Bot fly parasitism in mantled howler monkeys (Alouatta palliata): General patterns and climate influences.
Cuterebra
Los Tuxtlas
climate windows
host‐parasite dynamics
oestrids
Journal
American journal of primatology
ISSN: 1098-2345
Titre abrégé: Am J Primatol
Pays: United States
ID NLM: 8108949
Informations de publication
Date de publication:
27 Aug 2024
27 Aug 2024
Historique:
revised:
17
06
2024
received:
25
02
2024
accepted:
14
08
2024
medline:
28
8
2024
pubmed:
28
8
2024
entrez:
28
8
2024
Statut:
aheadofprint
Résumé
Parasitism is a strong selective pressure, and its study is crucial for predicting the persistence of host species. Mantled howler monkeys are infected by the larvae of the bot fly Cuterebra baeri. This parasitosis produces myiasis and may have negative impacts on host health, although systematic information on the dynamics of this host-parasite relationship is very limited. Currently, all available information on infection patterns of C. baeri comes from a single mantled howler monkey population (Barro Colorado Island, Panama). Therefore, in this study we describe temporal variation in infection patterns for a newly mantled howler monkey population and analyze the relationship between climate and infection likelihood. We assessed the presence of C. baeri nodules in 17 adult individuals in Los Tuxtlas for 10 months through direct observation and compiled data on ambient temperature and rainfall. Most subjects had nodules during the study and there were no differences between sexes in the number of nodules. Nodules were usually located in the neck. Prevalence and abundance of nodules peaked thrice during the study (February, April, and September), a pattern that was very similar to that of parasitism intensity (February, April, and August). Incidence closely tracked these peaks, increasing before and decreasing after them. The likelihood of nodule appearance increased when both mean and minimum temperature decreased in the 24-21 prior days to nodule appearance. It also increased with decreased rainfall in the 5-2 prior days to nodule appearance. Although only three of the eight analyzed climate variables had a significant effect on parasitosis, these results suggest that climate may affect pupal development and the access of larvae to hosts. Besides contributing data on C. baeri parasitism for a new mantled howler monkey population, our study provides novel information on the influence of environmental factors on the dynamics of host-parasite systems.
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
e23680Subventions
Organisme : Leakey Foundation
Organisme : Consejo Nacional de Humanidades, Ciencias y Tecnologías
ID : 1147976
Informations de copyright
© 2024 Wiley Periodicals LLC.
Références
Altizer, S., Dobson, A., Hosseini, P., Hudson, P., Pascual, M., & Rohani, P. (2006). Seasonality and the dynamics of infectious diseases. Ecology Letters, 9, 467–484. https://doi.org/10.1111/j.1461-0248.2005.00879.x
Anderson, R. M., & May, R. M. (1979). Population biology of infectious diseases: Part I. Nature, 280, 361–367. https://doi.org/10.1038/280361a0
Bailey, L. D., & van de Pol, M. (2016). Climwin: An R toolbox for climate window analysis. PLoS One, 11, e0167980. https://doi.org/10.1371/journal.pone.0167980
Balcells, C. D., & Vea, J. J. V. (2009). Developmental stages in the howler monkey, subspecies Alouatta palliata mexicana: a new classification using age‐sex categories. Neotropical Primates, 16, 1–8. https://doi.org/10.1896/044.016.0101
Baron, R. W., Colwell, D. D., & Milton, K. (1996). Antibody immunoglobulin G (IgG) response to Alouattamyia baeri (Diptera: Cuterebridae) parasitism of howler monkeys, Alouatta palliata, in Panama. Journal of Medical Entomology, 33, 946–951. https://doi.org/10.1093/jmedent/33.6.946
Breev, K. A., Zagretdinov, R. G., & Minár, J. (1980). Influence of constant and variable temperatures on pupal development of the sheep bot fly (Oestrus ovis L.). Folia Parasitologica, 27, 359–365.
Burnham, K. P., & Anderson, D. R. (2002). Model selection and multimodel inference. Springer.
Bush, A. O., Fernández, J. C., Esch, G. W., & Seed, J. R. (2001). Parasitism: The diversity and ecology of animal parasites. Cambridge University Press.
Calderón‐Arguedas, O., Troyo, A., Solano, M. E., Sánchez, R., Chinchilla, M., & Gutiérrez‐Espeleta, G. A. (2004). Infección por larvas de Alouattamyia baeri (Diptera: Cuterebridae) en monos aulladores, Alouatta palliata (Primates: Cebidae) de la Costa Caribe de Costa Rica. Neotropical Primates, 12, 21–24.
