Hostname: page-component-848d4c4894-tn8tq Total loading time: 0 Render date: 2024-06-24T14:05:36.611Z Has data issue: false hasContentIssue false

Parasites as bioindicators of environmental degradation in Latin America: A meta-analysis

Published online by Cambridge University Press:  27 June 2016

V.M. Vidal-Martínez*
Affiliation:
Centro de Investigación y de Estudios Avanzados del Instituto Politécnico Nacional, Unidad Mérida, Km 6 Carretera Antigua a Progreso, Cordemex, Mérida, Yucatán 97310, México
A.C. Wunderlich
Affiliation:
School of Biological Sciences, Royal Holloway, University of London, Egham, Surrey, TW20 0EX, UK

Abstract

Unregulated economic growth in Latin America has resulted in environmental degradation, including the release of toxic compounds into the environment. One strategy to understand and prevent the outcomes of this harmful environmental degradation is the use of bioindicators. These are free-living or parasite species that respond to habitat alterations with changes in their numbers, physiology or chemical composition. The aim of this review was to determine whether there is evidence of a significant parasite response to environmental damage in Latin America. We collected 26 papers published between 2003 and 2015 and conducted a meta-analysis to test the null hypothesis that there is no significant overall effect of environmental insults on parasites. The meta-analysis showed a low but still significant negative mean overall effect (Hedges’ g = −0.221; 95% CI: −0.241 to −0.200; P < 0.0001). However, the magnitudes and directions of the significant effects varied widely. These results suggest that different groups of parasites have distinct responses to various environmental insults and that the groups should be separately analysed after the accumulation of a sufficient number of studies. For future studies on this topic in Latin America, we suggest: (1) using field and experimental approaches to determine the response of parasites to environmental degradation; (2) using an interdisciplinary approach, including different types of biomarkers in both parasites and individual hosts to generate long-term datasets in polluted and reference areas; (3) conducting studies on parasites as accumulation bioindicators.

Type
Review Article
Copyright
Copyright © Cambridge University Press 2016 

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

Acosta, A.A., Queiroz, J., Brandão, H., Carvalho, E.D. & da Silva, R.J. (2013) Helminths of Steindachnerina insculpta in two distinct stretches of the Taquari River, state of São Paulo, Brazil. Revista Brasileira de Parasitología Veterinaria Jaboticabal 22, 539547.*Google Scholar
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, 14031408.*Google Scholar
Aldana, M., Pulgar, J.M., Orellana, N.F., Ojeda, F.P. & García-Huidobro, M.R. (2013) Increased parasitism of limpets by a trematode metacercaria in fisheries management areas of central Chile: effects on host growth and reproduction management areas and parasitism. Ecohealth 11, 215226.*Google Scholar
Amiard-Triquet, C., Amiard, J.C. & Rainbow, P.S. (2013) Ecological biomarkers: indicators of ecotoxicological effects. 434 pp. Boca Raton, FL, CRC Press, Taylor & Francis Group.Google Scholar
Arzua, M., Navarro-Da Silva, M.A., Famadas, K.M., Beati, L. & Moraes-Barros-Battesti, D.M. (2003) Amblyomma aureolatum and Ixodes auritulus (Acari: Ixodidae) on birds in southern Brazil, with notes on their ecology. Experimental and Applied Acarology 31, 283296.*Google Scholar
