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The impact of botfly parasitism on the health of the gracile mouse opossum (Gracilinanus agilis)

Published online by Cambridge University Press:  27 March 2019

Priscilla Lóra Zangrandi
Affiliation:
Departamento de Ecologia, Laboratório de Ecologia de Vertebrados, Instituto de Ciências Biológicas, Universidade de Brasília, Brasília, Distrito Federal 70919-900, Brazil
André Faria Mendonça
Affiliation:
Departamento de Ecologia, Laboratório de Ecologia de Vertebrados, Instituto de Ciências Biológicas, Universidade de Brasília, Brasília, Distrito Federal 70919-900, Brazil
Ariovaldo Pereira Cruz-Neto
Affiliation:
Instituto de Biociências de Rio Claro, Universidade Estadual Paulista Júlio de Mesquita Filho, Avenida 24A 1515 Bela Vista, 13506-900, Rio Claro, São Paulo, Brazil
Rudy Boonstra
Affiliation:
Department of Biological Sciences, Centre for the Neurobiology of Stress, University of Toronto Scarborough, MIC 1A4, Toronto, Canada
Emerson M. Vieira*
Affiliation:
Departamento de Ecologia, Laboratório de Ecologia de Vertebrados, Instituto de Ciências Biológicas, Universidade de Brasília, Brasília, Distrito Federal 70919-900, Brazil
*
Author for correspondence: Emerson M. Vieira, E-mail: [email protected]

Abstract

Fragmented habitats generally harbour small populations that are potentially more prone to local extinctions caused by biotic factors such as parasites. We evaluated the effects of botflies (Cuterebra apicalis) on naturally fragmented populations of the gracile mouse opossum (Gracilinanus agilis). We examined how sex, food supplementation experiment, season and daily climatic variables affected body condition and haemoglobin concentration in animals that were parasitized or not by botflies. Although parasitism did not affect body condition, haemoglobin concentrations were lower in parasitized animals. Among the non-parasitized individuals, haemoglobin concentration increased with the increase of maximum temperature and the decrease of relative humidity, a climatic pattern found at the peak of the dry season. However, among parasitized animals, the opposite relationship between haemoglobin concentration and relative humidity occurred, as a consequence of parasite-induced anaemia interacting with dehydration as an additional stressor. We conclude that it is critical to assess how climate affects animal health (through blood parameters) to understand the population consequences of parasitism on the survival of individuals and hence of small population viability.

Type
Research Article
Copyright
Copyright © Cambridge University Press 2019 

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References

Allan, BF, Keesing, F and Ostfeld, RS (2003) Effect of forest fragmentation on Lyme disease risk. Conservation Biology 17, 267272.Google Scholar
Andreazzi, CS, Rademaker, V, Gentile, R, Herrera, HM, Jansen, AM and D'Andrea, PS (2011) Population ecology of small rodents and marsupials in a semi-deciduous tropical forest of the southeast Pantanal, Brazil. Zoologia 28, 762770.Google Scholar
Aragona, M and Marinho-Filho, J (2009) História natural e biologia reprodutiva de marsupiais no Pantanal, Mato Grosso, Brasil. Zoologia 26, 220230.Google Scholar
Bartoń, K (2018) MuMIn: multi-model inference. R package version 1.42.1.Google Scholar
Bates, D, Maechler, M, Bolker, B and Walker, S (2015) Fitting linear mixed-effects models using lme4. Journal of Statistical Software 67, 148.Google Scholar
Becker, DJ, Streicker, DG and Altizer, S (2018) Using host species traits to understand the consequences of resource provisioning for host–parasite interactions. Journal of Animal Ecology 87, 511525.Google Scholar
Bennett, GF (1973) Some effects of Cuterebra emasculator Fitch (Diptera: Cuterebridae) on the blood and activity of its host, the eastern chipmunk. Journal of Wildlife Diseases 9, 8593.Google Scholar