Catts, E. P. (1982). Biology of new world bot flies: Cuterebridae. Annual Review of Entomology, 27, 313–338. https://doi.org/10.1146/annurev.en.27.010182.001525
Cepeda‐Palacios, R., & Scholl, P. J. (2000). Factors affecting the larvipositional activity of Oestrus ovis gravid females (Diptera: Oestridae). Veterinary Parasitology, 91, 93–105. https://doi.org/10.1016/s0304-4017(00)00265-x
Colwell, D. D., Baird, C. R., Lee, B., & Milton, K. (1999). Scanning electron microscopy and comparative morphometrics of eggs from six bot fly species (Diptera: Oestridae). Journal of Medical Entomology, 36, 803–810. https://doi.org/10.1093/jmedent/36.6.803
Colwell, D. D., & Milton, K. (1998). Development of Alouattamyia baeri (Diptera: Oestridae) from howler monkeys (Primates: Cebidae) on Barro Colorado island, Panama. Journal of Medical Entomology, 35, 674–680. https://doi.org/10.1093/jmedent/35.5.674
Cristóbal‐Azkarate, J., Dunn, J. C., Domingo Balcells, C., & Veà Baró, J. (2017). A demographic history of a population of howler monkeys (Alouatta palliata) living in a fragmented landscape in Mexico. PeerJ, 5, e3547. https://doi.org/10.7717/peerj.3547
Cristóbal‐Azkarate, J., Colwell, D. D., Kenny, D., Solórzano, B., Shedden, A., Cassaigne, I., & Luna, E. R. (2012). First report of bot fly (Cuterebra baeri) infestation in howler monkeys (Alouatta palliata) from Mexico. Journal of Wildlife Diseases, 48, 822–825. https://doi.org/10.7589/0090-3558-48.3.822
Dias, P. A. D., Coyohua‐Fuentes, A., Canales‐Espinosa, D., & Rangel‐Negrín, A. (2023). Demography and life‐history parameters of mantled Howler monkeys at La flor de Catemaco: 20 years post‐translocation. Primates, 64, 143–152. https://doi.org/10.1007/s10329-022-01030-z
Dunn, L. H. (1934). Entomological investigations in the Chiriqui region of Panama. Psyche: A Journal of Entomology, 41, 166–183. https://doi.org/10.1155/1934/21960
Eisen, R. J., Eisen, L., Ogden, N. H., & Beard, C. B. (2016). Linkages of weather and climate with Ixodes scapularis and Ixodes pacificus (Acari: Ixodidae), enzootic transmission of Borrelia burgdorferi, and lyme disease in North America. Journal of Medical Entomology, 53, 250–261. https://doi.org/10.1093/jme/tjv199
Esperon‐Rodriguez, M., Beaumont, L. J., Lenoir, J., Baumgartner, J. B., McGowan, J., Correa‐Metrio, A., & Camac, J. S. (2019). Climate change threatens the most biodiverse regions of Mexico. Biological Conservation, 240:108215. https://doi.org/10.1016/j.biocon.2019.108215
Fraiha, H., Lopes Chaves, L. C., Borges, I. C., & Barros de Freitas, R. (1984). Miíases humanas na Amazônia—III: miíase pulmonar por Alouattamyia baeri (Shannon & Greene, 1926) (Diptera, Cuterebridae). Revista da Fundação Serviço de Saúde Pública, 29, 63–68.
Goater, T. M., Goater, C. P., & Esch, G. W. (2014). Parasitism: The diversity and ecology of animal parasites (2da ed). Cambridge University Press.
Gorrell, J. C., & Schulte‐Hostedde, A. I. (2008). Patterns of parasitism and body size in red squirrels (Tamiasciurus hudsonicus). Canadian Journal of Zoology, 86, 99–107. https://doi.org/10.1139/Z07-123
Guimarães, J. H. (1971). Notes on the hosts of Neotropical Cuterebrini (Diptera, Cuterebridae), with new records from Brazil. Papéis Avulsos de Zoologia, 25, 89–94.
