Hostname: page-component-848d4c4894-x24gv Total loading time: 0 Render date: 2024-06-13T03:17:16.542Z Has data issue: false hasContentIssue false
  • English
  • Français

Following the infection dynamics of the tropical trematode Oligogonotylus mayae in its intermediate and definitive hosts for 13 years

Published online by Cambridge University Press:  03 November 2020

A.L. May-Tec ,
N.A. Herrera-Castillo ,
V.M. Vidal-Martínez Open the ORCID record for V.M. Vidal-Martínez [Opens in a new window]  and
M.L. Aguirre-Macedo Open the ORCID record for M.L. Aguirre-Macedo [Opens in a new window]
A.L. May-Tec
Affiliation:
Laboratorio de Patología Acuática, Departamento de Recursos del Mar, Centro de Investigación y de Estudios Avanzados del Instituto Politécnico Nacional, Unidad Mérida, Carretera Antigua a Progreso Km 6, Mérida, Yucatán, CP97310, Mexico
N.A. Herrera-Castillo
Affiliation:
Laboratorio de Patología Acuática, Departamento de Recursos del Mar, Centro de Investigación y de Estudios Avanzados del Instituto Politécnico Nacional, Unidad Mérida, Carretera Antigua a Progreso Km 6, Mérida, Yucatán, CP97310, Mexico
V.M. Vidal-Martínez
Affiliation:
Laboratorio de Patología Acuática, Departamento de Recursos del Mar, Centro de Investigación y de Estudios Avanzados del Instituto Politécnico Nacional, Unidad Mérida, Carretera Antigua a Progreso Km 6, Mérida, Yucatán, CP97310, Mexico
M.L. Aguirre-Macedo*
Affiliation:
Laboratorio de Patología Acuática, Departamento de Recursos del Mar, Centro de Investigación y de Estudios Avanzados del Instituto Politécnico Nacional, Unidad Mérida, Carretera Antigua a Progreso Km 6, Mérida, Yucatán, CP97310, Mexico
*
Author for correspondence: M.L. Aguirre-Macedo, E-mail: leopoldina.aguirre@cinvestav.mx
Get access Rights & Permissions [Opens in a new window]

Abstract

We present a time series of 13 years (2003–2016) of continuous monthly data on the prevalence and mean abundance of the trematode Oligogonotylus mayae for all the hosts involved in its life cycle. We aimed to determine whether annual (or longer than annual) environmental fluctuations affect these infection parameters of O. mayae in its intermediate snail host Pyrgophorus coronatus, and its second and definitive fish host Mayaheros urophthalmus from the Celestun tropical coastal lagoon, Yucatan, Mexico. Fourier time series analysis was used to identify infection peaks over time, and cross-correlation among environmental forcings and infection parameters. Our results suggest that the transmission of O. mayae in all its hosts was influenced by the annual patterns of temperature, salinity and rainfall. However, there was a biannual accumulation of metacercarial stages of O. mayae in M. urophthalmus, apparently associated with the temporal range of the El Niño-Southern Oscillation (five years) and the recovery of the trematode population after a devasting hurricane. Taking O. mayae as an example of what could be happening to other trematodes, it is becoming clear that environmental forcings acting at long-term temporal scales affect the population dynamics of these parasites.

Keywords

Temporal variationtrematodesseasonalitylong-term studiesdynamic of infection
Type
Research Paper
Information
Journal of Helminthology , Volume 94 , 2020 , e208
Copyright
Copyright © The Author(s), 2020. 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