Bergallo, HG, Martins-Hatano, F, Juca, N and Gettinger, D (2000) The effect of botfly parasitism of Metacuterebra apicalis (Diptera) on reproduction, survival and general health of Oryzomys russatus (Rodentia), in Southeastern Brazil. Mammalia 64, 439446.Google Scholar
Bocchiglieri, A, Mendonça, AF and Campos, JJB (2010) Diet composition of Gracilinanus agilis (Didelphimorphia, Didelphidae) in dry woodland areas of Cerrado in central Brazil. Mammalia 74, 225227.Google Scholar
Boonstra, R, Krebs, CJ and Beacham, T (1980) Impact of botfly parasitism on Microtus townsendii populations. Canadian Journal of Zoology 58, 16831692.Google Scholar
Bossi, DEP and Bergallo, HG (1992) Parasitism by cuterebrid botflies (Metacuterebra apicalis) in Oryzomys nitidus (Rodentia: Cricetidae) and Metachirus nudicaudatus (Marsupialia: Didelphidae) in a southeastern Brazilian rain forest. Journal of Parasitology 78, 142145.Google Scholar
Boutin, S (1990) Food supplementation experiments with terrestrial vertebrates: patterns, problems, and the future. Canadian Journal of Zoology 68, 203220.Google Scholar
Breiman, L (2001) Random forests. Machine Learning 45, 532.Google Scholar
Buffenstein, R, Maloney, SK and Bronner, GN (1999) Seasonal and daily variation in blood and urine concentrations of free-ranging Angolan free-tailed bats (Mops condylurus) in hot roosts in Southern Africa. South African Journal of Zoology 34, 1118.Google Scholar
Burnham, KP and Anderson, DR (2002) Model Selection and Multimodel Inference: A Practical Information-Theoretic Approach, 2nd Edn. New York, USA: Springer-Verlag.Google Scholar
Burns, CE, Goodwin, BJ and Ostfeld, RS (2005) A prescription for longer life? Bot fly parasitism of the white-footed mouse. Ecology 86, 753761.Google Scholar
Bustamante, M, Nardoto, G, Pinto, A, Resende, J, Takahashi, F and Vieira, L (2012) Potential impacts of climate change on biogeochemical functioning of Cerrado ecosystems. Brazilian Journal of Biology 72, 655671.Google Scholar
Calle, ML and Urrea, V (2010) Letter to the editor: stability of Random Forest importance measures. Briefings in Bioinformatics 12, 8689.Google Scholar
Camargo, NF, Ribeiro, JF, Camargo, AJA and Vieira, EM (2014) Diet of the gracile mouse opossum Gracilinanus agilis (Didelphimorphia: Didelphidae) in a neotropical savanna: intraspecific variation and resource selection. Acta Theriologica 59, 183191.Google Scholar
Campbell, TW (2015) Exotic Animal Hematology and Cytology, 4th Edn. Hoboken, USA: Wiley-Blackwell.Google Scholar
Cansi, ER (2011a) Caracterização das miíases em animais nas cidades de Brasília (Distrito Federal) e Formosa (Goiás) (PhD thesis). Universidade de Brasília, Brasília, Brazil.Google Scholar
Cansi, ER (2011b) Registro de miíase por Cuterebra apicalis em cão doméstico na região Central do Brasil. Acta Scientiae Veterinariae 39, 14.Google Scholar
Catts, EP (1982) Biology of New World bot flies: Cuterebridae. Annual Review of Entomology 27, 313338.Google Scholar
Clark, P (2004) Haematology of Australian Mammals. Collingwood, Australia: CSIRO Publishing.Google Scholar
Clark, BK and Kaufman, DW (1990) Prevalence of botfly (Cuterebra sp.) parasitism in populations of small mammals in eastern Kansas. The American Midland Naturalist 124, 2230.Google Scholar
Colwell, DD (2001) Bot flies and warble flies (Order Diptera: Family Oestridae). In Samuel, WM, Pybus, MJ and Kocan, AA (eds), Parasitic Diseases of Wild Mammals. Ames, USA: Iowa State University Press, pp. 4671.Google Scholar
Cooper, CE, Withers, PC and Cruz-Neto, AP (2009) Metabolic, ventilatory, and hygric physiology of the gracile mouse opossum (Gracilinanus agilis). Physiological and Biochemical Zoology 82, 153162.Google Scholar
Costa, LP, Leite, YL and Patton, JL (2003) Phylogeography and systematic notes on two species of gracile mouse opossums, genus Gracilinanus (marsupialia: Didelphidae) from Brazil. Proceedings of the Biological Society of Washington 116, 275292.Google Scholar
Cramer, MJ and Cameron, GN (2006) Effects of bot fly (Cuterebra fontinella) parasitism on a population of white-footed mice (Peromyscus leucopus). Journal of Mammalogy 87, 11031111.Google Scholar
