Vultures as an overlooked model in cognitive ecology.

Despite important recent advances in cognitive ecology, our current understanding of avian cognition still largely rests on research conducted on a few model taxa. Vultures are an ecologically distinctive group of species by being the only obligate carrion consumers across terrestrial vertebrates. Their unique scavenging lifestyle suggests they have been subject to particular selective pressures to locate scarce, unpredictable, ephemeral, and nutritionally challenging food. However, substantial variation exists among species in diet, foraging techniques and social structure of populations. Here, we provide an overview of the current knowledge on vulture cognition through a comprehensive literature review and a compilation of our own observations. We find evidence for a variety of innovative foraging behaviors, scrounging tactics, collective problem-solving abilities and tool-use, skills that are considered indicative of enhanced cognition and that bear clear connections with the eco-social lifestyles of species. However, we also find that the cognitive basis of these skills remain insufficiently studied, and identify new research areas that require further attention in the future. Despite these knowledge gaps and the challenges of working with such large animals, we conclude that vultures may provide fresh insight into our knowledge of the ecology and evolution of cognition.

Mandrills learn two-day time intervals in a naturalistic foraging situation.

Primates display high efficiency in finding food in complex environments. Knowledge that many plant species produce fruit simultaneously, can help primates to anticipate fruit finding at the start of fruiting seasons. Knowledge of elapsed time can help primates decide when to revisit food trees to find ripened fruit and to return before competitors find these fruits. To investigate whether mandrills are able to learn time intervals of recurring food, we recorded the foraging choices of captive mandrills in a group setting. We used a procedure with renewable food rewards that could be searched for: carrots and grapes, hidden underground in specific places with different renewal intervals (2 and 5 days, respectively). We monitored the first choice of location for individuals, if other individuals had not already searched at the same location, to exclude possible effects of individuals following others rather than relying on memory. Throughout the study, the mandrills became increasingly likely to first search at carrot locations on carrot days, while the probability of them searching at carrot locations decreased on days without carrot. Due to model instability, our results were inconclusive about an effect of grape days on the choice of the mandrills. Cues provided by conspecifics indicating the availability of simultaneously emerging food rewards did not affect the choice of the mandrills. We conclude that mandrills can take into account elapsed time in a foraging context. Thereby, this study indicates how mandrills can use temporal cognitive abilities to overcome temporal challenges of food-finding in a group setting.

Cuttlefish show flexible and future-dependent foraging cognition.

Some animals optimize their foraging activity by learning and memorizing food availability, in terms of quantity and quality, and adapt their feeding behaviour accordingly. Here, we investigated whether cuttlefish flexibly adapt their foraging behaviour according to the availability of their preferred prey. In Experiment 1, cuttlefish switched from a selective to an opportunistic foraging strategy (or vice versa) when the availability of their preferred prey at night was predictable versus unpredictable. In Experiment 2, cuttlefish exhibited day-to-day foraging flexibility, in response to experiencing changes in the proximate future (i.e. preferred prey available on alternate nights). In Experiment 1, the number of crabs eaten during the day decreased when shrimp (i.e. preferred food) were predictably available at night, while the consumption of crabs during the day was maintained when shrimp availability was unpredictable. Cuttlefish quickly shifted from one strategy to the other, when experimental conditions were reversed. In Experiment 2, cuttlefish only reduced their consumption of crabs during the daytime when shrimps were predictably available the following night. Their daytime foraging behaviour appeared dependent on shrimps' future availability. Overall, cuttlefish can adopt dynamic and flexible foraging behaviours including selective, opportunistic and future-dependent strategies, in response to changing foraging conditions.

Learned valuation during forage decision-making in cuttlefish.

Decision-making, when humans and other animals choose between two options, is not always based on the absolute values of the options but can also depend on their relative values. The present study examines whether decision-making by cuttlefish is dependent on relative values learned from previous experience. Cuttlefish preferred a larger quantity when making a choice between one or two shrimps (1 versus 2) during a two-alternative forced choice. However, after cuttlefish were primed under conditions where they were given a small reward for choosing one shrimp in a no shrimp versus one shrimp test (0 versus 1) six times in a row, they chose one shrimp significantly more frequently in the 1 versus 2 test. This reversed preference for a smaller quantity was not due to satiation at the time of decision-making, as cuttlefish fed a small shrimp six times without any choice test prior to the experiment still preferred two shrimps significantly more often in a subsequent 1 versus 2 test. This suggests that the preference of one shrimp in the quantity comparison test occurs via a process of learned valuation. Foraging preference in cuttlefish thus depends on the relative value of previous prey choices.

Spatio-temporal complexity of chimpanzee food: How cognitive adaptations can counteract the ephemeral nature of ripe fruit.

Ecological complexity has been proposed to play a crucial role in primate brain-size evolution. However, detailed quantification of ecological complexity is still limited. Here we assess the spatio-temporal distribution of tropical fruits and young leaves, two primary chimpanzee (Pan troglodytes) foods, focusing on the predictability of their availability in individual trees. Using up to 20 years of information on monthly availability of young leaf, unripe and ripe fruit in plant species consumed by chimpanzees from tropical forests in East, Central, and West Africa, we estimated: (1) the forest-wide frequency of occurrence of each food type and (2) the predictability of finding ripe fruit-bearing trees, focusing on the timing, frequency, and amount of ripe fruit present. In all three forests, at least half of all encountered trees belonged to species that chimpanzees were known to feed on. However, the proportion of these trees bearing young leaves and fruit fluctuated widely between months. Ripe fruit was the most ephemeral food source, and trees that had more than half of their crown filled were at least nine times scarcer than other trees. In old growth forests only one large ripe fruit crop was on average encountered per 10 km. High levels of inter-individual variation in the number of months that fruit was present existed, and in some extreme cases individuals bore ripe fruit more than seven times as often as conspecifics. Some species showed substantially less variation in such ripe fruit production frequencies and fruit quantity than others. We hypothesize that chimpanzees employ a suite of cognitive mechanisms, including abilities to: (1) generalize or classify food trees; (2) remember the relative metrics of quantity and frequency of fruit production across years; and (3) flexibly plan return times to feeding trees to optimize high-energy food consumption in individual trees, and efficient travel between them. Am. J. Primatol. 78:626-645, 2016. © 2016 Wiley Periodicals, Inc.

Mantled howler monkey spatial foraging decisions reflect spatial and temporal knowledge of resource distributions.

An animal's ability to find and relocate food items is directly related to its survival and reproductive success. This study evaluates how mantled howler monkeys make spatial foraging decisions in the wild. Specifically, discrete choice models and agent-based simulations are used to test whether mantled howler monkeys on Barro Colorado Island, Panama, integrate spatial information in order to maximize new leaf flush and fruit gain while minimizing distance traveled. Several heuristic models of decision making are also tested as possible alternative strategies (movement to core home range areas instead of individual trees, travel along a sensory gradient, movement along arboreal pathway networks without a predetermined destination, straight-line travel in a randomly chosen direction, and random walks). Results indicate that although leaves are the single most abundant item in the mantled howler monkey diet, long-distance travel bouts target the areas with the highest concentrations of mature fruits. Observed travel patterns yielded larger estimated quantities of fruit in shorter distances traveled than all alternative foraging strategies. Thus, this study both provides novel information regarding how primates select travel paths and suggests that a highly folivorous primate integrates knowledge of spatiotemporal resource distributions in highly efficient foraging strategies.