Belo, N.O., Pinheiro, R.T., Reis, E.S., Ricklefs, R.E. & Braga, E.M. (2011) Prevalence and lineage diversity of avian haemosporidians from three distinct cerrado habitats in Brazil. PLoS ONE 6, e17654.*Google Scholar
Caquet, T., Lagadic, L. & Sheffield, S.R. (2000) Mesocosms in ecotoxicology (1): outdoor aquatic systems. Reviews of Environmental Contamination and Toxicology 165, 138.Google Scholar
Cardoso, T.S., Simões, R.O., Luque, J.L.F., Maldonado, A. Jr & Gentile, R. (2015) The influence of habitat fragmentation on helminth communities in rodent populations from a Brazilian Mountain Atlantic Forest. Journal of Helminthology. Published online 23 July 2015. http://dx.doi.org/10.1017/S0022149X15000589, *Google Scholar
Castro-Diaz, E. & Kuna, Y. (2007) International expert group meeting on indigenous people and protection of the environment. Environment issues in the Latin American region. Khabarovsk, Russian Federation, 27–29 August 2007. United Nations PFII/2007/WS.3/4, 8 p.Google Scholar
Centeno-Chalé, O.A., Aguirre-Macedo, M.L., Gold-Bouchot, G. & Vidal-Martínez, V.M. (2015). Potential effects of chemical pollution on the helminth communities of the Mexican flounder Cyclopsetta chittendeni from the Campeche sound, Gulf of Mexico. Ecotoxicology and Environmental Safety 119, 162169.*Google Scholar
Cohen, J. (1988) Statistical power analysis for the behavioral sciences. 2nd edn. 567 pp. Hillsdale, NJ, Lawrence Erlbaum Associates.Google Scholar
Fajer-Ávila, E.J., García-Vázquez, A., Plascencia-González, H., Ios-Sicairos, J.R., García-De La Parra, L.M. & Betancourt-Lozano, M. (2006) Copepods and larvae of nematodes parasitizing the white mullet Mugil curema (Valenciennes, 1836): indicators of anthropogenic impacts in tropical coastal lagoons? Environmental Monitoring and Assessment 122, 221237.*Google Scholar
Gold-Bouchot, G., Zapata-Pérez, O., Ceja-Moreno, V., Rodríguez-Fuentes, G., Simá-Álvarez, R., Aguirre-Macedo, M.L. & Vidal-Martínez, V.M. (2007) Biological effects of environmental pollutants in American oyster, Crassostrea virginica: a field study in Laguna de Terminos, Mexico. International Journal Environmental Health 1, 171184.Google Scholar
Golestaninasab, A., Malek, M., Roohia, M.A., Karbassib, A.R., Amoozadeha, E., Rashidinejada, R., Ghayoumib, R. & Sures, B. (2014) A survey on bioconcentration capacities of some marine parasitic and free-living organisms in the Gulf of Oman. Ecological Indicators 37, 99104.Google Scholar
Gomes-Lopes, S., Costa-Junior, L.M. & Vasconcellos de Andrade, G. (2011) Ectoparasites of Tropidurus hispidus (Squamata: Tropiduridae) as bioindicators of human impact. 23rd International Conference of the World Association for the Advancement of Veterinary Parasitology, 2011, Buenos Aires, Argentina. p. 361.*Google Scholar
Hechinger, R.F., Lafferty, K.D. & Kuris, A.M. (2008). Trematodes indicate animal biodiversity in the Chilean intertidal and Lake Tanganyika. Journal of Parasitology 94, 966968.*Google Scholar
Hedges, L.V., Gurevitch, J. & Curtis, P.S. (1999) The meta-analysis of response ratios in experimental ecology. Ecology 80, 11501156.Google Scholar
Ikemoto, T., Kunito, T., Tanaka, H., Baba, N., Miyazaki, N. & Tanabe, S. (2004) Detoxification mechanism of heavy metals in marine mammals and seabirds: interaction of selenium with mercury, silver, copper, zinc, and cadmium in liver. Archives of Environmental Contamination and Toxicology 47, 402413.Google Scholar