Creighton, GK and Gardner, AL (2007) Genus gracilinanus. In Gardner, A (ed.) Mammals of South America. Vol. 1. Marsupials, Xenarthrans, Shrews, and Bats. Chicago, USA: The University of Chicago Press, pp. 4350. doi: 10.7208/chicago/9780226282428.001.0001.Google Scholar
Cutler, RD, Edwards, TC Jr, Beard, KH, Cutler, A, Hess, KT, Gibson, J and Lawler, JJ (2007) Random forests for classification in ecology. Ecology 88, 27832792.Google Scholar
Dai, A (2011) Drought under global warming: a review. Wiley Interdisciplinary Reviews: Climate Change 2, 4565.Google Scholar
De'ath, G and Fabricius, KE (2000) Classification and regression trees: a powerful yet simple technique for ecological data analysis. Ecology 81, 31783192.Google Scholar
Donohoe, C (2016) Fluid therapy. In Battaglia, AM and Steele, AM (eds), Small Animal Emergency and Critical Care for Veterinary Technicians. St. Louis, USA: Elsevier Inc., pp. 6177.Google Scholar
Dunaway, PB, Payne, JA, Lewis, LL and Story, J (1967) Incidence and effects of Cuterebra in Peromyscus. Journal of Mammalogy 48, 3851.Google Scholar
Eiten, G (1972) The cerrado vegetation of Brazil. The Botanical Review 38, 201338.Google Scholar
Evans, KD, Hewett, TA, Clayton, CJ, Krubitzer, LA and Griffey, SM (2010) Normal organ weights, serum chemistry, hematology, and cecal and nasopharyngeal bacterial cultures in the gray short-tailed opossum (Monodelphis domestica). Journal of the American Association for Laboratory Animal Science 49, 401406.Google Scholar
Everard, COR and Aitken, THG (1972) Cuterebrid flies from small mammals in Trinidad. Journal of Parasitology 58, 189190.Google Scholar
Fletcher, QE and Boonstra, R (2006) Impact of live trapping on the stress response of the meadow vole (Microtus pennsylvanicus). Journal of Zoology 270, 473478.Google Scholar
Forattini, OP and Lenko, K (1959) Nota biológica sobre Metacuterebra apicalis (Guérin, 1829/38) (Diptera, Cuterebridae). Arquivos da Faculdade de Higiene e Saúde Pública da Universidade de São Paulo 13, 155158.Google Scholar
Goertz, JW (1966) Incidence of warbles in some Oklahoma rodents. The American Midland Naturalist 75, 242245.Google Scholar
Golde, WT, Gollobin, P and Rodriguez, LL (2005) A rapid, simple, and humane method for submandibular bleeding of mice using a lancet. Lab Animal 34, 3943.Google Scholar
Guimarães, JH and Papavero, N (1999) Myiasis in Man and Animals in the Neotropical Region. Bibliographic Database. São Paulo, Brazil: Editora Plêiade/Fapesp.Google Scholar
Hoff, J (2000) Methods of blood collection in the mouse. Lab Animal 29, 4753.Google Scholar
Hunter, DM and Webster, JM (1973) Determination of the migratory route of botfly larvae, Cuterebra grisea (Diptera: Cuterebridae) in deermice. International Journal for Parasitology 3, 311316.Google Scholar
Hunter, DM and Webster, JM (1974) Effects of cuterebrid larval parasitism on deer-mouse metabolism. Canadian Journal of Zoology 52, 209217.Google Scholar
Hunter, DM, Sadleir, RMFS and Webster, JM (1972) Studies on the ecology of cuterebrid parasitism in deermice. Canadian Journal of Zoology 50, 2529.Google Scholar
Jaffe, G, Zegers, DA, Steele, MA and Merritt, JF (2005) Long-term patterns of botfly parasitism in Peromyscus maniculatus, P. leucopus, and Tamias striatus. Journal of Mammalogy 86, 3945.Google Scholar
Jakob, EM, Marshall, SD and Uetz, GW (1996) Estimating fitness: a comparison of body condition. Oikos 77, 6167.Google Scholar
Johnstone, CP, Lill, A and Reina, RD (2015) Use of erythrocyte indicators of health and condition in vertebrate ecophysiology: a review and appraisal. Biological Reviews 92, 150168.Google Scholar
Kottek, M, Grieser, J, Beck, C, Rudolf, B, Rubel, F, Centre, PC and Wetterdienst, D (2006) World map of the Köppen-Geiger climate classification updated. Meteorologische Zeitschrift 15, 259263.Google Scholar
Krebs, CJ (2011) Of lemmings and snowshoe hares: the ecology of northern Canada. Proceedings. Biological Sciences/The Royal Society 278, 481489.Google Scholar
