Hostname: page-component-586b7cd67f-dlnhk Total loading time: 0 Render date: 2024-11-26T21:43:32.943Z Has data issue: false hasContentIssue false

Testing temporal stability of the larval digenean community in Heleobia conexa (Mollusca: Cochliopidae) and its possible use as an indicator of environmental fluctuations

Published online by Cambridge University Press:  27 August 2010

M. J. MERLO*
Affiliation:
Laboratorio de Parasitología, Facultad de ciencias Exactas y Naturales, Universidad Nacional de Mar del Plata, Funes 3350, 7600 Mar del Plata, Argentina, CONICET
J. A. ETCHEGOIN
Affiliation:
Laboratorio de Parasitología, Facultad de ciencias Exactas y Naturales, Universidad Nacional de Mar del Plata, Funes 3350, 7600 Mar del Plata, Argentina, CONICET
*
*Corresponding author: Tel: +54 223 4752426. Fax: +54 223 4753150. E-mail: [email protected]

Summary

Larval digeneans have been proposed as indicators of abundance and diversity of vertebrate and other hosts as well as environmental disturbances. To evaluate its response to environmental changes and its potential use as an indicator of environmental fluctuations, the temporal stability of the community of larval digeneans in Heleobia conexa was comparatively analysed in 4 separate years (1996, 1999, 2004 and 2005) in Mar Chiquita coastal lagoon (Buenos Aires province, Argentina). In total, 4579 specimens of H. conexa were collected and 22 digenean species were observed. Overall prevalence presented inter-annual and seasonal differences. These differences correlate with seasonal changes in composition of the vertebrate definitive host community and with the elimination of the preferred habitat of H. conexa in 1999. In general, the larval digenean community of H. conexa showed a yearly re-establishment following the annual cycle of H. conexa and the presence of definitive hosts. This annual restructuring allowed inferences about the effects of short-term environmental changes in the lagoon. According to these observations, the larval digenean community of H. conexa could be considered as a good bio-indicator with quick response to environmental disturbances.

