anguillicoloid nematodes parasitic in vertebrates. Academia, Praha, Czech Republic.
Moravec, F. (2007). Some aspects of the taxonomy and biology of adult spirurine nematodes parasitic in fishes: A review. Folia Parasitologica 54, 239257.
Moravec, F., Magi, M. and Macchioni, F. (2008). Redescription of the gonadinfecting nematode Philometra saltatrix Ramachandran, 1973 (Philometridae) based on specimens from the type host Pomatomus saltatrix (L.) (Osteichthyes) from the Tuscan Sea, Italy. Folia Parasitologica 55, 219223.
Moravec, F. and Salgado-Maldonado, G. (2007). A new species of Philometra (Nematoda, Philometridae) from the gonads of the rock hind Epinephelus adscensionis (Osteichthyes) from the southern Gulf of Mexico. Acta Parasitologica 52, 376381. doi: 10.2478/s11686-007-0044-x.
Moravec, F., Vidal-Martinez, V. M. and Aguirre-Macedo, M. L. (1999). Branchiurids (Argulus) as intermediate host of the Daniconematid nematode Mexiconema cichlasomae. Folia Parasitologica 46, 79.
Moravec, F., Vidal-Martínez, V. M. and Salgado-Maldonado, G. (1992). Mexiconema cichlasomae gen, et sp. (Nematoda: Daniconematidae) from Cichlasoma spp. (Pices) from México. Folia Parasitologica 39, 3340.
Olden, J. D. and Neff, B. D. (2001). Cross-correlation bias in lag analysis of aquatic time series. Marine Biology 138, 10631070.
Oliva, M. E., Barrios, I., Thatje, S. and Laudien, J. (2007). Changes in prevalence and intensity of infection of Profilicollis altmani (Perry, 1942) cystacanth (Acanthocephala) parasitizing the mole crab Emerita analoga (Stimpson, 1857): an El Niño cascade effect?. Helgoland Marine Research. doi: 10.1007/s10152-007-0082-7.
Parmesan, C. and Galbraith, H. (2004). Observed Ecological Impacts of Climate Change in North America. Pew Center on Global Climate Change, Arlington, VA, USA.
Patz, J. A., Campbell-Lendrum, D., Holloway, T. and Foley, J. A. (2005). Impact of regional climate change on human health. Nature, London 438, 310317. doi:10.1038/nature04188.
Platt, D. and Denman, K. L. (1975). Spectral analysis in ecology. Annual Review of Ecology and Systematics 6, 189210.
Pech, D., Ardisson, P. L. and Hernández-Guevara, N. A. (2007). Benthic community response to habitat variation: A case of study from a natural protected area, the Celestun coastal. Continental Shelf Research 27, 25232533. doi:10.1016/j.csr.2007.06.017.
Pech, D., Aguirre-Macedo, M. L., Lewis, J. W. and 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, 937944. doi:10.1016/j.ijpara.2010.01.009.
Poulin, R. (2000). Variation in the intraspecific relationship between fish length and intensity of parasitic infection: biological and statistical causes. Journal of Fish Biology 56, 123137.
Poulin, R. and Mouritsen, K. N. (2006). Climate change, parasitism and the structure of intertidal ecosystems. Journal of Helminthology 80, 183191. doi: 10.1079/JOH2006341.
Press, W. H., Teukolsky, S. A., Vatterling, W. T. and Flannery, B. P. (1996). Numerical Recipes in Fortran 77: The Art of Scientific Computing. Cambridge University Press, Cambridge, UK.
Salgado-Maldonado, G. (1993). Ecología de Helmintos parásitos de Cichlasoma uropthalmus (Günther) (Pises: Cichlidae) en la península de Yucatán, México. Tesis de doctorado. Centro de investigación y de Estudios avanzados del Instituto Politécnico Nacional, México.
Salgado-Maldonado, G. and Kennedy, C. R. (1997). Richness and similarity of helminth communities in the tropical cichlid fish Cichlasoma urophthalmus from the Yucatan Peninsula, Mexico. Parasitology 107, 7178.
Scharlemann, J. P. W., Benz, D., Hay, S. I., Purse, B. V., Tatem, A. J., Wint, G. R. W., and Rogers, D. J. (2008). Global data for ecology and epidemiology: a novel algorithm for temporal fourier processing MODIS data. PLos One 3, e1408. 1, 13711408. doi: 10.1371/journal.pone.0001408.
