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

  • V.M. Vidal-Martínez (a1) and A.C. Wunderlich (a2)


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.


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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.*
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.*
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.*
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.
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.*
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.*
Caquet, T., Lagadic, L. & Sheffield, S.R. (2000) Mesocosms in ecotoxicology (1): outdoor aquatic systems. Reviews of Environmental Contamination and Toxicology 165, 138.
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., *
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.
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.*
Cohen, J. (1988) Statistical power analysis for the behavioral sciences. 2nd edn. 567 pp. Hillsdale, NJ, Lawrence Erlbaum Associates.
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.*
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.
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.
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.*
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.*
Hedges, L.V., Gurevitch, J. & Curtis, P.S. (1999) The meta-analysis of response ratios in experimental ecology. Ecology 80, 11501156.
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.
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.
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.
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.
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.
Kuris, A.M. (1980) Hosts as islands. American Naturalist 116, 570586.
Lafferty, K.D. (1997) Environmental parasitology: what can parasites tell us about human impacts on the environment? Parasitology Today 13, 251255.
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.*
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.*
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.*
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.
Marcogliese, D.J. (2005) Parasites of the superorganism: Are they indicators of ecosystem health? International Journal of Parasitology 35, 705716.
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.
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.
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.
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.*
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.
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.
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.*
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.
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.*
Rosenberg, M.S., Adams, D.C. & Gurevitch, J. (2000) MetaWin: Statistical software for Meta-analysis V2. 128 pp. Sunderland, Massachusetts, Sinauer Associates.
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.
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.*
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.
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.*
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.*
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.*
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.*
Sures, B. (2003) Accumulation of heavy metals by intestinal helminths in fish: an overview and perspective. Parasitology 126, S53S60.
Sures, B. (2008) Environmental parasitology: interactions between parasites and pollutants in the aquatic environment. Parasite 15, 434438.
Sures, B., Slidell, R. & Taraschewski, H. (1999) Parasites as accumulation indicators of heavy metal pollution. Parasitology Today 15, 1621.
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.
Tellez, M. & Merchant, M. (2015) Biomonitoring heavy metal pollution using an aquatic apex predator, the American alligator, and its parasites. PLoS ONE 10, e0142522.
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.
Vidal-Martínez, V.M. (2007) Helminths and protozoans of aquatic organisms as bioindicators of chemical pollution. Parassitologia 49, 177184.
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.*
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.*
Vidal-Martínez, V.M., Pech, D., Sures, B., Poulin, R. & Purucker, T. (2010) Can parasites really reveal environmental impact? Trends in Parasitology 26, 4451.
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.
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.*
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.
Warwick, R.M. (1993). Environmental impact studies on marine communities: pragmatical considerations. Australian Journal of Ecology 18, 6380.
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.*
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.
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.*

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

  • V.M. Vidal-Martínez (a1) and A.C. Wunderlich (a2)


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