Type
Research Article
Copyright
Copyright © Cambridge University Press 2010

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

REFERENCES

Botto, F., Iribarne, O. O. and Martínez, M. M. (1998). The effect of migratory shorebirds on the benthic species of three southwestern Atlantic Argentinean Estuaries. Estuaries 21, 700709. doi:10.2307/1353274.CrossRefGoogle Scholar
Bruschetti, M., Bazterrica, C., Luppi, T. A. and Iribarne, O. O. (2009). An invasive intertidal reef-forming polychaete affect habitat use and feeding behavior of migratory and locals birds in a SW Atlantic coastal lagoon. Journal of Experimental Marine Biology and Ecology 375, 7693. doi:10.1016/j.jembe.2009.05.008.CrossRefGoogle Scholar
Burger, J. (1986). The effect of human activity on shorebirds on two coastal bays in Northeastern United States. Environmental Conservation 13, 123130. doi:10.1017/S0376892900036717.CrossRefGoogle Scholar
Burger, J., Jettner, C., Clark, K. and Niles, L. J. (2004). The effect of human activities on migrant shorebirds: successful adaptive management. Environmental Conservation 31, 283288. doi:10.1017/S0376892904001626.CrossRefGoogle Scholar
Bustnes, J. O. and Galaktionov, K. (1999). Anthropogenic influences on the infestation of intertidal gastropods by seabird trematodes larvae on the southern Barents Sea coast. Marine Biology 133, 449453. doi:10.1007/s002270050484.CrossRefGoogle Scholar
Byers, J. E., Blakeslee, A. M. H., Linder, E., Cooper, A. B. and Maguire, T. J. (2008). Controls of spatial variation in the prevalence of trematode parasites infecting a marine snail. Ecology 89, 439451. doi:10.1890/06-1036.1.CrossRefGoogle ScholarPubMed
Curtis, L. A. (1997). Ilyanassa obsoleta (Gastropoda) as a host for trematodes in Delaware estuaries. Journal of Parasitology 83, 793803. doi:10.2307/3284270.CrossRefGoogle ScholarPubMed
Curtis, L. A. and Hubbard, K. M. (1990). Trematode infections in a gastropod host misrepresented by observing shed cercariae. Journal of Experimental Marine Biology and Ecology 143, 131137. doi:10.1016/0022-0981(90)90115-S.CrossRefGoogle Scholar
Curtis, L. A. and Hurd, L. E. (1983). Age, sex, and parasites: spatial heterogeneity in a sandflat population of Ilyanassa obsoleta. Ecology 64, 819828. doi:10.2307/1937205.CrossRefGoogle Scholar
De Francesco, C. G. and Isla, F. I. (2001). Gasterópodos bioindicadores de salinidad en Mar Chiquita. In Reserva de Biósfera Mar Chiquita: Características Físicas, Biológicas y Ecológicas (ed. Iribarne, O. O.), pp. 115119. Editorial Martin, Mar del Plata, Argentina.Google Scholar
De Francesco, C. G. and Isla, F. I. (2003). Distribution and abundance of hydrobiid snails in mixed estuary and coastal lagoon, Argentina. Estuaries 26, 790797. doi:10.1007/BF02711989.CrossRefGoogle Scholar
De Francesco, C. G. and Isla, F. I. (2004). The life cycle and growth of Heleobia australis (D'orbigny, 1835) and H. conexa (Gailard, 1974) (Gastropoda: Rissooidea) in Mar Chiquita coastal lagoon (Argentina). Journal of Molluscan Studies 70, 173178. doi:10.1093/mollus/70.2.173.CrossRefGoogle Scholar
Esch, G. W., Barger, M. A. and Fellis, K. J. (2002). The transmission of digenetic trematodes: style, elegance, complexity. Integrative and Comparative Biology 42, 304312. doi:10.1093/icb/42.2.304.CrossRefGoogle ScholarPubMed
Esch, G. W., Curtis, L. A. and Barger, M. A. (2001). A perspective on the ecology of trematode communities in snails. Parasitology 123 (Suppl.), S57S75. doi:10.1017/S0031182001007697.CrossRefGoogle ScholarPubMed
Esch, G. W. and Fernández, J. (1994). Snail trematode interactions and parasite community dynamics in aquatic systems: a review. American Midland Naturalist 131, 209237. doi:10.2307/2426248.CrossRefGoogle Scholar
Etchegoin, J. A. (1997). Sistemas parasitarios presentes en la albufera Mar Chiquita. Tesis Doctoral. Facultad de Ciencias Exactas y Naturales. Universidad Nacional de Mar del Plata, Argentina.Google Scholar
Etchegoin, J. A. (2001). Dinámica de los sistemas parasitarios. In Reserva de Biósfera Mar Chiquita: Características Físicas, Biológicas y Ecológicas (ed. Iribarne, O. O.), pp. 227250. Editorial Martin, Mar del Plata, Argentina.Google Scholar
Etchegoin, J. A. and Martorelli, S. R. (1997). Description of a new species of Maritrema (Digenea: Microphallidae) from Mar Chiquita coastal lagoon (Buenos Aires, Argentina) with notes on its life cycle. Journal of Parasitology 83, 709713. doi:10.2307/3284251.CrossRefGoogle Scholar