Guimarães, J. H., & Coimbra, Jr., C. E. A. (1982). Miíase humana por Alouattamyia baeri (Shannon & Greene) (Diptera, Cuterebridae). Comunicação de dois casos na região norte do Brasil. Revista Brasileira de Zoologia, 1, 35–39. https://doi.org/10.1590/S0101-81751982000100005
Harvell, C. D., Mitchell, C. E., Ward, J. R., Altizer, S., Dobson, A. P., Ostfeld, R. S., & Samuel, M. D. (2002). Climate warming and disease risks for terrestrial and marine biota. Science, 296, 2158–2162. https://doi.org/10.1126/science.1063699
Hatcher, M. J., Dick, J. T. A., & Dunn, A. M. (2006). How parasites affect interactions between competitors and predators. Ecology Letters, 9, 1253–1271. https://doi.org/10.1111/j.1461-0248.2006.00964.x
Heeb, P., Kölliker, M., & Richner, H. (2000). Brid‐ectoparasite interactions, nest humidity, and ectoparasite community structure. Ecology, 81, 958–968. https://doi.org/10.1890/0012-9658(2000)081[0958:beinha]2.0.co;2
Hopkins, M. E., & Milton, K. (2016). Adverse effects of ball‐chain radio‐collars on female mantled howlers (Alouatta palliata) in Panama. International Journal of Primatology, 37, 213–224. https://doi.org/10.1007/s10764-016-9896-y
Margolis, L., Esch, G. W., Holmes, J. C., Kuris, A. M., & Schad, G. A. (1982). The use of ecological terms in parasitology (Report of an Ad Hoc Committee of the American Society of Parasitologists). The Journal of Parasitology, 68, 131–133. https://doi.org/10.2307/3281335
Milton, K. (1980). The foraging strategy of howler monkeys: A study of primate economics. Columbia University Press.
Milton, K. (1996). Effects of bot fly (Alouattamyia baeri) parasitism on a free‐ranging howler monkey (Alouatta palliata) population in Panama. Journal of Zoology, 239, 39–63. https://doi.org/10.1111/j.1469-7998.1996.tb05435.x
Moyer, B. R., Drown, D. M., & Clayton, D. H. (2002). Low humidity reduces ectoparasite pressure: Implications for host life history evolution. Oikos, 97, 223–228. https://doi.org/10.1034/j.1600-0706.2002.970208.x
Needham, G. R., & Teel, P. D. (1991). Off‐host physiological ecology of Ixodid ticks. Annual Review of Entomology, 36, 659–681. https://doi.org/10.1146/annurev.en.36.010191.003303
Nilssen, A. C. (1997). Effect of temperature on pupal development and eclosion dates in the reindeer oestrids Hypoderma tarandi and Cephenemyia trompe (Diptera: Oestridae). Environmental Entomology, 26, 296–306. https://doi.org/10.1093/ee/26.2.296
Oda, F. H., Kitagawa, C., Noronha, J. D. C., Rodrigues, D. D. J., Martins, T. F., Valadão, M. C., Carvalho, L. M., & Campos, A. K. (2018). Amblyomma tick species infesting amphibians and reptiles in the seasonally dry Amazon forest, with new host records for Amblyomma rotundatum (Acari: Ixodida: Ixodidae). Systematic and Applied Acarology, 23, 387–392. https://doi.org/10.11158/saa.23.2.14
Ogden, N. H., & Lindsay, L. R. (2016). Effects of climate and climate change on vectors and vector‐borne diseases: Ticks are different. Trends In Parasitology, 32, 646–656. https://doi.org/10.1016/j.pt.2016.04.015
Oorebeek, M., & Kleindorfer, S. (2008). Climate or host availability: What determines the seasonal abundance of ticks? Parasitology Research, 103, 871–875. https://doi.org/10.1007/s00436-008-1071-8
Oorebeek, M., & Kleindorfer, S. (2009). The prevalence and intensity of tick infestation in passerines from South Australia. Emu ‐ Austral Ornithology, 109, 121–125. https://doi.org/10.1071/MU08052
van de Pol, M., Bailey, L. D., McLean, N., Rijsdijk, L., Lawson, C. R., & Brouwer, L. (2016). Identifying the best climatic predictors in ecology and evolution. Methods in Ecology and Evolution, 7, 1246–1257. https://doi.org/10.1111/2041-210X.12590
Poulin, R. (2006). Global warming and temperature‐mediated increases in cercarial emergence in trematode parasites. Parasitology, 132, 143–151. https://doi.org/10.1017/S0031182005008693
R Core Team. (2024). R: A language and environment for statistical computing. R Foundation for Statistical Computing. R Core Team. https://www.R-project.org/
Rangel‐Negrín, A., Coyohua‐Fuentes, A., de la Torre Herrera, A., Cano‐Huertes, B., Reynoso‐Cruz, E., Ceccarelli, E., Gómez‐Espinosa, E. E., Chavira‐Ramírez, D. R., Moreno‐Espinoza, D. E., Canales‐Espinosa, D., Maya‐Lastra, N., Cruz‐Miros, P., Cañadas‐Santiago, S., Garau, S., & Dias, P. A. D. (2021). Female reproductive energetics in mantled howler monkeys (Alouatta palliata): A follow‐up study. American Journal of Physical Anthropology, 174, 396–406. https://doi.org/10.1002/ajpa.24222
Robar, N., Burness, G., & Murray, D. L. (2010). Tropics, trophics and taxonomy: The determinants of parasite‐associated host mortality. Oikos, 119, 1273–1280. https://doi.org/10.1111/j.1600-0706.2009.18292.x
Roberts, L. S., Janovy, Jr., J., & Nadler, S. (2013). Gerald D. Schmidt & Larry S. Roberts’ foundations of parasitology (9th ed). McGraw‐Hill.
