Seabirds: studies with parasitofauna and potential indicator for environmental anthropogenic impacts

Andressa Maria Rorato Nascimento de Matos, Camila Domit, Ana Paula Frederico Rodrigues Loureiro Bracarense

Abstract


The aim of this review was to present the main anthropogenic threats to seabirds, a taxonomic group described as environmental sentinels, and the dynamics between parasites and hosts and their relationship with the health of the marine ecosystem. Coastal marine environments support various anthropogenic activities, exposing seabirds to multiple and synergistic environmental changes. These activities are considered negative to the maintenance of several seabird species, such as exposure to constant aquatic contaminants and fishing. In addition, parasitic and infectious diseases (viral, bacterial, and fungal) may also play an important role in maintaining some seabird populations. Some pathogenic organisms have public health importance and/or may indicate environmental quality. Host-parasite interaction may be positive, negative, or absent depending on some environmental factors potentially associated with degradation, as well as intrinsic factors of host or parasite. In addition, investigating aspects of seabird mortality also contributes to the constant population monitoring and understanding of the interaction between animals, humans, and the environment. Thus, seabirds and their parasitofauna can provide important ecological and health information, including those related to environmental health, supporting strategies for reducing degradation and maintaining marine ecosystems.

Keywords


Environment; Host-parasite interaction; Parasite; Threats.

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References


Abollo, E., Gestal, C., & Pascual, S. (2001). Anisakid infection in the European shag Phalacrocorax aristotelis aristotelis. Journal of Helminthology, 75(3), 209-214. doi: 10.1079/JOH200051

Amato, J. F. R., & Amato, S. B. (2010). Técnicas gerais para coleta e preparação de helmintos endoparasitos de aves. In S. Von Matter, F. C. Straube, V. de Queiroz Piacentini, I. A. Accordi, & J. J. F. Cândido (Eds.), Ornitologia e conservação: ciência aplicada, técnicas de pesquisa e levantamento (pp. 369-393). Rio de Janeiro, RJ: Technical Books.

Barbieri, E. (2009). Occurrence of plastic particles in procellariiforms, south of Sao Paulo State (Brazil). Brazilian Archives of Biology and Technology, 52(2), 341-348. doi: 10.1590/S1516-89132009000200011

Barnes, D. K., Galgani, F., Thompson, R. C., & Barlaz, M. (2009). Accumulation and fragmentation of plastic debris in global environments. Philosophical Transactions of the Royal Society of London B: Biological Sciences, 364(1526), 1985-1998. doi: 10.1098/rstb.2008.0205

Brandão, M. L., Moreira, J., & Luque, J. L. (2014). Checklist of Platyhelminthes, Acanthocephala, Nematoda and Arthropoda parasitizing penguins of the world. Check List, 10(3), 562-573. doi: 10.1007/s11230-013-9410-2

Bueno, M. G., Lopez, R. P. G., Menezes, R. M. T. de, Jesus Costa-Nascimento, M. de, Castro Lima, G. F. M. de, Sousa Araújo, R. A. de,... Kirchgatter, K. (2010). Identification of Plasmodium relictum causing mortality in penguins (Spheniscus magellanicus) from São Paulo Zoo, Brazil. Veterinary Parasitology, 173(1-2), 123-127. doi: 10.1016/j.vetpar.2010.06.026

Burger, J., & Gochfeld, M. (2004). Marine birds as sentinels of environmental pollution. Ecohealth, 1(3), 263-274. doi: 10.1007/s10393-004-0096-4

Burgos-Núñez, S., Navarro-Frómeta, A., Marrugo-Negrete, J., Enamorado-Montes, G., & Urango-Cárdenas, I. (2017). Polycyclic aromatic hydrocarbons and heavy metals in the Cispata Bay, Colombia: A marine tropical ecosystem. Marine Pollution Bulletin, 120(1-2), 379-386. doi: 10.1016/j.marpolbul.2017.05.016