Etchegoin, J. A. and Martorelli, S. R. (1998). Nuevos estadios larvales de digeneos parásitos de Heleobia conexa (Mollusca: Hydrobiidae) en Mar Chiquita (Buenos Aires, Argentina). Neotrópica 44, 4150.Google Scholar
Faltýnková, A., Valtonen, E. T. and Karvonen, A. (2008). Spatial and temporal structure of the trematode component community in Valvata macrostoma (Gastropoda, Prosobranchia). Parasitology 135, 16911699. doi:10.1017/S0031182008005027.CrossRefGoogle ScholarPubMed
Fernández, J. and Esch, G. W. (1991 a). Guild structure of larval trematodes in the snail Helisoma anceps: Patterns and processes at the individual host level. Journal of Parasitology 77, 528539. doi:10.2307/3283156.CrossRefGoogle ScholarPubMed
Fernández, J. and Esch, G. W. (1991 b). The component community structure of larval trematodes in the pulmonate snail Helisoma anceps. Journal of Parasitology 77, 540550. doi:10.2307/3283157.CrossRefGoogle ScholarPubMed
Ferrero, L. (2001). La avifauna de Mar Chiquita. Sintesis de la tesis Doctoral de M. M. Martínez. In Reserva de Biósfera Mar Chiquita: Características Físicas, Biológicas y Ecológicas (ed. Iribarne, O. O.), pp. 227250. Editorial Martín, Mar del Plata, Argentina.Google Scholar
Fingerut, J. T., Zimmer, C. A. and Zimmer, R. K. (2003). Patterns and processes of larval emergence in an estuarine parasite system. The Biological Bulletin 205, 110120. doi:10.2307/1543232.CrossRefGoogle Scholar
Fredensborg, B. L., Mouritsen, K. N. and Poulin, R. (2006). Relating bird host distibution and spatial heterogeneity in trematodes infection in an intertidal snail-from small to large scale. Marine Biology 149, 275283. doi:10.1007/s00227-005-0184-1.CrossRefGoogle Scholar
Granovitch, A. I., Sergievsky, S. O. and Sokolova, I. M. (2000). Spatial and temporal variation of trematode infection in coexisting populations of intertidal gastropods Littorina saxatilis and L. obtusata in the White Sea. Diseases of Aquatic Organisms 41, 5364. doi:10.3354/dao041053.CrossRefGoogle ScholarPubMed
Hechinger, R. F. and Lafferty, K. D. (2005). Host diversity begets parasite diversity: bird final host and trematodes in snail intermediate hosts. Proceedings of the Royal Society of London, B 272, 10591066. doi:10.1098/rspb.2005.3070.Google ScholarPubMed
Hechinger, R. F., Lafferty, K. D., Huspeni, T. C., Brooks, A. J. and Kuris, A. M. (2007). Can parasites be indicators of free-living diversity? Relationships between species richness and the abundance of larval trematodes and of local benthos and fishes. Oecologia 151, 8292. doi:10.1007/s00442-006-0568-z.CrossRefGoogle ScholarPubMed
Hechinger, R. F., Lafferty, K. D., Mancini, F. T. III, Warner, R. R. and Kuris, A. M. (2008). How large is the hand in the puppet? Ecological and evolutionary factors affecting body mass of 15 trematode parasitic castrators in their snail host. Evolutionary Ecology 23, 651667. doi:10.1007/s10682-008-9262-4.CrossRefGoogle Scholar
Huspeni, T. C., Hechinger, R. F. and Lafferty, K. D. (2005). Trematode parasites as estuarine indicators: opportunities, applications, and comparisons with conventional community approaches. In Estuarine Indicators (ed. Bortone, S.), pp. 297314. CRC Press. Boca Raton, FL, USA.Google Scholar
Huspeni, T. C. and Lafferty, K. D. (2004). Using larval trematodes that parasitize snails to evaluate a salt-marsh restoration project. Ecological Applications 14, 795804. doi:10.1890/01-5346.CrossRefGoogle Scholar
Jokela, J. and Lively, C. M. (1995). Spatial variation in infection by digenetic trematodes in a population of freshwater snails (Potamopyrgus antipodarum). Oecologia 103, 509517. doi:10.1007/BF00328690.CrossRefGoogle Scholar
Keas, B. E. and Blankespoor, H. D. (1997). The prevalence of cercariae from Stagnicola emarginata (Lymnaeidae) over 50 years in Northern Michigan. Journal of Parasitology 83, 536540. doi:10.2307/3284427.CrossRefGoogle ScholarPubMed
Krebs, C. J. (1999). Ecological Methodology, 2nd Edn. Addison-Wesley Educational Publisher, Menlo Park, CA, USA.Google Scholar
Kube, J., Kube, S. and Dierschke, V. (2002). Spatial and temporal variation in the trematode component community of the mudsnail Hydrobia ventrosa in relation to the occurrence of waterfowl as definitive hosts. Journal of Parasitology 88, 10751086.CrossRefGoogle Scholar
Kuris, A. M. (1991). Guild structure of larval trematodes in molluscan hosts: prevalence, dominance and significance of competition. In Parasite Communities: Patterns and Processes (ed. Esch, G. W., Bush, A. and Aho, J.), pp. 69100. Chapman and Hall, London, UK.Google Scholar