Labocha, MK, Schutz, H and Hayes, JP (2014) Which body condition index is best? Oikos 123, 111119.Google Scholar
Led, JE, Colacelli, A, Boero, JJ and Colombo, EG (1976) Parasitismo por Cuterebra apicalis, Guerin 1829 (Insecta, Diptera, Cuterebridae) en rata (Rattus norvegicus). Analecta Veterinaria 6–8, 3537.Google Scholar
Leite, ACR and Williams, P (1988) The life cycle of Metacuterebra apicalis (Diptera: Cuterebridae). Memórias do Instituto Oswaldo Cruz 83, 485491.Google Scholar
Liaw, A and Wiener, M (2002) Classification and regression by randomForest. R News 2, 1822.Google Scholar
Linardi, PM (2012) Os ectoparasitos de marsupiais brasileiros. In Cáceres, NC (ed.) Os Marsupiais do Brasil: Biologia, Ecologia E Conservação. Campo Grande, Brazil: UFMS, pp. 129158.Google Scholar
Lopes, GP and Leiner, NO (2015) Semelparity in a population of Gracilinanus agilis (Didelphimorphia: Didelphidae) inhabiting the Brazilian cerrado. Mammalian Biology 80, 16.Google Scholar
Lynch, AM, Respess, M, Boll, AE, Bozych, M, Mcmichael, M, Fletcher, DJ, De Laforcade, AM and Rozanski, EA (2016) Hospital-acquired anemia in critically ill dogs and cats: a multi-institutional study. Journal of Veterinary Internal Medicine 30, 141146.Google Scholar
Macdonald, DW (1996) Dangerous liaisons and disease. Nature 379, 400401.Google Scholar
Martins, EG, Bonato, V, Da-Silva, CQ and Reis, SF (2006) Partial semelparity in the neotropical didelphid marsupial Gracilinanus microtarsus. Journal of Mammalogy 87, 915920.Google Scholar
Mello, DA (1978) Nota sobre a biologia de Cuterebra apicalis (Guérin, 1829/38) (Diptera-Cuterebridae). Revista Brasileira de Pesquisas Médicas e Biológicas 11, 329331.Google Scholar
Mendonça, AF, Armond, T, Camargo, ACL, Camargo, NF, Ribeiro, JF, Zangrandi, PL and Vieira, EM (2015) Effects of an extensive fire on arboreal small mammal populations in a neotropical savanna woodland. Journal of Mammalogy 96, 368379.Google Scholar
Mendonça, AF, Armond, T, Camargo, ACL, Zangrandi, PL and Vieira, EM (2017) Round-pot feeder: low-cost apparatus for field studies on food supplementation for arboreal small mammals. Mammalia 82, 6871.Google Scholar
Munger, JC and Karasov, WH (1991) Sublethal parasites in white-fooded mice: impacts on survival and reproduction. Canadian Journal of Zoology 69, 398404.Google Scholar
Nichols, LB (1994) The effect of bot fly (Cuterebra) infestation on cold-night trap mortality in cactus mice (Peromyscus eremicus). The Southwestern Naturalist 39, 383386.Google Scholar
Oliveira-Filho, A, Ratter, J and Flora, W (2002) Vegetation physiognomies and woody flora of the cerrado biome. In Oliveira, P and Marquis, R (eds), The Cerrados of Brazil. Ecology and Natural History of a Neotropical Savanna. New York, USA: Columbia University Press, pp. 91120.Google Scholar
Papavero, N and Guimarães, JH (2009) Catalogue of neotropical diptera. Cuterebridae. Neotropical Diptera 11, 117.Google Scholar
Peig, J and Green, AJ (2009) New perspectives for estimating body condition from mass/length data: the scaled mass index as an alternative method. Oikos 118, 18831891.Google Scholar
Peig, J and Green, AJ (2010) The paradigm of body condition: a critical reappraisal of current methods based on mass and length. Functional Ecology 24, 13231332.Google Scholar
Pinto, CM and Claps, GL (2005) First record of Cuterebra almeidai (Guimarães and Carrera) from Argentina, new host records for Cuterebra apicalis Guérin-Méneville, and list of Cuterebra (diptera: Oestridae) in the collection of the Instituto-Fundación Miguel Lillo. Proceedings of the Entomological Society of Washington 107, 572575.Google Scholar
Prevedello, JA, Dickman, CR, Vieira, MV and Vieira, EM (2013) Population responses of small mammals to food supply and predators: a global meta-analysis. Journal of Animal Ecology 82, 927936.Google Scholar
Prudhomme, C, Giuntoli, I, Robinson, EL, Clark, DB, Arnell, NW, Dankers, R, Fekete, BM, Franssen, W, Gerten, D, Gosling, SN, Hagemann, S, Hannah, DM, Kim, H, Masaki, Y, Satoh, Y, Stacke, T, Wada, Y and Wisser, D (2014) Hydrological droughts in the 21st century, hotspots and uncertainties from a global multimodel ensemble experiment. Proceedings of the National Academy of Sciences 111, 32623267.Google Scholar