Camphuysen, C. J., & Van Franeker, J. A. (1992). The value of beached bird surveys in monitoring marine oil pollution. Zeist: Technisch Rapport Vogelbescherming 10. Retrieved from https://www.researchgate.net/profile/Jan_Van_Franeker/publication/287490289_The_value_of_beached_bird_surveys_in_monitoring_marine_oil_pollution/links/5a647d08a6fdccb61c55cbec/The-value-of-beached-bird-surveys-in-monitoring-marine-oil-pollution.pdf

Colabuono, F. I., Taniguchi, S., & Montone, R. C. (2012). Organochlorine contaminants in albatrosses and petrels during migration in South Atlantic Ocean. Chemosphere, 6(7), 701-708. doi: 10.1016/j.chemosphere.2011.10.043

Eiras, J. C. (1994). Platelminta. In Elementos de Ictioparasitologia (pp. 147-169). Porto: Fundação Eng Antonio de Almeida.

Freitas, J. F. T. (1955). Sobre dois trematódeos parasitos de aves: Philophthalmus lachrymosus Braun, 1902 e Renicola mirandaribeiroi n. sp. Arquivos do Museu Nacional, 32(42), 585-610. Retrieved from http://www.museunacional.ufrj.br/publicacoes/wp-content/arquivos/Arqs%20v%2042-II%20p%20585-610%20Tremat%c3%b3deos%20parasitos%20de%20aves.pdf

Furness, R. W. (2003). Impacts of fisheries on seabird communities. Scientia Marina, 67(S2), 33-45. doi: 10.3989/scimar.2003.67s233

Galaktionov, K. V. (1996). Impact of seabird helminths on host populations and coastal ecosystems. Bulletin of the Scandinavian Society of Parasitology, 6(2), 50-64. Retrieved from http://sbsp.eu/images/PDF/Bulletin_SBSP/Old/SSP_Bulletin_1996_Vol_6_No_2.pdf#page=60

Gómez, A., & Nichols, E. (2013). Neglected wild life: parasitic biodiversity as a conservation target. International Journal for Parasitology: Parasites and Wildlife, 2, 222-227. doi: 10.1016/j.ijppaw.2013.07.002

Gutiérrez, J. S., Rakhimberdiev, E., Piersma, T., & Thieltges, D. W. (2017). Migration and parasitism: habitat use, not migration distance, influences helminth species richness in Charadriiform birds. Journal of Biogeography, 44(5), 1137-1147. doi: 10.1111/jbi.12956

Hoberg, E. P. (1996). Faunal diversity among avian parasite assemblages: the interaction of history, ecology, and biogeography in marine systems. Bulletin of the Scandinavian Society for Parasitology, 6(2), 65-89. Retrieved from https://digitalcommons.unl.edu/parasitologyfacpubs/789/

Hoberg, E. P. (2005). Marine birds and their helminths parasites. In Rohde, K (Ed.), Marine Parasitology (pp. 414-425). Oxon: CABI Publishing.

Hubálek, Z. (2004). An annotated checklist of pathogenic microorganisms associated with migratory birds. Journal of Wildlife Diseases, 40(4), 639-659. doi: 10.7589/0090-3558-40.4.639

Instituto Chico Mendes de Conservação da Biodiversidade (2014). Aves marinhas e costeiras. Brasília: Author. Recuperado de http://www.icmbio.gov.br/portal/faunabrasileira/estado-de-conservacao/3632-aves-marinhas-e-costeiras

Instituto Chico Mendes de Conservação da Biodiversidade. (2016). Relatório anual de rotas e áreas de concentração de aves migratórias no Brasil. Brasília: Author. Recuperado de http://www.icmbio.gov.br/portal/images/stories/DCOM_Miolo_Rotas_Migrat%C3%B3rias_2016_final.pdf