Aguirre-Macedo, ML, Vidal-Martínez, VM and Lafferty, KD (2011) Trematode communities in snails can indicate impact and recovery from hurricanes in a tropical coastal lagoon. International Journal for Parasitology 41, 1403–1408.CrossRefGoogle Scholar
Bullard, SA and Overstreet, RM (2008) Digeneans as enemies of fishes. pp. 817–976 in Eiras, JC, Segnar, H, Wahli, T and Kapoor, BG (Eds) Fish diseases. Enfield, Science Publishers.Google Scholar
Bush, AO, Lafferty, KD, Lotz, JM and Shostak, AW (1997) Parasitology meets ecology on its own terms: Margolis et al. revisited. Journal of Parasitology 83, 575–583.CrossRefGoogle Scholar
Byers, JE, Holmes, ZC and Blakeslee, AMH (2016) Consistency of trematode infection prevalence in host populations across large spatial and temporal scales. Ecology 7, 1643–1649.CrossRefGoogle Scholar
Chatfield, C (1980) The analysis of time-series: an introduction. London, Chapman & Hall.CrossRefGoogle Scholar
Chubb, JC (1979) Seasonal occurrence of helminths in freshwater fishes. Part II. Trematoda. Advances in Parasitology 17, 142–313.Google Scholar
des Clers, S (1994) Sampling to detect infections and estimate prevalence in aquaculture. Stirling, Scotland, Pisces Press.Google Scholar
Ditrich, O, Scholz, T, Aguirre-Macedo, L and Vargas-Vazquez, J (1997) Larval stages of trematodes from freshwater mollusks of the Yucatán Peninsula, Mexico. Folia Parasitologica 44, 109–127.Google Scholar
Drake, P and Arias, AM (1995) Distribution and production of Chirononomus salinarius (Diptera: Chironomidae) in a shallow coastal lagoon in the Bay of Cádiz. Hydrobiologia 299, 195–206.CrossRefGoogle Scholar
Faltynková, A, Valtonen, ET and Karvonen, A (2008) Spatial and temporal structure of the trematode component community in Valvata macrostoma (Gastropoda, Prosobranchia). Parasitology 135, 1691–1699.CrossRefGoogle Scholar
Fermer, J, Culloty, SC, Kelly, TC and O'Riordan, RM (2010) Temporal variation of Meiogymnophallus minutus infections in the first and second intermediate host. Journal of Helminthology 84, 362–368.CrossRefGoogle ScholarPubMed
Fernandez, J and Esch, GW (1991a) The component community structure of larval trematodes in the pulmonate snail Helisoma anceps. Journal of Parasitology 77, 540–550.CrossRefGoogle Scholar
Fernandez, J and Esch, GW (1991b) Guild structure of the larval trematodes in the snail Helisoma anceps: patterns and processes at the individual host level. Journal of Parasitology 77, 528–539.CrossRefGoogle Scholar
Fingerut, JT, Zimmer, CA and Zimmer, RK (2003) Patterns and processes of larval emergence in an estuarine parasite system. Marine Biological Laboratory 205, 110–120.CrossRefGoogle Scholar
Galaktionov, KV (1992) Seasonal dynamics of age composition in component populations of daughter sporocyst of microphallids of the ‘‘pygmaeus’’ group (Trematoda, Microphallidae) in the intertidal molluscs Littorina saxatilis in the Barents Sea. Parazitologiya 26, 462–469.Google Scholar
Galaktionov, KV, Irwin, SWB, Prokofiev, VV, Saville, DH, Nikolaev, KE and Levakin, IA (2006) Trematode transmission in coastal communities—temperature dependence and climate change perspectives. pp. 85–90 in 11th International Congress of Parasitology (ICOPA XI), Glasgow (Scotland, United Kingdom), August 6–11, 2006. Medimond International Proceedings.Google Scholar
Galaktionov, KV, Nikolaev, KE, Aristov, DA, Levakin, IA and Kozminsky, EV (2018) Parasites on the edge: patterns of trematode transmission in the Arctic intertidal at the Pechora Sea (South-Eastern Barents Sea). Polar Biology 49, 1719–1737.Google Scholar