Puida, DBC and Paglia, AP (2015) Primary productivity and the demography of Gracilinanus agilis, a small semelparous marsupial. Journal of Mammalogy 96, 221229.Google Scholar
Pujol-Luz, J, Mendonça, A and Henriques, R (2004) Registro de Gracilinanus agilis (Marsupialia, Didelphidae) parasitado por Metacuterebra apicalis (Diptera, Cuterebridae) no Cerrado de Brasília, Distrito Federal, Brasil. Entomología y Vectores 11, 669672.Google Scholar
Püttker, T, Meyer-Lucht, Y and Sommer, S (2008) Effects of fragmentation on parasite burden (nematodes) of generalist and specialist small mammal species in secondary forest fragments of the coastal Atlantic Forest, Brazil. Ecological Research 23, 207215.Google Scholar
R Core Team (2017) R: A Language and Environment for Statistical Computing. Vienna, Austria: R Foundation for Statistical Computing.Google Scholar
Schulte-Hostedde, AI, Millar, JS and Hickling, GJ (2001) Evaluating body condition in small mammals. Canadian Journal of Zoology 79, 10211029.Google Scholar
Sealander, JA (1961) Hematological values in deer mice in relation to botfly infection. Journal of Mammalogy 42, 5760.Google Scholar
Silverstein, D and Campbell, J (2012) Fluid therapy. In Tobias, KM and Johnston, SA (eds), Veterinary Surgery: Small Animal. St. Louis, USA: Saunders, pp. 4372.Google Scholar
Slansky, F (2007) Insect/mammal associations: effects of cuterebrid bot fly parasites on their hosts. Annual Review of Entomology 52, 1736.Google Scholar
Smith, DH (1977) The natural history and development of Cuterebra approximata (Diptera: Cuterebridae) in its natural host, Peromyscus maniculatus (Rodentia: Cricetidae), in western Montana. Journal of Medical Entomology 14, 137145.Google Scholar
Smith, DH (1978) Effects of bot fly (Cuterebra) parasitism on activity patterns of Peromyscus maniculatus in the laboratory. Journal of Wildlife Diseases 14, 2839.Google Scholar
Spessot, MLG, Gomez, D and Priotto, JW (2013) Demographic responses of Akodon azarae (Rodentia: Cricetidae) enclosed populations to Rogenhofera bonaerensis bot fly parasitism. Mastozoología Neotropical 20, 387392.Google Scholar
Thrall, MA (2012) Classification of and diagnostic approach to anemia. In Thrall, MA, Weiser, G, Allison, RW and Campbell, TW (eds), Veterinary Hematology and Clinical Chemistry, 2nd Edn. Oxford, UK: Wiley-Blackwell, pp. 7580.Google Scholar
Tompkins, DM and Begon, M (1999) Parasites can regulate wildlife populations. Parasitology Today 15, 311313.Google Scholar
Twigg, GI (1965) Warbles on Holochilus sciureus from the Coast of British Guiana. Journal of Mammalogy 24, 98100.Google Scholar
Vieira, EM (1993) Occurrence and prevalence of bot flies, Metacuterebra apicalis (Diptera: Cuterebridae), in rodents of cerrado from central Brazil. Journal of Parasitology 79, 792795.Google Scholar
Vieira, EM, Camargo, NF, Colas, PF, Ribeiro, JF and Cruz-Neto, AP (2017) Geographic variation in daily temporal activity patterns of a neotropical marsupial (Gracilinanus agilis). PLoS ONE 12, e0168495.Google Scholar
Watson, MJ (2013) What drives population-level effects of parasites? Meta-analysis meets life-history. International Journal for Parasitology: Parasites and Wildlife 2, 190196.Google Scholar
Wecker, SC (1962) The effects of bot fly parasitism on a local population of the white-footed mouse. Ecology 43, 561565.Google Scholar
Wilder, SM, Raubenheimer, D and Simpson, SJ (2016) Moving beyond body condition indices as an estimate of fitness in ecological and evolutionary studies. Functional Ecology 30, 108115.Google Scholar
Zuleta, GA and Vignau, ML (1990) Bot fly parasitism (Rogenhofera bonaerensis) (Diptera, Cuterebridae) in the pampean grassland mouse (Akodon azarae), in Argentina. Journal of Wildlife Diseases 26, 1117.Google Scholar
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