Jezierska, B. & Witeska, M. (2006) The metal uptake and accumulation in fish living in polluted waters. pp. 107114 in Twardowska, I., Allen, H.E., Häggblom, M.M. & Stefaniak, S. (Eds) Viable methods of soil and water pollution monitoring, protection and remediation. The Netherlands, Nato Science Series, Springer Netherlands.Google Scholar
Johnson, P.T.J., Chase, J.M., Dosch, K.L., Hartson, R.B., Gross, J.A., Larson, D.J., Sutherland, D.R. & Carpenter, S.R. (2007) Aquatic eutrophication promotes pathogenic infection in amphibians. Proceedings of the National Academy of Sciences, USA 104, 1578115786.Google Scholar
Khaleghzadeh-Ahangar, H., Malek, M. & Mackenzie, K. (2011) The parasitic nematodes Hysterothylacium sp. type MB larvae as bioindicators of lead and cadmium: a comparative study of parasite and host tissues. Parasitology 138, 14001405.Google Scholar
Kleinertz, S., Eckhardt, K.-U., Theisena, S., Palma, H.W. & Leinweber, P. (2015) Acanthocephalan fish parasites (Rhadinorhynchidae Lühe, 1912) as potential biomarkers: Molecular–chemical screening by pyrolysis-field ionization mass spectrometry. Journal of Sea Research. DOI: 10.1016/j.seares.2015.10.001.Google Scholar
Kuris, A.M. (1980) Hosts as islands. American Naturalist 116, 570586.Google Scholar
Lafferty, K.D. (1997) Environmental parasitology: what can parasites tell us about human impacts on the environment? Parasitology Today 13, 251255.Google Scholar
Lafferty, K.D., Hechinger, R.F., Lorda, J. & Soler, L. (2005) Trematodes associated with mangrove habitat in Puerto Rican salt marshes. Journal of Parasitology 91, 697699.*Google Scholar
Loot, G., Aldana, M. & Navarrete, S.A. (2005) Effects of human exclusion on parasitism in intertidal food webs of central Chile. Conservation Biology 19, 203212.*Google Scholar
Magalhães-Campião, K., Delatorre, M., Batista-Rodrigues, R., da Silva, R.J. & Ferreira, V.L. (2012) The effect of local environmental variables on the helminth parasite communities of the pointedbelly frog Leptodactylus podicipinus from ponds in the Pantanal wetlands. Journal of Parasitology 98, 229235.*Google Scholar
Malek, M., Haseli, M., Mobedi, I., Ganjali, M.R. & Mackenzie, K. (2007) Parasites as heavy metal bioindicators in the shark Carcharhinus dussumieri from the Persian Gulf. Parasitology 134, 10531066.Google Scholar
Marcogliese, D.J. (2005) Parasites of the superorganism: Are they indicators of ecosystem health? International Journal of Parasitology 35, 705716.Google Scholar
May-Tec, A.L., Pech, D., Aguirre-Macedo, M.L., Lewis, J.W. & Vidal-Martínez, V.M. (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, 385395.Google Scholar
Nachev, M. & Sures, B. (2016) Environmental parasitology: parasites as accumulation bioindicators in the marine environment. Journal of Sea Research (in press). doi:10.1016/j.seares.2015.06.005.Google Scholar
Nachev, M., Schertzinger, G. & Sures, B. (2013) Comparison of the metal bioconcentration capacity between the acanthocephalan Pomphorhynchus laevis and larval nematodes of the genus Eustrongylides sp. infecting barbel (Barbus barbus). Parasites & Vectors 6, 21.Google Scholar
Neira-O., P., Muñoz-S., N., Stanley-V., B., Gosh-C., M. & M. Rosales-L., M.J. (2010) Cryptosporidium parvum en gastrópodos silvestres como bioindicadores de contaminación fecal en ecosistemas terrestres. Revista Chilena de Infectología 27, 211218.*Google Scholar
Ortega-Álvarez, R. & MacGregor-Fors, I. (2011) Dusting-off the file: A review of knowledge on urban ornithology in Latin America. Landscape and Urban Planning 101, 110.Google Scholar
Palm, H.W., Kleinertz, S. & Rückert, S. (2011) Parasite diversity as an indicator of environmental change? An example from tropical grouper (Epinephelus fuscoguttatus) mariculture in Indonesia. Parasitology 138, 17931803.Google Scholar
