The cost of living in larger primate groups includes higher fly densities

EcoHealth - Tập 19 - Trang 290-298 - 2022
Jan F. Gogarten1,2,3, Mueena Jahan1,4, Sébastien Calvignac-Spencer1,2, Colin A. Chapman5,6,7, Tony L. Goldberg8, Fabian H. Leendertz1,9, Jessica M. Rothman10
1Epidemiology of Highly Pathogenic Organisms, Robert Koch Institute, Berlin, Germany
2Viral Evolution, Robert Koch Institute, Berlin, Germany
3Applied Zoology and Nature Conservation, University of Greifswald, Greifswald, Germany
4Department of Microbiology and Public Health, Bangabandhu Sheikh Mujibur Rahman Agricultural University, Gazipur, Bangladesh
5Center for the Advanced Study of Human Paleobiology, George Washington University, Washington, USA
6School of Life Sciences, University of KwaZulu-Natal, Pietermaritzburg, South Africa
7Shaanxi Key Laboratory for Animal Conservation, Northwest University, Xi’an, China
8Department of Pathobiological Sciences, University of Wisconsin-Madison, Madison, USA
9Helmholtz Institute for One Health, Greifswald, Germany
10Department of Anthropology, Hunter College, City University of New York, New York, USA

Tóm tắt

Flies are implicated in carrying and mechanically transmitting many primate pathogens. We investigated how fly associations vary across six monkey species (Cercopithecus ascanius, Cercopithecus mitis, Colobus guereza, Lophocebus albigena, Papio anubis, and Piliocolobus tephrosceles) and whether monkey group size impacts fly densities. Fly densities were generally higher inside groups than outside them, and considering data from these primate species together revealed that larger groups harbored more flies. Within species, this pattern was strongest for colobine monkeys, and we speculate this might be due to their smaller home ranges, suggesting that movement patterns may influence fly–primate associations. Fly associations increase with group sizes and may thus represent a cost to sociality.

