Where and what? Frugivory is associated with more efficient foraging in three semi-free ranging primate species

Abstract

Foraging in seasonal environments can be cognitively challenging. Comparative studies have associated brain size with a frugivorous diet. We investigated how fruit distribution ( where ) and preference ( what ) affect foraging decisions in three semi-free ranging primate species with different degrees of frugivory: Macaca tonkeana ( N indiv = 5; N trials = 430), M. fascicularis ( N indiv = 3; N trials = 168) and Sapajus apella ( N indiv = 6; N trials = 288). We used 36 boxes fixed on trees and filled with highly and less preferred fruits with different (weekly) spatio-temporal distributions. Individuals were tested in two conditions: (1) same fruit provided concurrently in the same quantity but in a scattered and in a clumped distribution, (2) highly preferred fruit was scattered while the less preferred was clumped. Generally, primates preferred feeding first on the boxes of the clumped distribution in both conditions, with the more frugivorous species at a higher degree than the less frugivorous species in condition (1), but not (2). Therefore, what fruit was available changed the foraging decisions of the more frugivorous species who also engaged more in goal-directed travel. When feeding on preferred fruit, primates probably maximized foraging efficiency regardless of their degree of frugivory. Our findings emphasize that the food type and distribution may be a preponderant driver in cognitive evolution.

Linking ecology and cognition: does ecological specialisation predict cognitive test performance?

“…Interspecific differences in cognitive performance have been reported as a function of variation in ranging behaviour and search strategies (Teichroeb and Vining 2019;Trapanese et al 2019), foraging activity (Day et al 1999a;Day et al 2003;Jones et al 2017), foraging techniques (Day et al 2003), characteristics of preferred dietary items (Pleskacheva et al 2000;Henry and Stoner 2011;Teichroeb and Vining 2019), adaptations to habitat complexity (Pleskacheva et al 2000;Clarin et al 2013;White and Brown 2015a) or adaptations to seasonality (Cristol et al 2003; Barkley and Jacobs 2007;Henry and Stoner 2011) (Fig. 2).…”

“…At least in birds, rodents and primates, there is evidence that the evolution of spatial memory abilities parallels a species-specific foraging ecology. Better spatial cognition has been reported for species feeding on dispersed items of rather unpredictable abundance (Platt et al 1996;Pleskacheva et al 2000;Rosati and Hare 2012;Clarin et al 2013), frugivorous species (Rosati et al 2014;Teichroeb and Vining 2019;Trapanese et al 2019), scatter hoarders (Barkley and Jacobs 2007) or migrating species (Cristol et al 2003). In such cases, better-adapted species evolve greater hippocampi as an adaptation to the highly demanding ecological challenge of memorising previous food locations or caches.…”

Do primates flexibly use spatio-temporal cues when foraging?

“…In capuchins, naïve subjects twice visited Non-baited Fake boxes, which seems to support the hypothesis of a bias due to our experimental protocol. However, the fact that naïve subjects visited Non-baited boxes along the way to baited boxes as much as the non-naïve subjects, it seems plausible that those mistakes were simply the results of their opportunistic foraging strategy as also seen in another study (Trapanese et al, 2019). Naïve long-tailed macaques never made mistakes when choosing the first three boxes at the unexpected seasonal changes showing that likely they were using the information provided by the new temporal cues, rather than basing their foraging decisions on the notyet acquired knowledge of the position of the majority of the Real boxes.…”

“…Most of the time, the visited Non-baited Real boxes were those opportunistically found close to the baited boxes or along the path to find them. This was particularly true for capuchin monkeys; being more insectivorous than macaques, they may profit more from visiting multiple close feeding sites or revisiting the same feeding sites because invertebrates are generally more randomly distributed than fruit (Teichroeb & Vining, 2019;Trapanese et al, 2019). In our previous studies, we showed that the capuchin monkeys displayed less goal-directed movements towards resources and had higher revisiting rates of the feeding sites than the other two more frugivorous study species (Tonkean and long-tailed macaques; Trapanese et al, 2019, under review).…”

“…Primates may use abstract mental representations to acquire, store, and decode spatial, temporal, and ecological information (i.e., cognitive maps; O' Keefe & Nadel, 1978;Poucet, 1993). Studies on captive and wild primates revealed that several species seem to remember where resources are, generally optimising their travel during foraging (e.g., Janmaat et al, 2006;Noser & Byrne, 2013;Valero & Byrne, 2007;Trapanese et al, 2019). Several different studies investigated the role played by what and where variables in primate spatial foraging strategies (e.g., De Lillo et al, 1997;Janson, 1998;Trapanese et al, 2019, under review), but information about the when component is still largely lacking (Trapanese et al, 2018).…”