Cognitive maps in the wild: revealing the use of metric information in black howler monkey route navigation

ABSTRACT When navigating, wild animals rely on internal representations of the external world – called ‘cognitive maps’ – to take movement decisions. Generally, flexible navigation is hypothesized to be supported by sophisticated spatial skills (i.e. Euclidean cognitive maps); however, constrained movements along habitual routes are the most commonly reported navigation strategy. Even though incorporating metric information (i.e. distances and angles between locations) in route-based cognitive maps would likely enhance an animal's navigation efficiency, there has been no evidence of this strategy reported for non-human animals to date. Here, we examined the properties of the cognitive map used by a wild population of primates by testing a series of cognitive hypotheses against spatially explicit movement simulations. We collected 3104 h of ranging and behavioural data on five groups of black howler monkeys (Alouatta pigra) at Palenque National Park, Mexico, from September 2016 through August 2017. We simulated correlated random walks mimicking the ranging behaviour of the study subjects and tested for differences between observed and simulated movement patterns. Our results indicated that black howler monkeys engaged in constrained movement patterns characterized by a high path recursion tendency, which limited their capacity to travel in straight lines and approach feeding trees from multiple directions. In addition, we found that the structure of observed route networks was more complex and efficient than simulated route networks, suggesting that black howler monkeys incorporate metric information into their cognitive map. Our findings not only expand the use of metric information during route navigation to non-human animals, but also highlight the importance of considering efficient route-based navigation as a cognitively demanding mechanism.

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

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.

Arboreal route navigation in a Neotropical mammal: energetic implications associated with tree monitoring and landscape attributes

Background Although navigating along a network of routes might constrain animal movement flexibility, it may be an energetically efficient strategy. Routinely using the same route allows for visually monitoring of food resources, which might reduce the cognitive load and as such facilitate the process of movement decision-making. Similarly, locating routes in areas that avoid costly landscape attributes will enhance their overall energy balance. In this study we determined the benefits of route navigation in an energy minimiser arboreal primate, the black howler monkey (Alouatta pigra). Methods We monitored five neighbouring groups of black howler monkeys at Palenque National Park, Mexico from September 2016 through August 2017. We recorded the location of the focal group every 20 m and mapped all travel paths to establish a route network (N = 1528 travel bouts). We constructed linear mixed models to assess the influence of food resource distribution (N = 931 trees) and landscape attributes (slope, elevation and presence of canopy gaps) on the location of routes within a route network. Results The number of food trees that fell within the visual detection distance from the route network was higher (mean: 156.1 ± SD 44.9) than randomly simulated locations (mean: 121.9 ± SD 46.4). Similarly, the number of food trees found within the monkey’s visual range per meter travelled increased, on overage, 0.35 ± SE 0.04 trees/m with increasing use of the route. In addition, route segments used at least twice were more likely to occur with increasing density of food resources and decreasing presence of canopy gaps. Route segments used at least four times were more likely to occur in elevated areas within the home ranges but only under conditions of reduced visual access to food resources. Conclusions Route navigation emerged as an efficient movement strategy in a group-living arboreal primate. Highly used route segments potentially increased visual access to food resources while avoiding energetically costly landscape features securing foraging success in a tropical rainforest.