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.

Energetic constraints on the reproduction of female mantled howlers

“…Additionally, although glucocorticoids have been linked to energy expenditure in this population (Dias et al, ), which was further confirmed in this study by their negative correlation with thyroid hormone levels, they are also associated with other factors, such as social challenges. Participation in agonistic interactions and glucocorticoid levels have been found to co‐vary in this and in other howler monkey species (Dias et al, ; Gómez‐Espinosa et al, ; Rangel‐Negrín, Coyohua‐Fuentes, Chavira‐Ramírez, Canales‐Espinosa & Dias, ). Therefore, variation in female exposure to psychosocial challenges could account for some of the observed variation in both conception probabilities and IBI.…”

Maternal glucocorticoid levels affect sex allocation in black howler monkeys

“…Previous research indicated that the glucocorticoid levels of howler monkeys could be affected by energetic and psychosocial stressors (Crist obal-Azkarate et al, 2007;Dunn et al, 2013;G omez-Espinosa et al, 2014), as well as by living in either extensive or fragmented forests (Mart ınez- Mota et al, 2007;Rangel-Negr ın et al, 2014b). We therefore modeled variation in maternal glucocorticoids as a function of habitat type (females in five groups in extensive vs. females in five groups in fragmented forests), the amount of time spent traveling (a proxy for energetic stress), and participation in agonistic social interactions (a proxy for psychosocial stress).…”

“…The glucocorticoid levels of howler monkeys are generally higher in fragmented than in extensive forests as a consequence of low food availability, high anthropogenic pressures and both high feeding and reproductive competition (Crist obal- Azkarate et al, 2007;Mart ınez-Mota et al, 2007;Dunn et al, 2013;G omez-Espinosa et al, 2014;Rangel-Negr ın et al, 2014b). Therefore, glucocorticoid elevation in forest fragments signals a myriad of adverse environmental conditions that may have negative consequences for infant survival, and as a consequence, female reproductive success (Dias et al, 2015a(Dias et al, , 2016.…”

Validation of an enzyme immunoassay and comparison of fecal cortisol metabolite levels in black and gold howler monkeys (Alouatta caraya) inhabiting fragmented and continuous areas of the humid Chaco region, Argentina

“…In general, anthropogenic changes to primate habitats impact primate populations by changing the availability, density, abundance, and distribution of plant species (Milich, Stumpf, Chambers, & Chapman, ) which in turn, can trigger a physiological stress response reflected in higher cortisol levels (e.g., Alouatta pigra (Arroyo‐Rodriguez & Dias, ; Martínez‐Mota, Valdespino, Sánchez‐Ramos, & Serio‐Silva, ), Piliocolobus tephrosceles (Chapman, Saj, & Snaith, ), L. catta (Cavigelli, ), P. troglodytes (Muller & Wrangham, ), Papio anubis (Sapolsky, )). For arboreal primates like howler monkeys, the potential stressors include terrestrial locomotion (an atypical situation that may increase susceptibility to predation) or increased human presence in the fragment (Rangel‐Negrín, Coyohua‐Fuentes, Chavira, Canales‐Espinosa, & Dias, ).…”