Gérard, C, Carpentier, A and Paillisson, JM (2008) Long-term dynamics and community structure of freshwater gastropods exposed to parasitism and other environmental stressors. Freshwater Biological Association 53, 470–484.CrossRefGoogle Scholar
Gordon, DM and Rau, ME (1982) Possible evidence for mortality induced by the parasite Apatemon gracilis in a population of brook sticklebacks (Culaea inconstans). Parasitology 84, 41–47.CrossRefGoogle Scholar
Granovitch, AI, Sergievsky, SO and Sokolova, IM (2000) Spatial and temporal variation of trematode infestation in coexisting populations of intertidal gastropods Littorina saxatilis and L. obtusata in the White Sea. Diseases of Aquatic Organisms 41, 53–64.CrossRefGoogle Scholar
Greer, JG and Corkum, KC (1979) Life cycle studies of three digenetic trematodes, including descriptions of two new species (Digenea:Cryptogonimidae). Proceedings of the Helminthological Society of Washington 46, 188–200.Google Scholar
Herrera-Silveira, JA (1994) Spatial heterogeneity and seasonal patterns in a tropical coastal lagoon. Journal of Coastal Research 10, 738–746.Google Scholar
Herrera-Silveira, JA and Morales-Ojeda, SM (2009) Evaluation of the health status of a coastal ecosystem in southeast Mexico: assessment of water quality, phytoplankton and submerged aquatic vegetation. Marine Pollution Bulletin 59, 72–86.CrossRefGoogle ScholarPubMed
Hofmann, H, Blasco-Costa, I, Knudsen, R, Matthaei, CD, Valois, A and Lange, K (2016) Parasite prevalence in an intermediate snail host is subject to multiple anthropogenic stressors in a New Zealand river system. Ecological Indicators 60, 845–852.CrossRefGoogle Scholar
Hughes, RN and Answer, P (1982) Growth, spawning and trematode infection of Littorina littorea (L.) from an exposed shore in North Wales. Journal of Molluscan Studies 48, 321–330.CrossRefGoogle Scholar
Jiménez-García, MI and Vidal-Martínez, VM (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, 1008–1014.CrossRefGoogle ScholarPubMed
Klockars, J, Huffman, J and Fried, B (2007) Survey of seasonal trematode infections in Helisoma trivolvis (Gastropoda) from lentic ecosystems in New Jersey, U.S.A. Comparative Parasitology 74, 75–80.CrossRefGoogle Scholar
Koprivnikar, J and Poulin, R (2009) Interspecific and intraspecific variation in cercariae release. Journal of Parasitology 95, 14–19.CrossRefGoogle ScholarPubMed
Koprivnikar, J, Ellis, D, Shim, KC and Forbes, MR (2014) Effects of temperature and salinity on emergence of Gynaecotyla adunca cercariae from the intertidal gastropod Ilyanassa obsoleta. Journal of Parasitology 100, 242–245.CrossRefGoogle ScholarPubMed
Kube, S, Kube, J and Bick, A (2002) Component community of larval trematodes in the mudsnail Hydrobia ventrosa: temporal variation in prevalence in relation to host life history. Journal of Parasitology 88, 730–737.CrossRefGoogle Scholar
Kuris, AM, Hechinger, RF, Shaw, JC, et al. (2008) Ecosystem energetic implications of parasite and free-living biomass in three estuaries. Nature 454, 515–518.CrossRefGoogle ScholarPubMed
Lafferty, KD, Dobson, AP and Kuris, AM (2006) Parasites dominate food web links. Proceedings of the National Academy of Sciences of the United States of America 103, 11211–11216.CrossRefGoogle ScholarPubMed
Legendre, P and Legendre, L (1998) Numerical ecology. 2nd edn. Amsterdam, the Netherlands, Elsevier Science BV.Google Scholar
