Necropsies disclose a low helminth parasite diversity in periurban howler monkeys

Abstract

Primate-parasite interactions are often investigated via coprological studies given ethical and conservation restrictions of collecting primate hosts. Yet, these studies are inadequate to recover adult helminths for taxonomic identification and to accurately assess their prevalence, intensity, abundance, and site of infection. Fresh carcasses found in anthropogenic landscapes come as informative and reliable alternatives. In this study, we identified the helminths of brown howler monkeys (Alouatta guariba clamitans) and their sites of infection, and measured their prevalence, intensity, and abundance of infection. We necropsied 18 adult males, 11 adult females, and 7 juvenile males that died in conflicts with the anthropogenic environment (domestic dog attacks, n = 11; electrocutions and road-kills, n = 10 each; unknown, n = 5) in periurban landscapes of southern Brazil between 2013 and 2019. We found three nematodes (Trypanoxyuris minutus, Dipetalonema gracile, and Parabronema bonnei) and one cestode (Bertiella cf. studeri), a diversity estimated to account for a sampling completeness of 99%. Prevalence ranged from 3% for P. bonnei to 100% for T. minutus. Mean abundance ranged from 2 (D. gracile and B. cf. studeri) to 55,116 (T. minutus) and mean intensity of infection ranged from 4 (B. cf. studeri) to 55,116 (T. minutus). Trypanoxyuris minutus sex ratio was strongly malebiased. The intensity of infection with T. minutus was higher in juvenile males and adult females than in adult males. The low parasite diversity and the helminths' mode of transmission are compatible with howlers' arboreality and folivorous-frugivorous diet. The howlers were not infected with soil-transmitted helminth parasites of humans and domestic animals on the ground and probably did not eat invertebrates to complement the diet. Given the lack of evidence of howler health problems, we suggest that the causes of death of the necropsied howlers are the major threats to the long-term conservation of the species at the study periurban landscapes.

Wildlife is imperiled in peri-urban landscapes: threats to arboreal mammals

“…This finding supports evidence that domestic and feral dogs regularly kill primates (e.g. Alouatta guariba clamitans:Buss, 2012;Bicca-Marques et al, 2020;Lopes et al, 2021; C. nigritus: Oliveira et al, 2008) and other terrestrial mammals (e.g.Buttler et al, 2004, Lacerda et al, 2009Home et al, 2017;Gatti et al, 2018). In the study regions, these attacks often occur when brown howler monkeys descend to the ground to access cultivated fruits in subsistence orchards guarded by domestic dogs(Buss 2012;Chaves and Bicca-Marques, 2017;Corrêa et al, 2018) or, when they cross roads, gardens or pastures to access another Atlantic Forest remnant (Óscar M. Chaves and João Claudio Godoy, personal observations).…”

“…Whenever possible, we frozen the brown howler monkey carcasses in the collection of biological material of CEPESBI in SC, and in the Laboratório de Primatologia or the Museu de Ciências e Tecnologia/PUCRS, or the Museu de Ciências Naturais (SEMA/RS) in RS. A subsample of carcasses from RS was necropsied in a study on the taxon's helminth parasite fauna (Lopes et al, 2021). Injured brown howler monkeys were rescued by local authorities, researchers, or volunteers, who, then, sent them to veterinarian hospitals/clinics or authorized wildlife rehabilitation centers.…”