Instituto Chico Mendes de Conservac?a?o da Biodiversidade. (2018). Livro Vermelho da fauna brasileira ameac?ada de extinc?a?o: volume III - aves. Brasi?lia: Author. Recuperado de http://www.icmbio.gov.br/portal/component/content/article/10187

Jerdy, H., Baldassin, P., Werneck, M. R., Bianchi, M., Ribeiro, R. B., & Carvalho, E. C. Q. (2016). First report of kidney lesions due to Renicola sp. (Digenea: Trematoda) in free-living Magellanic Penguins (Spheniscus magellanicus Forster, 1781) found on the coast of Brazil. Journal of Parasitology, 102(6), 650-652. doi: 10.1645/16-29

Khan, R. A. (1987). Crude oil and parasites of fish. Parasitology Today, 3(4), 99-100. doi: 10.1016/0169-4758(87)90043-3

Komar, N., & Clark, G. G. (2006). West Nile virus activity in Latin America and the Caribbean. Revista Panamericana de Salud Pública, 19(2), 112-117. doi: 10.1590/s1020-49892006000200006

Lafferty, K. D. (1997). Environmental parasitology: what can parasites tell us about human impacts on the environment? Parasitology Today, 13(7), 251-255. doi: 10.1016/S0169-4758(97)01072-7

Lafferty, K. D. (2013). Parasites in marine food webs. Bulletin of Marine Science, 89(1), 123-134. doi: 10.5343/bms.2011.1124

Lafferty, K. D., & Kuris, A. M. (1999). How environmental stress affects the impacts of parasites. Limnology and Oceanography, 44(3), 925-931. doi: 10.5343/bms.2011.1124

Leighton, F. A. (1986). Clinical, gross, and histological findings in herring gulls and Atlantic puffins that ingested Prudhoe Bay crude oil. Veterinary Pathology, 23(3), 254-263. doi: 10.1177/030098588602300305

Leighton, F. A. (1993). The toxicity of petroleum oils to birds. Environmental Reviews, 1(2), 92-103. doi: 10.1139/a93-008

Mackenzie, K. (2005). Parasites as biological tags. In Rohde, K (Ed.), Marine Parasitology (pp. 351-355). Oxon: CABI Publishing.

Mariani, D. B. (2016). Causas de encalhes de aves marinhas no nordeste do Brasil. Dissertação de mestrado, Universidade Federal Rural de Pernambuco, Recife, PE, Brasil. Recuperado de http://ww2.pgvet.ufrpe.br/sites/ww2.prppg.ufrpe.br/files/2016.dissertacao-daniela_bueno_mariani.pdf

Matos, A. M. R. N., Lavorente, F. L. P., Lorenzetti, E., Meira, M. R. C., Fº., Nóbrega, D. F., Chryssafidis, A. L.,... Bracarense, A. P. F. R. L. (2019). Molecular identification and histological aspects of Renicola sloanei (Digenea: Renicolidae) in Puffinus puffinus (Aves: Procellariiformes): a first record. Revista Brasileira de Parasitologia Veterinária, 28(3), 367-375. doi: 10.1590/S1984-29612019025

Munyer, P. D., & Holloway, H. L., Jr. (1990). Renicola williamsi n. sp. (Trematoda: Digenea: Renicolidae) from the south polar skua, Catharacta maccormiki. Transactions of the American Microscopical Society, 109(1), 98-102. doi: 10.2307/3226600

National Research Council (1991). Animals as sentinels of environmental health hazards. Washington, DC: The National Academy Press. Retrieved from https://www.ncbi.nlm.nih.gov/books/NBK234944/

Neves, D. P. (2009). Parasitologia dinâmica. 3nd ed. São Paulo: Atheneu.