Levakin, IA, Nikolaev, KE and Galaktionov, KV (2013) Long-term variation in trematode (Trematoda, Digenea) component communities associated with intertidal gastropods is linked to abundance of final hosts. Hydrobiologia 706, 103–118.CrossRefGoogle Scholar
Loy, C and Haas, W (2001) Prevalence of cercariae from Lymnaea stagnalis snails in a pond system in Southern Germany. Journal of Parasitology Research 87, 878–882.Google Scholar
Martínez-Palacios, CA and Ross, LG (1988) The feeding ecology of the Central American cichlid Cichlasoma urophthalmus (Gunther). Journal of Fish Biology 33, 665–670.CrossRefGoogle Scholar
May-Tec, AL, Pech, D, Aguirre-Macedo, ML and Vidal-Martínez, VM (2013) 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. Parasitology 140, 385–395.CrossRefGoogle ScholarPubMed
McCreesh, N, Arinaitwe, M, Arineitwe, W, Tukahebwa, E M and Booth, M (2014) Effect of water temperature and population density on the population dynamics of Schistosoma mansoni intermediate host snails. Parasites & Vectors 7, 503.CrossRefGoogle ScholarPubMed
Mehlhorn, H (2016) Digenea. pp. 689–708 in Mehlhorn, H (Ed.) Encyclopedia of parasitology. Berlin, Heidelberg, Springer.Google Scholar
Mladenka, GC and Minshall, GW (2001) Variation in the life history and abundance of three populations of Bruneau hot springsnails (Pyrgulopsis bruneauensis). Western North American Naturalist 61, 204–212.Google Scholar
Morley, NJ (2012) Cercariae (Platyhelminthes: Trematoda) as neglected components of zooplankton communities in freshwater habitats. Hydrobiologia 691, 7–19.CrossRefGoogle Scholar
Mouritsen, KN, Jensen, T and Jensen, KT (1997) Parasites on an intertidal Corophium-bed: factors determining the phenology of microphallid trematodes in the intermediate host populations of the mud-snail Hydrobia ulvae and the amphipod Corophium volutator. Hydrobiologia 355, 61–70.CrossRefGoogle Scholar
Namsanor, J, Sithithaworn, P, Kopolrat, K, Kiatsopit, N, Pitaksakulrat, O, Tesana, S, Andrews, RH and Petney, TN (2015) Seasonal transmission of Opisthorchis viverrini sensu lato and a Lecithodendriid trematode species in Bithynia siamensis goniomphalos snails in northeast Thailand. American Journal of Tropical Medicine and Hygiene 93, 87–93.CrossRefGoogle Scholar
Nikolaev, KE, Levakin, IA and Galaktionov, KV (2020) Seasonal dynamics of trematode infection in the first and the second intermediate hosts: a long-term study at the subarctic marine intertidal. Journal of Sea Research 164, 101931.CrossRefGoogle Scholar
NOAA (2005) National Oceanic Data Center: coastal water temperature guide. Available at http://www.cpc.noaa.gov/index.php (accessed 4 February 2018).Google Scholar
Olden, JD and Neff, BD (2001) Cross-correlation bias in lag analysis of aquatic time series. Marine Biology 138, 1063–1070.CrossRefGoogle Scholar
Orduña-Rojas, J, Robledo, D and Dawes, CJ (2002) Studies on the tropical agarophyte Gracilaria cornea J. Agardh (Rhodophyta, Gracilariales) from Yucatan, Mexico. I. Seasonal physiological and biochemical responses. Botanica Marina 45, 453–458.Google Scholar
Pech, D, Aguirre-Macedo, ML, Lewis, JW and Vidal-Martínez, VM (2011) Rainfall induces time-lagged changes in the proportion of tropical aquatic hosts infected with metazoan parasites. International Journal for Parasitology 40, 937–944.CrossRefGoogle Scholar
Poulin, R and Valtonen, ET (2001) Interspecific association among larval helminths in fish. International Journal for Parasitology 31, 1589–1596.CrossRefGoogle Scholar
Pulkkinen, K and Valtonen, ET (1999) Accumulation of plerocercoids of Triaenophorus crassus in the second intermediate host Coregonus lavaretus and their effect on growth of the host. Journal of Fish Biology 55, 115–126.Google Scholar