Pech, D., Vidal-Martínez, V.M., Aguirre-Macedo, M.L., Gold-Bouchot, G., Herrera-Silveira, J., Zapata-Pérez, O. & Marcogliese, D. (2009) The checkered puffer (Spheroides testudineus) and its helminths as bioindicators of chemical pollution in Yucatan coastal lagoons. Science of the Total Environment 407, 23152324.*Google Scholar
Podolska, M., Nadolna, K. & Szostakowska, B. (2014) Acetylcholinesterase activity in the host–parasite system of the cod Gadus morhua and acanthocephalan Echinorhynchus gadi from the southern Baltic Sea. Marine Pollution Bulletin 79, 100106.Google Scholar
Ribeiro, T.S., Ghisi, N.C., Prioli, A.J., Oliveira, E.C. & Takemoto, R.M. (2013) Diversity of Nematodes of red-tail-lambari Astyanax aff. paranae (Teleostei: Characidae) from polluted sites of a tropical river system. Neotropical Helminthology 7, 271281.*Google Scholar
Rosenberg, M.S., Adams, D.C. & Gurevitch, J. (2000) MetaWin: Statistical software for Meta-analysis V2. 128 pp. Sunderland, Massachusetts, Sinauer Associates.Google Scholar
Sánchez-Ramírez, C. (2007) Aspectos biológicos de la tilapia Oreochromis niloticus y poblaciones del monogeneo Cichlidogyrus sclerosus como indicadores de contaminación química en un ambiente lagunar tropical. PhD thesis, Centro de Investigación y de Estudios Avanzados del Instituto Politécnico Nacional Unidad Mérida.Google Scholar
Sánchez-Ramírez, C., Vidal-Martinez, V.M., Aguirre-Macedo, M.L., Rodríguez-Canul, R.P., Gold-Bouchot, G. & Sures, B. (2007) Cichlidogyrus sclerosus (Monogenea: Ancyrocephalinae) and its host the nile tilapia (Oreochromis niloticus) as bioindicators of chemical pollution. Journal of Parasitology 93, 10971106.*Google Scholar
Sciortino, J.A. & Ravikumar, R. (1999) Fishery harbour manual on the prevention of pollution. Bay of Bengal Programme. 215 pp. Madras, India, FAO/BOBP/MAG/22.Google Scholar
Silva, V., Valenzuela, A., Ruiz, P. & Oyarzún, C. (2005) Trypanosoma humboldti in Schroederichthys chilensis (Chondrichthyes, Elasmobranchii, Scyliorhinidae) as non destructive indicator of contamination. Gayana 69, 160165.*Google Scholar
Simões, R., Gentile, R., Rademaker, V., D'Andrea, P., Herrera, H., Freitas, T., Lanfredi, R. & Maldonado, A. Jr (2010) Variation in the helminth community structure of Thrichomys pachyurus (Rodentia: Echimyidae) in two sub-regions of the Brazilian Pantanal: the effects of land use and seasonality. Journal of Helminthology 84, 266275.*Google Scholar
Simões, R., Maldonado, A. Jr, Olifiers, N., Garcia, J.S., Bertolino, A.V.F.A. & Luque, J.L. (2014) A longitudinal study of Angiostrongylus cantonensis in an urban population of Rattus norvegicus in Brazil: the influences of seasonality and host features on the pattern of infection. Parasites & Vectors 7, 100.*Google Scholar
Simões, R., Luque, J.L., Gentile, R., Rosa, M.C.S., Costa-Neto, S. & Maldonado, A. Jr (2016) Biotic and abiotic effects on the intestinal helminth community of the brown rat Rattus norvegicus from Rio de Janeiro, Brazil. Journal of Helminthology 90, 2127.*Google Scholar
Sures, B. (2003) Accumulation of heavy metals by intestinal helminths in fish: an overview and perspective. Parasitology 126, S53S60.Google Scholar
Sures, B. (2008) Environmental parasitology: interactions between parasites and pollutants in the aquatic environment. Parasite 15, 434438.Google Scholar
Sures, B., Slidell, R. & Taraschewski, H. (1999) Parasites as accumulation indicators of heavy metal pollution. Parasitology Today 15, 1621.Google Scholar