Neves, T., Bugoni, L., & Rossi-Wongtschowski, C. L. D. B. (2006). Aves oceânicas e suas interações com a pesca na Região Sudeste-Sul do Brasil. Série Documentos Revizee: Score Sul. Recuperado de https://www.marinha.mil.br/secirm/sites/www.marinha.mil.br.secirm/files/documentos/revizee/score-sul-5.pdf

Organização das Nações Unidas (2019). Our planet is drowning in plastic pollution. Retrieved from: https://www.unenvironment.org/interactive/beat-plastic-pollution/

Pedersen, A. B., Jones, K. E., Nunn, C. L., & Altizer, S. (2007). Infectious diseases and extinction risk in wild mammals. Conservation Biology, 21(5), 1269-1279. doi: 10.1111/j.1523-1739.2007.00776.x

Penn, D. J. (2001). Coevolution: host-parasite. Trends in Genetics, 8, 213-219. doi: 10.1038/npg.els.0001765

Petróleo Brasileiro S.A. (2019). Projeto de monitoramento de praias. Recuperado de https://www.comunicabaciadesantos.com.br/programa-ambiental/projeto-de-monitoramento-de-praias-pmp.html

Petry, M. V., & Benemann, V. R. (2017). Ingestion of marine debris by the White-chinned Petrel (Procellaria aequinoctialis): is it increasing over time off southern Brazil? Marine Pollution Bulletin, 117(1-2), 131-135. doi: 10.1016/j.marpolbul.2017.01.073

Poulin, R., & Morand, S. (2000). The diversity of parasites. The Quarterly Review of Biology, 75(3), 277-293. doi: 10.1086/393500

Rohde, K. (2005). Economic and environmental importance. In Rohde, K (Ed.), Marine parasitology (pp.76-87). Oxon: CABI Publishing.

Schramm, C. C., Mascarenhas, C. S., Gastal, S. B., Scheer, S., Müller, G., & Robaldo, R. B. (2018). Acuariidae (Nematoda) in Procellariiformes (Aves) on the southern coast of Rio Grande do Sul, Brazil. Revista Brasileira de Parasitologia Veterinária, 27(1), 7-11. doi: 10.1590/s1984-29612017073

Serafini, P. P., & Lugarini, C. (2014). Procellariiformes e outras aves de ambientes marinhos (albatroz, petrel, fragata, atobá, biguá, gaivota). In Z. S. Cubas, J. C. R. Silva, & J. L. Catão-Dias (Eds.), Tratado de animais selvagens-medicina veterinária (2a ed., pp. 470-494). São Paulo: Editora Roca.

Sick, H. (1997). Ornitologia brasileira. Rio de Janeiro: Nova Fronteira.

Spotorno, B., Colabouno, F., Barquete, V., & Vooren, C. (2005). Lesiones causadas por nemátodeos en el proventrículo de procellariiformes en el litoral sur del Brasil. Anais do Congreso Latinoamericano de Ciencias del Mar, Viña del Mar, Chile, 11.

Sures, B. (2004). Environmental parasitology: relevancy of parasites in monitoring environmental pollution. Trends in Parasitology, 20(4), 170-177. doi: 10.1016/j.pt.2004.01.014

Sures, B. (2008). Host-parasite interactions in polluted environments. Journal of Fish Biology, 73(9), 2133-2142. doi: 10.1111/j.1095-8649.2008.02057.x

Sures, B., & Taraschewski, H. (1995). Cadmium concentrations in two adult acanthocephalans, Pomphorhynchus laevis and Acanthocephalus lucii, as compared with their fish hosts and cadmium and lead levels in larvae of A. lucii as compared with their crustacean host. Parasitology Research, 81(6), 494-497. doi: 10.1007/BF00931792

Sures, B., Taraschewski, H., & Jackwerth, E. (1994). Lead accumulation in Pomphorhynchus laevis and its host. Journal of Parasitology, 80(3), 355-357. doi: 10.2307/3283403

Tasker, M. L., Camphuysen, C. J., Cooper, J., Garthe, S., Montevecchi, W. A., & Blaber, S. J. (2000). The impacts of fishing on marine birds. ICES Journal of Marine Science, 57(3), 531-547. doi: doi:10.1006/jmsc.2000.00714

Thatcher, V. E. (1993). Trematódeos neotropicais. Manaus, AM: INPA.