Salgado-Maldonado, G (1993) Ecología de helmintos parásitos de Cichlasoma uropthalmus (Gunther) (Pisces: Cichlidae) en la Península de Yucatán, Mexico. Doctoral thesis, CINVESTAV IPN Mérida, Mexico.Google Scholar
Salgado-Maldonado, G and Kennedy, CR (1997) Richness and similarity of helminth communities in the tropical cichlid fish Cichlasoma urophthalmus from the Yucatán Peninsula, México. Parasitology 114, 581–590.Google Scholar
Schade, FM, Raupach, MJ and Wegner, KM (2016) Seasonal variation in parasite infection patterns of marine fish species from the Northern Wadden Sea in relation to interannual temperature fluctuations. Journal of Sea Research 113, 73–84.CrossRefGoogle Scholar
Scharlemann, JPW, Benz, D, Hay, SI, Purse, BV, Tatem, AJ, Wint, GRW and Rogers, DJ (2008) Global data for ecology and epidemiology: a novel algorithm for temporal Fourier processing MODIS data. PLoS ONE 3, e1408.CrossRefGoogle ScholarPubMed
Scholz, T and Aguirre-Macedo, MA (2000) Metacercariae of trematodes parasitizing freshwater fish in Mexico: a reappraisal and methods of study. pp. 101–115 in Salgado-Maldonado, G, García Aldrete, AN, Vidal-Martinez, VM (Eds) Metazoan parasites in the neotropics: a systematic and ecological perspective. Mexico, Instituto de Biologia, UNAM. Mexico City.Google Scholar
Scholz, T, Lavadores, JI, Vargas, J, Mendoza, EF, Rodríguez, R and Vivas, C (1994) Life cycle of Oligogonotylus manteri (Digenea: Cryptogonomidae), a parasite of cichlid fishes in Southern México. Journal of the Helminthological Society of Washington 61, 190–199.Google Scholar
Scholz, T, Vargas-Vázquez, J, Moravec, F, Vivas-Rodríguez, C and Mendoza-Franco, E (1995a) Cenotes (sinkholes) of the Yucatán Peninsula, México, as habitat of adult trematodes of fish. Folia Parasitologica 42, 37–47.Google Scholar
Scholz, T, Vargas-Vázquez, J, Moravec, F, Vivas-Rodríguez, C and Mendoza-Franco, E (1995b) Metacercariae of trematodes of fishes from cenotes (sinkholes) of the Yucatán Peninsula, México. Folia Parasitologica 42, 173–192.Google Scholar
Servicio Meteorológico Nacional (2005) Resumen de la temporada de ciclones Tropicales 2005. Available at http://smn.conagua.gob.mx/tools/DATA/Ciclones%20Tropicales/Resumenes/2005.pdf (accessed 10 October 2020).Google Scholar
Snyder, SD and Esch, GW (1993) Trematode community structure in the pulmonate snail Physa gyrina. Journal of Parasitology 79, 205–215.CrossRefGoogle ScholarPubMed
Soniat, TM, Hofmann, EE, Klinck, JM and Powell, EN (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, 99–114.CrossRefGoogle Scholar
Sosa-Medina, T, Vidal-Martínez, VM and Aguirre-Macedo, ML (2015) Metazoan parasites of fishes from the Celestun coastal lagoon, Yucatan, Mexico. Zootaxa 4007, 529–544.CrossRefGoogle ScholarPubMed
Sousa, WP (1990) Spatial scale and the processes structuring a guild of larval trematode parasites. pp. 41–67 in Esch, GW, Bush, AO and Aho, JM (Eds) Parasite communities: patterns and processes. London, Chapman & Hall.CrossRefGoogle Scholar
Stenseth, NC, Ottersen, G, Hurrell, JW, Mysterud, A, Lima, M, Chan, KS, Yoccoz, NG and Dlandsvik, B (2003) Studying climate effects on ecology through the use of climate indices: the North Atlantic Oscillation, El Niño Southern Oscillation and beyond. Proceedings of the Royal Society Biological Sciences 270, 2087–2096.CrossRefGoogle ScholarPubMed