Sures, B., Scheible, T., Bashtar, A.R. & Taraschewski, H. (2003) Lead concentrations in Hymenolepis diminuta adults and Taenia taeniaeformis larvae compared to their rat hosts (Rattus norvegicus) sampled from the city of Cairo, Egypt. Parasitology 127, 483487.Google Scholar
Tellez, M. & Merchant, M. (2015) Biomonitoring heavy metal pollution using an aquatic apex predator, the American alligator, and its parasites. PLoS ONE 10, e0142522.Google Scholar
Tweedley, J.R., Warwick, R.M., Clarke, K.R. & Potter, I.C. (2014) Family-level AMBI is valid for use in the north-eastern Atlantic but not for assessing the health of microtidal Australian estuaries. Estuaries and Coastal Shelf Science 141, 8596.Google Scholar
Vidal-Martínez, V.M. (2007) Helminths and protozoans of aquatic organisms as bioindicators of chemical pollution. Parassitologia 49, 177184.Google Scholar
Vidal-Martínez, V.M., Aguirre-Macedo, M.L., Noreña-Barroso, E., Gold-Bouchot, G. & Caballero-Pinzón, P.I. (2003) Potential interactions between metazoan parasites of the mayan catfish Ariopsis assimilis and chemical pollution in Chetumal Bay, Mexico. Journal of Helminthology 77, 173184.*Google Scholar
Vidal-Martínez, V.M., Aguirre-Macedo, M.L., Del Rio Rodríguez, R., Gold-Bouchot, G., Rendón-von Osten, J. & Miranda-Rosas, G.A. (2006) The pink shrimp Farfantepenaeus duorarum, its symbionts and helminths as bioindicators of chemical pollution in Campeche Sound, Mexico. Journal of Helminthology 80, 159174.*Google Scholar
Vidal-Martínez, V.M., Pech, D., Sures, B., Poulin, R. & Purucker, T. (2010) Can parasites really reveal environmental impact? Trends in Parasitology 26, 4451.Google Scholar
Vidal-Martínez, V.M., Pal, P., Aguirre-Macedo, M.L., May Tec, A.L. & Lewis, J.W. (2014a) Temporal variation in the dispersion patterns of metazoan parasites of a coastal fish species from the Gulf of Mexico. Journal of Helminthology 88, 112122.Google Scholar
Vidal-Martinez, V.M., Centeno-Chale, O.A., Torres-Irineo, E., Sánchez-Ávila, J.I., Gold-Bouchot, G. & Aguirre-Macedo, M.L. (2014b) The metazoan parasite communities of the shoal flounder (Syacium gunteri) as bioindicators of chemical contamination in the southern Gulf of Mexico. Parasites & Vectors 7, 541.*Google Scholar
Vidal-Martínez, V.M., Torres-Irineo, E., Romero, D., Gold-Bouchot, G., Martínez-Meyer, E. & Aguirre-Macedo, M.L. (2015). Environmental and anthropogenic factors affecting the probability of occurrence of Oncomegas wageneri (Cestoda: Trypanorhyncha) in the southern Gulf of Mexico. Parasites & Vectors 8, 609.Google Scholar
Warwick, R.M. (1993). Environmental impact studies on marine communities: pragmatical considerations. Australian Journal of Ecology 18, 6380.Google Scholar
Woelfl, S., Mages, M. & Torres, P. (2008) Trace metal concentrations in single specimens of the intestinal broad flatworm (Diphyllobothrium latum), compared to their fish host (Oncorhynchus mykiss) measured by total reflection X-ray fluorescence spectrometry. Spectrochimica Acta Part B 63, 14501454.*Google Scholar
Wright, J. (2010) Biomonitoring with aquatic benthic macroinvertebrates in southern Costa Rica in support of community based watershed monitoring. MSc Thesis, York University, Ontario, Canada.Google Scholar
Wunderlich, A.C., Silva, R.J., Zica, E.O.P., Parente, T.E.M. & Vidal-Martínez, V.M. (2014) Can parasites and EROD activity in fish indicate environmental impact in tropical/subtropical reservoirs? The 89th Annual Meeting of the American Society of Parasitologists, New Orleans, Louisiana, 24–27 July 2014.*Google Scholar