Thieltges, D. W., Hussel, B., & Baekgaard, H. (2006). Endoparasites in common eiders Somateria mollissima from birds killed by an oil spill in the northern Wadden Sea. Journal of Sea Research, 55(4), 301-308. doi: 10.1016/j.seares.2005.12.001

Thomas, N. J., & Cole, R. A. (1996). The risk of disease and threats to the wild population. Endangered Species Update, 13(2), 24-28. Retrieved from https://pubs.er.usgs.gov/publication/1003893

Vanstreels, R. E. T., Silva, R. P., Fº., Kolesnikovas, C. K. M., Bhering, R. C. C., Ruoppolo, V., Epiphanio, S.,… Catão-Dias, J. L. (2015). Epidemiology and pathology of avian malaria in penguins undergoing rehabilitation in Brazil. Veterinary Research, 46(1), 30. doi: 10.1186/s13567-015-0160-9

Vanstreels, R. E., & Parson, N. J. (2014). Malária aviária e outros hemosporídeos aviários. In Z. S. Cubas, J. C. R. Silva, & J. L. Catão-Dias (Eds.), Tratado de animais selvagens-medicina veterinária (2a ed., pp. 1557-1574). São Paulo: Editora Roca.

Vidal-Martínez, V. M., Pech, D., Sures, B., Purucker, S. T., & Poulin, R. (2010). Can parasites really reveal environmental impact? Trends in Parasitology, 26(1), 44-51. doi: 10.1016/j.pt.2009.11.001

Vooren, C. M., & Brusque, L. F. (1999). As aves do ambiente costeiro do Brasil: biodiversidade e conservação. Rio Grande, RS: Fundação UFRG. Recuperado de http://rodadas.anp.gov.br/arquivos/Round7/arquivos_r7/PERFURACAO_R7/refere/Aves.pdf

Weinstein, S. B., & Lafferty, K. D. (2015). How do humans affect wildlife nematodes? Trends in Parasitology, 31(5), 222-227. doi: 10.1016/j.pt.2015.01.005

Wilcox, C., Van Sebille, E., & Hardesty, B. D. (2015). Threat of plastic pollution to seabirds is global, pervasive, and increasing. Proceedings of the National Academy of Sciences, 112(38), 11899-11904. doi: 10.1073/pnas.1502108112

Wood, C. L., Lafferty, K. D., & Micheli, F. (2010). Fishing out marine parasites? Impacts of fishing on rates of parasitism in the ocean. Ecology Letters, 13, 761-775. doi: 10.1111/j.1461-0248.2010.01467.x

Wright, C. A. (1954a). Trematodes of the genus Renicola from birds in British zoos, with descriptions of two new species. Proceedings of the Zoological Society of London, 124(1), 51-61. doi: 10.1111/j.1096-3642.1954.tb01477.x

Wright, C. A. (1954b). Trematodes of the genus Renicola from the kidneys of birds in Brazil. Revista Brasileira de Biologia, 14(1), 61-64.

Wright, S. L., Thompson, R. C., & Galloway, T. S. (2013). The physical impacts of microplastics on marine organisms: a review. Environmental Pollution, 178, 483-492. doi: 10.1016/j.envpol.2013.02.031

Yamashita, R., Takada, H., Nakazawa, A., Takahashi, A., Ito, M., Yamamoto, T.,… Watanuk, Y. (2018). Global monitoring of persistent organic pollutants (POPs) using seabird preen gland oil. Archives of environmental contamination and toxicology, 75(4), 545-556. doi: 10.1007/s00244-018-0557-3




DOI: http://dx.doi.org/10.5433/1679-0359.2020v41n4p1439

Semina: Ciênc. Agrár.
Londrina - PR
E-ISSN 1679-0359
DOI: 10.5433/1679-0359
E-mail: semina.agrarias@uel.br
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