Takahashi, T, Mori, K and Shigeta, Y (1961) Phototactic, thermotactic and geotactic responses of miracidia of Schistosoma japonicum. Japanese Journal of Parasitology 10, 686–691.Google Scholar
Tapia González, FU, Herrera-Silveira, JA and Aguirre-Macedo, ML (2008) Water quality variability and eutrophic trends in karstic tropical coastal lagoons of the Yucatán Peninsula. Estuarine Coastal and Shelf Science 76, 418–430.CrossRefGoogle Scholar
Varotsos, CA, Tzanis, CG and Sarlis, NV (2016) On the progress of the 2015-2016 El Niño event. Atmospheric Chemistry and Physics 16, 2007–2011.CrossRefGoogle Scholar
Väyrynen, T, Siddall, R, Tellervo Valtonen, E and Taskinen, J (2000) Patterns of trematode parasitism in lymnaeid snails from northern and central Finland. Annales Zoologici Fennici 37, 189–199.Google Scholar
Vega-Cendejas, ME (2004) Ictiofauna de la reserva de la Biosfera Celestún, Yucatán: una contribución al conocimiento de su biodiversidad. Anales del Instituto de Biología, Universidad Nacional Autónoma de México. Serie Zoología 75, 193–206.Google Scholar
Vidal-Martínez, VM, Aguirre-Macedo, ML, Scholz, T, González-Solís, D and Mendoza-Franco, E (2001) Atlas of the helminth parasites of cichlid fish of Mexico. Academia, Prague. 165 pp.Google Scholar
Vidal-Martínez, VM, Pal, P, Aguirre-Macedo, ML, May-Tec, AL and Lewis, JW (2014) Temporal variation in the dispersion patterns of metazoan parasites of a coastal fish species from the Gulf of Mexico. Journal of Helminthology, 88, 112–122.CrossRefGoogle ScholarPubMed
Voutilainen, A, Van Ooik, T, Puurtinen, M, Kortet, R and Taskinen, J (2009) Relationship between prevalence of trematode parasite Diplostomum sp. and population density of its snail host Lymnaea stagnalis in lakes and ponds in Finland. Aquatic Ecology 43, 351–357.CrossRefGoogle Scholar
Wei, WWS (1990) Time series analysis: univariate and multivariate methods. New York, Adisson–Wesley.Google Scholar
Wilson, K, Bjornstad, ON, Dobson, AP, Merler, S, Poglayen, G, Randolph, SE, Read, AF and Skorping, A (2002) Heterogeneities in macroparasite infections: patterns and processes. pp. 6–44 in Hudson, PJ, Rizzoli, A, Grenfell, BT, Heesterbeek, H and Dobson, AP (Eds) The ecology of wildlife diseases. Oxford, UK, Oxford University Press.Google Scholar
Yamaguti, S (1971) Synopsis of digenetic trematodes of vertebrates. Parts I, II. Tokyo, Keigaku Publishing Co. 1074 pp.Google Scholar
Yurlova, NI, Vodyanitskaya, SN, Serbina, EA, Biserkov, VY, Georgiev, BB and Chipev, NH (2006) Temporal variation in prevalence and abundance of metacercariae in the pulmonate snail Lymnaea stagnalis in Chany Lake, West Siberia, Russia: long-term patterns and environmental covariates. Journal of Parasitology 92, 249–259.CrossRefGoogle ScholarPubMed
Zemmer, SA, Wyderko, J, Da Silva Neto, J, Cedillos, I, Clay, L, Benfield, EF and Belden, LK (2017) Seasonal and annual variation in trematode infection of stream snail Elimia proxima in the southern Appalachian Mountains of Virginia. Journal of Parasitology 103, 213–220.CrossRefGoogle ScholarPubMed
Supplementary material: File

May-Tec et al. Supplementary Materials

May-Tec et al. Supplementary Materials 1

Download May-Tec et al. Supplementary Materials(File)
File 54.5 KB
Supplementary material: Image

May-Tec et al. Supplementary Materials

May-Tec et al. Supplementary Materials 2

Download May-Tec et al. Supplementary Materials(Image)
Image 6.7 MB
Supplementary material: Image

May-Tec et al. Supplementary Materials

May-Tec et al. Supplementary Materials 3

Download May-Tec et al. Supplementary Materials(Image)
Image 10.9 MB