Significance Measurements of daily energy expenditure indicate that primates, including humans, expend only half of the calories expected for mammals of similar body size. As energy expenditure is central to organismal biology, these results hold important implications for life history, evolutionary biology, and foraging ecology for primates and other mammals. Specifically, we show that primates’ remarkably low metabolic rates account for their distinctively slow rates of growth, reproduction, and aging. Humans and other primates are distinct among placental mammals in having exceptionally slow rates of growth, reproduction, and aging. Primates’ slow life history schedules are generally thought to reflect an evolved strategy of allocating energy away from growth and reproduction and toward somatic investment, particularly to the development and maintenance of large brains. Here we examine an alternative explanation: that primates’ slow life histories reflect low total energy expenditure (TEE) (kilocalories per day) relative to other placental mammals. We compared doubly labeled water measurements of TEE among 17 primate species with similar measures for other placental mammals. We found that primates use remarkably little energy each day, expending on average only 50% of the energy expected for a placental mammal of similar mass. Such large differences in TEE are not easily explained by differences in physical activity, and instead appear to reflect systemic metabolic adaptation for low energy expenditures in primates. Indeed, comparisons of wild and captive primate populations indicate similar levels of energy expenditure. Broad interspecific comparisons of growth, reproduction, and maximum life span indicate that primates’ slow metabolic rates contribute to their characteristically slow life histories.

Primate Energy Expenditure and Life History

Dropping is a common antipredator defence that enables rapid escape from a perceived threat. However, despite its immediate effectiveness in predator-prey encounters (and against other dangers such as a parasitoid or an aggressive conspecific), it remains an under-appreciated defence strategy in the scientific literature. Dropping has been recorded in a wide range of taxa, from primates to lizards, but has been studied most commonly in insects. Insects have been found to utilise dropping in response to both biotic and abiotic stimuli, sometimes dependent on mechanical or chemical cues. Whatever the trigger for dropping, the decision to drop by prey will present a range of inter-related costs and benefits to the individual and so there will be subtle complexities in the trade-offs surrounding this defensive behaviour. In predatory encounters, dropping by prey will also impose varying costs and benefits on the predator - or predators - involved in the system. There may be important trade-offs involved in the decision made by predators regarding whether to pursue prey or not, but the predator perspective on dropping has been less explored at present. Beyond its function as an escape tactic, dropping has also been suggested to be an important precursor to flight in insects and further study could greatly improve understanding of its evolutionary importance. Dropping in insects could also prove of significant practical importance if an improved understanding can be applied to integrated pest-management strategies. Currently the non-consumptive effects of predators on their prey are under-appreciated in biological control and it may be that the dropping behaviour of many pest species could be exploited via management practices to improve crop protection. Overall, this review aims to provide a comprehensive synthesis of the current literature on dropping and to raise awareness of this fascinating and widespread behaviour. It also seeks to offer some novel hypotheses and highlight key avenues for future research.

/pdf/dropping-to-escape-a-review-of-an-under-appreciated-2xpjbci22l.pdf

Dropping to escape: a review of an under-appreciated antipredator defence.

For arboreal primates, ground use may increase dispersal opportunities, tolerance to habitat change, access to ground-based resources, and resilience to human disturbances, and so has conservation implications. We collated published and unpublished data from 86 studies across 65 localities to assess titi monkey (Callicebinae) terrestriality. We examined whether the frequency of terrestrial activity correlated with study duration (a proxy for sampling effort), rainfall level (a proxy for food availability seasonality), and forest height (a proxy for vertical niche dimension). Terrestrial activity was recorded frequently for Callicebus and Plecturocebus spp., but rarely for Cheracebus spp. Terrestrial resting, anti-predator behavior, geophagy, and playing frequencies in Callicebus and Plecturocebus spp., but feeding and moving differed. Callicebus spp. often ate or searched for new leaves terrestrially. Plecturocebus spp. descended primarily to ingest terrestrial invertebrates and soil. Study duration correlated positively and rainfall level negatively with terrestrial activity. Though differences in sampling effort and methods limited comparisons and interpretation, overall, titi monkeys commonly engaged in a variety of terrestrial activities. Terrestrial behavior in Callicebus and Plecturocebus capacities may bolster resistance to habitat fragmentation. However, it is uncertain if the low frequency of terrestriality recorded for Cheracebus spp. is a genus-specific trait associated with a more basal phylogenetic position, or because studies of this genus occurred in pristine habitats. Observations of terrestrial behavior increased with increasing sampling effort and decreasing food availability. Overall, we found a high frequency of terrestrial behavior in titi monkeys, unlike that observed in other pitheciids.

