Effects of variation in forest fragment habitat on black howler monkey demography in the unprotected landscape around Palenque National Park, Mexico

Abstract

Habitat loss and fragmentation are leading threats to biodiversity today, and primates are particularly vulnerable to anthropogenic habitat disturbance. However, few studies have examined how differential effects of variation in forest fragment characteristics on males and females in a primate population may affect demography and population persistence. We quantified the effects of variation in forest fragment characteristics on the within-fragment demography of black howler monkeys (Alouatta pigra) in forest fragments around Palenque National Park, Mexico, and how these effects differed between adult males and females. We quantified forest loss in the landscape between 2000 and 2017, and used a redundancy analysis to examine the effects of 15 variables quantifying fragment dimensions, forest composition and physical structure, and isolation on fragment population size and density, the proportion of adult males and females in the fragment population, and the mean number of adult males and females per group in 34 fragments (N = 393 monkeys). We hypothesized that (i) population size is positively correlated with fragment area, while population density is negatively correlated, and (ii) the composition of fragment populations results from differential effects of fragment variables on adult males and females. Forest cover decreased by 23.3% from 2000 to 2017. Our results showed a significant effect of fragment variables on population demography in fragments, accounting for 0.69 of the variance in the demographic response variables. Population size increased with fragment area and connectivity, while density decreased. Larger, less isolated fragments with better connectivity, characteristics indicative of abundant secondary growth, and those with more diverse vegetation but lower Simpson's evenness indices tended to have more adult females per group and a higher proportion of adult females in the population. In contrast, fragments that were largely similar in characteristics of forest composition and structure, but that were more isolated from nearby fragments, had more adult males per group and a higher proportion of adult males. These results may stem from black howler females preferentially remaining in natal groups and fragments when possible, and dispersing shorter distances when they disperse, while males may be more likely to disperse between fragments, traveling longer distances through the matrix to more isolated fragments. These differential effects on males and females have important conservation implications: if females are more abundant in larger, less isolated fragments, while males are more abundant in more isolated fragments, then to effectively conserve this population, both landscape connectivity and fragment areas should be maintained and increased.

Keywords: Alouatta pigra; Arboreal primate; Demography; Dispersal; Forest fragment habitat quality; Habitat loss and fragmentation; Landscape connectivity.

Figure 1. Map of study area.

(A) Map highlighting the core area of Palenque National Park (PNP), and the 34 study fragments located within 10 km of PNP. In white: fragment ID numbers; one fragment is not visible on the map due to its small size (fragment 49; 0.2 ha). White rectangle denotes area shown in greater detail in (B). Google Earth© 2018. (B) Enlarged section of study area highlighting different elements in the landscape: (1) oil palm plantation; (2) riparian corridors; (3) town; (4) forest fragments not included in this study; (5) pastureland matrix; (6) road. Google Earth© 2018. (C) Location of study site within Chiapas, Mexico, marked by red dot. Google Maps© 2018.

Figure 2. Photos detailing characteristics of the study fragments and their black howler monkey populations.

(A) Cattle grazing in typical pastureland matrix found around study fragments (photo credit: Keren Klass); (B) a group of black howlers in a mature, tall tree at the edge of a forest fragment (photo credit: Keren Klass); (C) stream running through an area of mainly secondary growth in a forest fragment, with a single extremely large, mature Ficus insipida tree on the right (photo credit: Keren Klass); (D) black howler monkeys using low barbed wire fencing to cross the matrix between two stands of trees (photo credit: Alvaro Campos Villanueva); (E) adult male carrying an infant in a Miconia argentea tree, a secondary growth species commonly found in the study fragments (photo credit: Keren Klass); (F) a forest fragment bordered by low secondary growth and cornfield matrix (photo credit: Keren Klass).

Figure 3. Forest loss and landscape connectivity in the study area.

Fragment ID numbers noted in black; one fragment (#49) not visible on the map due to its small size.

Figure 4. Heatmap of Spearman rank correlations among all explanatory and response variables.

Scale on the right denotes magnitude and direction of correlations among pairs of variables; white asterisks denote statistically significant correlations (p < 0.05). Definitions of abbreviated variable names: explanatory variables: area, fragment area; SI, shape index; stem.density, stem density; min.dbh, min. tree DBH; max.dbh, max. tree DBH; min.height, min. tree height; max.height, max. tree height; Shannon.I, Shannon’s index; Simpson.EI, Simpson’s evenness index; no.stump, number of stumps; ave.dbh.stump, mean DBH of stumps; isol.near.frag, distance to nearest fragment; isol.PNP, distance to PNP; no.treelines, number of treelines extending from fragment; forcov.buffer, proportion of forest cover in the buffer. Response variables: ave.grp.size, mean group size in fragment; tot.pop, total number of individuals per fragment; prop.AM, proportion of AM in the fragment population; prop.AF, proportion of AF in the fragment population; ave.AM.grp, mean number of AM per group in the fragment; ave.AF.grp, mean number of AF per group in the fragment; pop.density, fragment population density.

Figure 5. Triplot of RDA results: effects of fragment variables on black howler monkey population size, density and composition in forest fragments.

Proportion of variance in demographic data explained by each axis noted in parentheses in axis labels. For definitions of variable names, see Fig. 4.