Kuris, A. M. and Lafferty, K. D. (1994). Community structure: larval trematodes in snail host. Annual Review of Ecology and Systematics 25, 189217. doi:10.1146/annurev.es.25.110194.001201.CrossRefGoogle Scholar
Lafferty, K. D. (1997). Environmental parasitology: what can parasites tell us about human impacts on the environment?. Parasitology Today 13, 251255. doi:10.1016/S0169-4758(97)01072-7.CrossRefGoogle ScholarPubMed
Lafferty, K. D. (2001). Birds at Southern California Beach: seasonality, habitat use and disturbance by human activity. Biodiversity and Conservation 10, 19491962. doi:10.1023/A:1013195504810.CrossRefGoogle Scholar
Lafferty, K. D., Goodman, D. and Sandoval, C. P. (2006 b). Restoration of breeding by snowy plovers following protection from disturbance. Biodiversity and Conservation 15, 22172230. doi:10.1007/s10531-004-7180-5.CrossRefGoogle Scholar
Lafferty, K. D., Hechinger, R. F., Shaw, J. C., Whitney, K. and Kuris, A. M. (2006 a). Food webs and parasites in a salt marsh ecosystem. In Disease Ecology: Community Structure and Pathogen Dynamics (ed. Collinge, S. K. and Ray, C.), pp. 119134. Oxford University Press, Oxford, UK.CrossRefGoogle Scholar
Lafferty, K. D. and Kuris, A. M. (2004). Parasitism and environmental disturbances. In Parasitism and Ecosystems (ed. Thomas, F., Renaud, F. and Guégan, J-F), pp. 113123. Oxford University Press, Oxford, UK.Google Scholar
Lafferty, K. D., Sammond, D. T. and Kuris, A. M. (1994). Analysis of larval trematode communities. Ecology 75, 22752285. doi:10.2307/1940883.CrossRefGoogle Scholar
Loot, G., Aldana, M. and Navarrete, S. A. (2005). Effects of human exclusion on parasitism in intertidal food webs of central Chile. Conservation Biology 19, 203212. doi:10.1111/j.1523-1739.2005.00396.x.CrossRefGoogle Scholar
Loot, G., Blanchet, S., Aldana, S. and Navarrete, S. A. (2008). Evidence of plasticity in the reproduction of trematode parasite: the effect of host removal. Journal of Parasitology 94, 2327. doi:10.1645/GE-1278.1.CrossRefGoogle ScholarPubMed
Ludwig, J. A. and Reynolds, J. F. (1988). Statistical Ecology. John Wiley and Sons, Inc. New York, USA.Google Scholar
Luppi, T. A. and Bas, C. C. (2002). The role of invasive polychaete Ficopomatus enigmatus Fauvel 1923 (Polychaeta: Serpulidae) reefs in the recruitment of Cyrtograpsus angulatus Dana 1851 (Brachyura: Grapsidae) in the Mar Chiquita coastal lagoon, Argentina. Ciencias Marinas 28, 319330.CrossRefGoogle Scholar
Magurran, A. E. (1988). Ecological Diversity and its Measurement. 1st Edn. Princeton University Press. Princeton, NJ, USA.CrossRefGoogle Scholar
Marcogliese, D. J. (2005). Parasites of the superorganism: are they indicators of ecosystem health?. International Journal for Parasitology 35, 705716. doi:10.1016/j.ijpara.2005.01.015.CrossRefGoogle ScholarPubMed
Martorelli, S. R. (1986). Estudio sistemático y biológico de un digeneo perteneciente a la familia Microphallidae Travassos, 1920.I: Microphallus szidati sp. nov. parásito intestinal de Rallus sanguinolentus sanguinolentus (Aves: Rallidae) e Himantopus melanurus (Aves: Recurvirostridae). Revista Ibérica de Parasitología 46, 373378.Google Scholar
Martorelli, S. R. (1988). El ciclo biológico de Levinseniella cruzi Travassos, 1920 (Digenea, Microphallidae) parásita de los ciegos cólicos de Rollandia rooland chilensis (Aves, Podicipedidae) e Himantopus melanurus (Aves, Recurvirostridae). Iheringia 68, 4962.Google Scholar
Martorelli, S. R. (1989). Estudios parasitológicos en la albufera Mar Chiquita, provincia de Buenos Aires, República Argentina. II. Cercarias (Digenea) parásitas de Heleobia conexa (Mollusca: Hydrobiidae), pertenecientes a las familias Schistosomatidae, Haploporidae y Homalometridae. Neotrópica 35, 8190.Google Scholar
Martorelli, S. R. (1990). Estudios parasitológicos en la albufera Mar Chiquita, provincia de Buenos Aires, República Argentina. III: Sobre dos cercarias parásitas de Heleobia conexa (Mollusca: Hydrobiidae) pertenecientes a la superfamilia Echinostomatoidea. Neotrópica 36, 5563.Google Scholar
Martorelli, S. R. (1991). El ciclo biológico de Microphallus simillimus (Travassos, 1920), comb. n. (Digenea: Microphallidae), parásito de Heleobia conexa (Mollusca: Hydrobiidae) y de Himantopus melanurus (Aves: Recurvirostridae) en Argentina. Iheringia 71, 9198.Google Scholar