/pdf/terrestrial-behavior-in-titi-monkeys-callicebus-cheracebus-1o4wt4bd7v.pdf

Terrestrial behavior in titi monkeys (Callicebus, Cheracebus, and Plecturocebus) : potential correlates, patterns, and differences between genera

Seeds of Amazonian plants

Claw morphology, and claw-closing forces of four species of intertidal crabs from San Juan Island, Washington were compared and related these findings were related to prey size selection, shell breaking times and total handling times on their snail prey, Littorina sitkana Philippi. Two functional groups of crabs emerged: generalists and specialists on hard-shelled prey. The generalist, Hemigrapsus nudus (Dana), has an omnivorous diet and possesses weak claws with small, fine denticles and mechanical advantage (MA) of the claw's lever system 0.3. The claws of the generalist, H. nudus, exhibited weaker claw closing forces (5 N) than those of similar sized specialists (>12 N). When crabs of similar weight were offered four size categories of Littorina sitkana, the generalist, Hemigrapsus nudus, exhibited a consistent preference for the smallest size categories, while the three specialists attacked all size classes offered. Hemigrapsus nudus took significantly longer (134 s) than the specialists (30–52 s) to break open a 4 mm L. sitkana. This difference in shell-breaking time between the generalist and the specialists increased with increasing prey size. The rate of successful attacks on increasingly larger L. sitkana decreased with prey size in the generalist (70% on 4 mm, 37% on 6 mm, and 0% on 8 mm snails), but remained high in the specialists (70–100%). Strength limitation of the claws is the best hypothesis to explain the avoidance of large snails by the generalist, H. nudus.

Claw morphology, prey size selection and foraging efficiency in generalist and specialist shell-breaking crabs

Honest error, precaution or alertness advertisement? Reactions to vertebrate pseudopredators in red‐nosed cuxiús (Chiropotes albinasus), a high‐canopy neotropical primate

\n Predation risk is important in influencing animal behaviour. We investigated how the choice of nocturnal sleeping and diurnal resting sites by two species of primates was influenced by the most likely forms of attack (diurnal raptors and nocturnal felids). We recorded vertical and horizontal patterns of occupancy for 47 sleeping and 31 resting sites, as well as the presence of lianas or vines on trees. We compared the heights of trees used as resting or sleeping sites by the monkeys with those of 200 forest trees that the monkeys did not use. Trees used as nocturnal sleeping sites were taller than those used as diurnal resting sites, and taller than trees that the monkeys did not use. However, while trees used as diurnal resting sites were not significantly taller than non-used trees, diurnal resting sites were located on branches closer to the ground, closer to the main trunk of the tree and in trees with more lianas/vines than nocturnal sleeping sites. The differences in site location can be explained by the type of predator most likely to attack at a particular time: raptors in the day and felids at night.

Being hunted high and low: do differences in nocturnal sleeping and diurnal resting sites of howler monkeys (Alouatta nigerrima and Alouatta discolor) reflect safety from attack by different types of predator?

© 2020 Association for Tropical Biology and Conservation 1Zoology Graduate Program, Amazonas Federal University, Manaus, Brazil 2Ecology Graduate Program, National Amazon Research Institute, Manaus, Brazil 3Biology Department, Amazonas Federal University, Manaus, Brazil 4School of Behavioral Sciences, Czech University of Life Sciences Prague, Prague, Czech Republic 5School of Life Sciences, Roehampton University, London, UK 6Zoology Department, Pernambuco Federal University, Recife, Brazil

Juggling options: Manipulation ease determines primate optimal fruit‐size choice

Various species of animals maximise energy gained through foraging by minimising excessive energy spent on nonessential activities. Avoiding predation is key for maximising an individual's lifespan, as well as that of its kin; however, anti-predation behaviours can be energetically costly. We investigated the relationship between the potential threat levels by predators, pseudo-predators, and non-predators, and the subsequent energetic cost of behavioural reactions to these threats, in the white-bellied spider monkey (Ateles belzebuth), golden-backed uacari (Cacajao ouakary), and red-nosed cuxiu (Chiropotes albinasus). We analyzed a total of 270 interactions across three independent field studies of the three primate species. Our results revealed significant differences in the behavioural response to predators and non-predators for both C. ouakary and C. albinasus, but not for A. belzebuth. In terms of risk-categorized behaviours, response to predators differed from response to non-predators (being much more intense and energy intensive), while there was no difference in response to predators versus pseudo-predators. Thus, response to potential predators represents an integral part of the time-management and defence strategies of two of the three studied species, and should be integrated into future studies of primate responses to varying levels of predation threat.

Pavel Tomanek

Papers

Honest error, precaution or alertness advertisement? Reactions to vertebrate pseudopredators in red‐nosed cuxiús (Chiropotes albinasus), a high‐canopy neotropical primate

Being hunted high and low: do differences in nocturnal sleeping and diurnal resting sites of howler monkeys (Alouatta nigerrima and Alouatta discolor) reflect safety from attack by different types of predator?

Juggling options: Manipulation ease determines primate optimal fruit‐size choice

Calls for concern: Matching alarm response levels to threat intensities in three Neotropical primates