Simková, A. (2005). Associations between fish reproductive cycle and the dynamics of metazoan parasite infection. Journal of Parasitology Research 95, 6572. doi: 10.1007/s00436-004-1261-y.
Smith, J. L., Wootten, R. and Sommerville, C. (2007). The pathology of the early stages of the crustacean parasite, Lernaeocera branchialis (L.), on Atlantic cod, Gadus morhua L. Journal of Fish Diseases 30, 111.
Soniat, M. T., Hofmann, E. E., Klinck, M. J. and Powell, N. E. (2009). Differential modulation of eastern oyster (Crassostrea virginica) disease parasites by the El-Niño-Southern Oscillation and the North Atlantic Oscillation. International Journal of Earth Sciences 98, 99114. doi: 10.1007/s00531-008-0364-6.
Steinauer, M. and Font, W. (2003). Seasonal dynamics of the helminthes of bluegill (Lepomis macrochirus) in a subtropical region. Journal of Parasitology 89, 324328.
Stenseth, N., Ottersen, G., Hurrell, J., Mysterud, A., Lima, M., Chan, K., Yoccoz, N. and Ådlandsvik, B. (2003). Review article. Studying climate effects on ecology through the use of climate indices: the North Atlantic Oscillation, El Niño Southern Oscillation and beyond. Proceedings The Royal of Society of London, B 270, 20872096. doi: 10.1098/rspb.2003.2415.
Trexler, J. C., Loftus, W. F., Jordan, F., Lorenz, J. J., Chick, J. H. and Kobza, R. M. (2000). Empirical assessment of fish introductions in a subtropical wetland: an evaluation of constrasting views. Biological Invasions 2, 265277.
Thiel, M., Romano, M. C., Schwarz, U., Kurths, J. and Timmer, J. (2004). Surrogate- based hypothesis test without surrogates. International Journal of Bifurcation and Chaos 14, 2107.
Tikhomirova, V. A. (1980). On nematodes of the family Skrjabillanidae (Nematoda: Camallanata:). Parazitologya 14, 258262.
Ujvari, B., Andersson, S., Brown, G., Shine, R. and Madsen, T. (2010). Climate-driven impacts of prey abundance on the population structure of a tropical aquatic predator. Oikos 119, 188196. doi: 10.1111/j.1600-0706.2009.17795.x.
Vidal-Martínez, V. M., Scholz, T., Aguirre-Macedo, M. L., Gonzalez-Solis, D. and Mendoza-Franco, E. F. (2001). Atlas of the Helminth Parasites of Cichlid Fishes of México. Academia, Prague, Czech Republic.
Vincent, A. and Font, W. (2003). Host specificity and population structure of two exotic helminths, Camallanus cotti (nematoda) and Bothriocephalus acheilognathi (cestoda), parasitizing exotic fishes in Waianu Stream, O'Ahu, Hawaii. Journal of Parasitology 89, 540544.
Violante-González, J., Aguirre-Macedo, M. L. and Vidal-Martínez, V. M. (2008). Temporal variation in the helminth parasite comunities of the pacific fat sleeper, Dormitator latifrons, from Tres Palos Lagoon, Guerrero, Mexico. Journal of Parasitology 94, 326334.
Walker, P. D., Flik, G. and Wendelaar Bonga, S. J. (2004). The biology of parasites from the genus Argulus and a review of the interactions with its host. In Host-Parasite Interactions. (ed. Wiegertjes, G. F. and Flik, G.), pp 107129. Garland Science/BOIS Scientific Publishers. Hampshire, UK.
Wei, W. W. S. (1990). Time Series Analysis: Univariate and Multivariate Methods. Adisson–Wesley, New York, USA.
Yildiz, K. and Kumantas, A. (2002). Argulus foliaceus infection in a goldfish (Carassius auratus). Israel Journal of Veterinary Medicine 57, 118120.
Zander, C. D. (2003). Four-year monitoring of parasite communities in gobiid fishes of the southwestern Baltic. I. Guild and component community. Journal of Parasitology Research 90, 502511.
Zander, C. D. (2004). Four-year monitoring of parasite communities in gobiid fishes of the southwestern Baltic. II. Infracommunity. Journal of Parasitology Research 93, 1729.
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. Journal of Parasitology Research 95, 136144.
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