Primates living outside protected habitats are more stressed: the case of black howler monkeys in the Yucatán Peninsula.

Abstract

The non-invasive monitoring of glucocorticoid hormones allows for the assessment of the physiological effects of anthropogenic disturbances on wildlife. Variation in glucocorticoid levels of the same species between protected and unprotect areas seldom has been measured, and the available evidence suggests that this relationship may depend on species-specific habitat requirements and biology. In the present study we focused on black howler monkeys (Alouatta pigra), a canopy-dwelling primate species, as a case study to evaluate the physiological consequences of living in unprotected areas, and relate them with intragroup competition and competition with extragroup individuals. From February 2006 to September 2007 we collected 371 fecal samples from 21 adults belonging to five groups (two from protected and three from unprotected areas) in Campeche, Mexico. We recorded agonistic interactions within groups and encounters with other groups (1,200 h of behavioral observations), and determined fecal glucocorticoid metabolite (FGM) concentrations with radioimmunoassays. We used linear mixed models and Akaike's information criterion to choose the best model explaining variation in FGM concentrations between protected and unprotected areas calculated from five categorical variables: habitat type (protected vs. unprotected), participation in agonistic interactions, intergroup encounters, sex and female reproductive state, and season. The best model included habitat type, the interaction between habitat type and agonism, and the interaction between habitat type and season. FGM concentrations were higher in unprotected habitats, particularly when individuals were involved in agonistic interactions; seasonal variation in FGM concentrations was only detected in protected habitats. High FGM concentrations in black howler monkeys living in unprotected habitats are associated with increased within-group food competition and probably associated with exposure to anthropogenic stressors and overall food scarcity. Because persistent high GC levels can be detrimental to health and fitness, populations living in disturbed unprotected areas may not be viable in the long-term.