Tài liệu tham khảo

Adenusi AA, Adewoga TO (2013) Studies on the potential and public health importance of non-biting synanthropic flies in the mechanical transmission of human enterohelminths. Transactions of the Royal Society of Tropical Medicine and Hygiene 107:812–818 Baker M (1996) Fur rubbing: use of medicinal plants by capuchin monkeys (Cebus capucinus). American Journal of Primatology 38:263–270 Blackburn JK, Van Ert M, Mullins JC, Hadfield TL, Hugh-Jones ME (2014) The necrophagous fly anthrax transmission pathway: empirical and genetic evidence from wildlife epizootics. Vector-Borne and Zoonotic Diseases 14:576–583 Braverman I, Dano I, Saah D, Gapany B (1994) Aural myiasis caused by flesh fly larva, Sarcophaga haemorrhoidalis. The Journal of Otolaryngology 23:204–205 Calibeo-Hayes D, Denning SS, Stringham S, Guy JS, Smith LG, Watson DW (2003) Mechanical transmission of turkey coronavirus by domestic houseflies (Musca domestica Linnaeaus). Avian Diseases 47:149–153 Clavel A, Doiz O, Morales S, Varea M, Seral C, Castillo FJ, Fleta J, Rubio C, Gómez-Lus R (2002) House fly (Musca domestica) as a transport vector of Cryptosporidium parvum. Folia Parasitologica 49:163–164 Davies C, Ayres J, Dye C, Deane L (1991) Malaria infection rate of Amazonian primates increases with body weight and group size. Functional Ecology 87:655–662 Dudley R, Milton K (1990) Parasite deterrence and the energetic costs of slapping in howler monkeys, Alouatta palliata. Journal of Mammalogy 71:463–465 Forsey T, Darougar S (1981) Transmission of chlamydiae by the housefly. British Journal of Ophthalmology 65:147–150 Francesconi F, Lupi O (2012) Myiasis. Clinical Microbiology Reviews 25:79–105 Freeland W (1976) Pathogens and the evolution of primate sociality. Biotropica 8:12–24 Gogarten JF, Düx A, Mubemba B, Pléh K, Hoffmann C, Mielke A, Müller-Tiburtius J, Sachse A, Wittig RM, Calvignac-Spencer S, Leendertz FH (2019) Tropical rainforest flies carrying pathogens form stable associations with social nonhuman primates. Molecular Ecology 28:4242–4258 Gogarten JF, Jacob AL, Ghai RR, Rothman JM, Twinomugisha D, Wasserman MD, Chapman CA (2015) Group size dynamics over 15+ years in an African forest primate community. Biotropica 47:101–112 Graczyk TK, Knight R, Gilman RH, Cranfield MR (2001) The role of non-biting flies in the epidemiology of human infectious diseases. Microbes and Infection 3:231–235 Greenberg B (1971) Flies and disease. Ecology, Classification and Biotic Associations 87:815 Griffin RH, Nunn CL (2012) Community structure and the spread of infectious disease in primate social networks. Evolutionary Ecology 26:779–800 Hoffmann C, Zimmermann F, Biek R, Kuehl H, Nowak K, Mundry R, Agbor A, Angedakin S, Arandjelovic M, Blankenburg A, Brazolla G, Corogenes K, Couacy-Hymann E, Deschner T, Dieguez P, Dierks K, Düx A, Dupke S, Eshuis H, Formenty P, Ginath Yuh Y, Gogarten JF, Goedmakers A, Granjon A, McGraw S, Grunow R, Hart J, Jones S, Junker J, Kiang J, Langergraber K, Lapuente J, Lee K, Leendertz SAJ, Leinert V, Löhrich T, Marrocoli S, Mätz-Rensing K, Meier A, Merkel K, Metzger S, Murai M, De Nys HM, Sachse A, Schenk S, van Schijndel J, Thiesen U, Ton E, Wieler LH, Boesch C, Klee SR, Wittig RM, Calvignac-Spencer S, Leendertz FH (2017) Persistent anthrax as a major driver of wildlife mortality in a tropical rainforest. Nature 548:82–86 Jusino MA, Banik MT, Palmer JM, Wray AK, Xiao L, Pelton E, Barber JR, Kawahara AY, Gratton C, Peery MZ, Lindner DL (2019) An improved method for utilizing high-throughput amplicon sequencing to determine the diets of insectivorous animals. Molecular Ecology Resources 19:176–190 Krebs BL, Anderson TK, Goldberg TL, Hamer GL, Kitron UD, Newman CM, Ruiz MO, Walker ED, Brawn JD (2014) Host group formation decreases exposure to vector-borne disease: a field experiment in a ‘hotspot’ of West Nile virus transmission. Proceedings of the Royal Society b: Biological Sciences 281:20141586 Kumm HW, Turner TB (1936) The transmission of yaws from man to rabbits by an insect vector, Hippelates pallipes Loew. American Journal of Tropical Medicine 16:968 Lindsay SW, Lindsay TC, Duprez J, Hall MJ, Kwambana BA, Jawara M, Nurudeen IU, Sallah N, Wyatt N, D’Alessandro U (2012) Chrysomya putoria, a putative vector of diarrheal diseases. PLoS Neglected Tropical Diseases 6:e1895 MacKinnon J (1974) The behaviour and ecology of wild orang-utans (Pongo pygmaeus). Animal Behaviour 22:3–74 Manlove KR, Cassirer EF, Cross PC, Plowright RK, Hudson PJ (2014) Costs and benefits of group living with disease: a case study of pneumonia in bighorn lambs (Ovis canadensis). Proceedings of the Royal Society b: Biological Sciences 281:20142331 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 Milton K, May ML (1976) Body weight, diet and home range area in primates. Nature 259:459–462 Nunn CL, Altizer S, Jones KE, Sechrest W (2003) Comparative tests of parasite species richness in primates. The American Naturalist 162:597–614 Nunn CL, Heymann EW (2005) Malaria infection and host behavior: a comparative study of Neotropical primates. Behavioral Ecology and Sociobiology 59:30–37 Oksanen, J., F. G. Blanchet, M. Friendly, R. Kindt, P. Legendre, D. McGlinn, P. R. Minchin, R. O’Hara, G. Simpson, P. Solymos, M. H. H. Stevens, E. Szoecs, and H. Wagner. 2020. vegan: Community Ecology Package. R package version 2.5–7. Porter TM, Hajibabaei M (2018) Automated high throughput animal CO1 metabarcode classification. Scientific Reports 8:1–10 R Core Team. 2021. R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. URL https://www.R-project.org/. Steelman CD (1976) Effects of external and internal arthropod parasites on domestic livestock production. Annual Review of Entomology 21:155–178 Tella JL (2002) The evolutionary transition to coloniality promotes higher blood parasitism in birds. Journal of Evolutionary Biology 15:32–41 van Schaik CP, Kappeler PM (1997) Infanticide risk and the evolution of male–female association in primates. Proceedings of the Royal Society of London Series B: Biological Sciences 264:1687–1694 Wang Q, Garrity GM, Tiedje JM, Cole JR (2007) Naive Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Applied and Environmental Microbiology 73:5261–5267 Weldon PJ, Aldrich JR, Klun JA, Oliver JE, Debboun M (2003) Benzoquinones from millipedes deter mosquitoes and elicit self-anointing in capuchin monkeys (Cebus spp.). Naturwissenschaften 90:301–304 White MA, Whiley H, Ross KE (2019) A review of Strongyloides spp. environmental sources worldwide. Pathogens 8:91