Martorelli, S. R. and Etchegoin, J. A. (1996). Cercarias de la superfamilia Opistorchioidea en Heleobia conexa (Mollusca: Hydrobiidae) de la albufera de Mar Chiquita. Neotrópica 42, 6167.Google Scholar
Obenat, S. and Pezzani, S. (1989). Ecological studies of Ficopomatus (Mercierella) enigmaticus (Annelida: Polychaeta) in Mar Chiquita coastal lagoon (Buenos Aires, Argentina). In Conservation and Development: the Sustainable Use of Wetland Resources, pp. 165166.Third International Wetlands Conference. Editions du Museum National d'Histoire Naturelle, Paris, France.Google Scholar
Obenat, S. and Pezzani, S. (1994). Life cycle and population structure of the polychaete Ficopomatus enigmaticus (Serpulidae) in Mar Chiquita coastal lagoon, Argentina. Estuaries 17, 263270. doi:10.2307/1352574.CrossRefGoogle Scholar
Obenat, S., Spivak, E., Garrido, L. (2006). Life history and reproductive biology of the invasive amphipod Melita palmata (Amphipoda: Melitidae) in the Mar Chiquita coastal lagoon, Argentina. Journal of the Marine Biological Association of the United Kingdom 86, 13811387. doi:10.1017/S002531540601441X.CrossRefGoogle Scholar
Pezzani, S. and Obenat, S. (1988). Estudio integrado de la laguna costera Mar Chiquita, Provincia de Buenos Aires, Argentina. 1. Características de la población de Ficopomatus enigmaticus. In Informe UNESCO Ciencias Marinas 47, pp. 101102. UNESCO, Argentina.Google Scholar
Pietrock, M. and Marcogliese, D. J. (2003). Free-living endohelminth stages: at the mercy of environmental conditions. Trends in Parasitology 19, 293299. doi:10.1016/S1471-4922(03)00117-X.CrossRefGoogle ScholarPubMed
Poulin, R. (2006). Global warming and temperature-mediated increases in cercarial emergence in trematode parasites. Parasitology 132, 143151. doi:10.1017/S0031182005008693.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
Reta, R., Martos, P., Perillo, G. M. E., Piccolo, M. C. and Ferrante, A. (2001). Características hidrográficas del estuario de la laguna Mar Chiquita. In Reserva de Biósfera Mar Chiquita: Características Físicas, Biológicas y Ecológicas (ed. Iribarne, O. O.), pp. 3152. Editorial Martín, Mar del Plata, Argentina.Google Scholar
Rohde, K. (1981). Population dynamics of two snail species, Planaxis sulcatus and Cerithium moniliferum, and their trematode species at Heron Island, Great Barrier Reef. Oecologia 49, 344352. doi:10.1007/BF00347596.CrossRefGoogle ScholarPubMed
Sapp, K. K. and Esch, G. W. (1994). The effects of spatial and temporal heterogeneity as structuring forces for parasite communities in Helisoma anceps and Physa gyrina. American Midland Naturalist 132, 91103. doi:10.2307/2426204.CrossRefGoogle Scholar
Schwindt, E., Bortolus, A. and Iribarne, O. O. (2001). Invasion of a reef-builder polychaete: direct and indirect impacts on the native benthic community structure. Biological Invasions 3, 137149. doi:10.1023/A:1014571916818.CrossRefGoogle Scholar
Schwindt, E. and Iribarne, O. O. (2000). Settlement sites, survival and effects on benthos of an introduced reef-building polychaete in a SW Atlantic coastal lagoon. Bulletin of Marine Science 67, 7382.Google Scholar
Skirnisson, K., Galaktionov, K. V. and Kozminsky, E. V. (2004). Factors influencing the distribution of digenetic trematode infections in a mudsnail (Hydrobia ventrosa) population inhabiting salt marsh ponds in Iceland. Journal of Parasitology 90, 5059. doi:10.1645/GE-118R.CrossRefGoogle Scholar
Smith, N. F. (2007). Associations between shorebird abundante and parasites in the sand crab, Emerita Analoga, along the California coast. Journal of Parasitology 93, 265273. doi:10.1645/GE-1002R.1.CrossRefGoogle Scholar
Sousa, W. P. (1991). Spatial scale and the processes structuring a guild of larval trematode parasites. In Parasite Communities: Patterns and Processes (ed. Esch, G. W., Bush, A. and Aho, J.), pp. 4167. Chapman and Hall, London, UK.Google Scholar
Sousa, W. P. (1993). Interspecific antagonism and species coexistence in a diverse guild of larval trematode parasites. Ecological Monographs 63, 103128. doi:10.2307/2937176.CrossRefGoogle Scholar
Vidal-Martínez, V. M., Pech, D., Sures, B., Purucker, S. T. and Poulin, R. (2010). Can parasites really reveal environmental impact? Trends in Parasitology 26, 4451. doi:10.1016/j.pt.2009.11.001.CrossRefGoogle ScholarPubMed
Zar, J. H. (2009). Biostatistical Analysis, 5th Edn. Pearson Education, Inc. New Jersey, NJ, USA.Google Scholar