Rondón, S., Cavallero, S., Link, A., De Meo, M., González, C., & D'Amelio, S. (2023). Cuterebra baeri infecting grey‐legged night monkeys (Aotus griseimembra) and red howler monkeys (Alouatta seniculus) in Colombia. Journal of Wildlife Diseases, 59, 181–185. https://doi.org/10.7589/JWD-D-22-00062
Sánchez, C. A., Becker, D. J., Teitelbaum, C. S., Barriga, P., Brown, L. M., Majewska, A. A., Hall, R. J., & Altizer, S. (2018). On the relationship between body condition and parasite infection in wildlife: A review and meta‐analysis. Ecology Letters, 21, 1869–1884. https://doi.org/10.1111/ele.13160
Schwanz, L. E. (2008). Chronic parasitic infection alters reproductive output in deer mice. Behavioral Ecology and Sociobiology, 62, 1351–1358. https://doi.org/10.1007/s00265-008-0563-y
Sher, A., & Coffman, R. L. (1992). Regulation of immunity to parasites by T‐cells and T‐cell derived cytokines. Annual Review of Immunology, 10, 385–409. https://doi.org/10.1146/annurev.iy.10.040192.002125
Solórzano‐García, B., & Pérez‐Ponce de León, G. (2018). Parasites of neotropical primates: A review. International Journal of Primatology, 39, 155–182. https://doi.org/10.1007/s10764-018-0031-0
Soto, M., & Gama, L. (1997). Climas. In R. Vogt, E. Gónzalez‐Soriano, & R. Dirzo (Eds.), Historia natural de Los Tuxtlas (pp. 7–25). UNAM.
Stromberg, B. E. (1997). Environmental factors influencing transmission. Veterinary Parasitology, 72, 247–264. https://doi.org/10.1016/s0304-4017(97)00100-3
de Thoisy, B., Vogel, I., Reynes, J.‐M., Pouliquen, J.‐F., Carme, B., Kazanji, M., & Vié, J.‐C. (2001). Health evaluation of translocated free‐ranging primates in French Guiana. American Journal of Primatology, 54, 1–16. https://doi.org/10.1002/ajp.1008
Treves, A., & Carlson, A. E. (2012). Botfly parasitism and tourism on the endangered black howler monkey of Belize. Journal of Medical Primatology, 41, 284–287. https://doi.org/10.1111/j.1600-0684.2012.00549.x
Vilchez‐Delgado, F., Ramírez‐Montano, L. F., Merino‐Merino, X., Ojeda‐Juárez, R. R., Espinoza‐Román, M. H., & Duarte‐Quiroga, A. (2022). Botfly parasitism on two primates of the Cebidae family in Peru. Journal of Wildlife Diseases, 58, 415–420. https://doi.org/10.7589/JWD-D-21-00175
Zeledón, R., Otto Jiménez, Q., & Brenes, R. R. (1957). Cuterebra baeri Shannon y Greene, 1926 en el mono aullador de Costa Rica. Revista de biología tropical, 5, 129–134.
Zumpt, F. (1965). Myasis in man and animals in the old world: A textbook for physicians, veterinarians, and zoologists. Butterworths.