“A Trick of the Tail”: Prehensile Tails and Primate Evolution

When we look at ourselves in the mirror each morning, we are constantly reminded of our ape ancestry. For, like our fellow ape cousins – the chimpanzees, gorillas and orangutans – we lack something that most other primates possess: a long tail. Yet while apes have evolved other neat adaptations for arboreal living (see Hunt [2016]¹ for these adaptations), for lemurs and monkeys, the tail is critical for daily life in the trees. Providing a source of balance while traversing narrow supports and aiding in weight distribution while clambering over unstable branches², tails are a hallmark of monkey ecology and an essential component of their distinctive image.

Yet some monkeys have taken things one step further, evolving a prehensile tail. In these monkeys, their tail functions almost as a dexterous fifth limb, and is used for sturdy grasping and body support while moving². Across all mammals, the prehensile tail is quite adaptive; it has independently evolved in six lineages of mammals, including marsupials, rodents and even some carnivores.³ It is thought that prehensile tails help animals move in tropical rainforest canopies, especially in those forests with large canopy gaps, fewer lianas and more fragile tree crowns.³Yet other mammals also use their prehensile tails to anchor their bodies while they are feeding, such as the arboreal anteater, the tamandua³. Despite its usefulness, the prehensile tail is found only in two groups of primates: Cebus – the capuchin monkeys– and the atelines, a group that includes the howler (Alouatta spp.) and spider (Ateles spp.) monkeys. These monkeys are only found in Central and South America. In contrast, no primates in African or Asian rainforests have evolved similar structures.

At quick glance, it appears that these two groups of monkeys must be closely related because they share this unique feature. But DNA evidence states otherwise. In fact, capuchins share a closer evolutionary relationship with the non-prehensile tailed squirrel monkeys (Saimiri spp.) than with either spider or howler monkeys⁴. We therefore have another case of independent evolution of the prehensile tail, this time within the primate lineage itself. But could we tell that from comparing patterns in their tail anatomies or behaviors?

In spider and howler monkeys, the prehensile tail is long, making up a sizable portion of the animal’s total body weight. Capuchins, by contrast, have an unremarkable tail size; they don’t deviate very much from other non-prehensile-tailed New World monkeys in their tail proportions ⁵. While both groups have increased muscular development⁶and neural innervation⁵ in their tails for strength and sensitivity, only the spider and howler monkeys have a dedicated region of their brains associated with tail control⁵. Capuchins do not have this region. Yet the most striking external difference is in the gripping surface of the tail⁷. For while the capuchin tail is fully haired and un-adorned, the tails of spider and howler monkeys have hairless, fingerprint-like friction pads on their grasping surfaces, covered with high densities of mechanoreceptors (specialized cells that transmit touch sensations)⁷. Compared to capuchins, the tails of spider and howler monkeys have more elaborate systems of mechanical strength, neural control, and tactile sensitivity. And yes, every tail print is unique, just like their fingerprints.

But does this anatomical difference translate into different patterns of behavioral usage? For spider and howler monkeys, the prehensile tail has diverse roles in both locomotion and feeding. Spider and howler monkeys engage in below branch suspensory foraging, relying on prehensile tails to support most, if not all, of their body weight⁸. This allows them access to a more diverse array of hard to reach foods in the canopy, often on thin branches at the edges of trees⁸. In addition, spider monkeys use their prehensile tails for rapid, arm swinging locomotion below branches⁹(commonly called ‘brachiation’). In this movement, their tail acts as a propulsive lever and a stable grip, allowing them to rapidly arm swing within and between tree crowns and support themselves when bridging perilous canopy gaps¹⁰. In contrast, howler monkeys are less athletic when it comes to using their prehensile tails for locomotion, preferring to slowly walk across supports while their tail grips the substrate⁸, almost like a safety harness. Howlers rarely perform the rapid, below-branch, tail-assisted ‘brachiation’ locomotion that is so common to see in spider monkeys².

Examples of the diversity of prehensile tail use in atelines (i.e., howler and spider monkeys). Top row: Peruvian spider monkeys (Ateles chamek) using tail assisted and tail-only foraging postures. The tail of spider monkeys makes up a larger portion of the body weight and is more muscular than the capuchin tail, and capuchins rarely perform ‘tail-only’ foraging postures. Bottom row: Bolivian howler monkeys (Alouatta sara) in the Peruvian Amazon using their prehensile tails to hold up their bodies while foraging. Howler monkeys do not usually use their tails for suspensory locomotion, like spider monkeys, instead preferring to travel on the tops of branches like non-prehensile tailed monkeys. Middle Right: A Peruvian spider monkey using tail-assisted, below-branch ‘brachiation’, a behavior not seen in either howler or capuchin monkeys. Top Row Photos by L. Fannin. Rest by C. Rohr.

Similar to howlers, capuchins use their prehensile tails more for support during foraging, rather than for locomotion¹¹. This includes below-branch foraging, although it is more common to see capuchins use their tails in combination with support from both of their hindlimbs¹¹. Unlike spider or howler monkeys, capuchins rarely support their body weight entirely with their tails. Uniquely, capuchins use their tail as anchors during extractive foraging, where both hands are freed to forcibly manipulate and twist food objects¹². Capuchins are notoriously famous for this behavior¹², and the tail provides much needed leverage while they rip open hives looking for invertebrate prey or plucking palm fruits from wobbly tree branches¹¹. Extractive foraging behaviors with the prehensile tail are not as common in spider or howler monkeys¹³, suggesting that this unique role for the prehensile tail may be adaptively significant to the capuchin¹¹.

Overall, the prehensile tails of these monkeys share key functional roles, even with very different anatomies. Both groups use their tails to increase their ability to access food in the most unstable parts of the canopy. Though the prehensile tails of howler monkeys are similar in appearance to spider monkeys, due to their close relatedness, they use their tails much more conservatively, likely because their low-energy, foliage-based diets prevent such elaborate movement8. By comparison, spider monkeys use their tail in acrobatic, below-branch moving, hence the greater elaboration of their neural and tactile abilities(5). They can fuel this taxing locomotor behavior with high-energy ripe fruits, which make up a substantial portion of their diets10. While capuchin tails may not share the elaborate adaptations relative to spider or howlers, they are nonetheless critical for manipulating difficult to reach food items. The reductions in strength and manual dexterity in the capuchin tail are reflected in its minimal use during locomotion, as well as the low frequency of ‘tail-only’ suspensory behaviors. Key ecological differences between capuchins and spider monkeys (and by a lesser extent, howlers) suggest that each monkey group evolved its prehensile tail in response to a unique set of ecological selective pressures. So, while there are quite a few ways to skin a cat, as the old saying goes, the ways to use a prehensile tail in primates may undoubtedly be a close second.

About the Author:

Luke Fannin is a PhD student at Dartmouth College and FPI alumni interested in functional primate morphology, where he uses living primates as models to interpret the dietary and locomotor behavior of fossil primates, including fossil hominins. He has done work with living primate in the jungles of Peru and Cöte d’Ivorie and has performed paleontological fieldwork in Tanzania. He has been a science staff writer at FPI for almost three years.

References:

1). Hunt, K. D. (2016). Why are there apes? Evidence for the co-evolution of ape and monkey ecomorphology. Journal of Anatomy, 228, 630-685. https://doi.org/10.1111/joa.12454

2.) Garber, P. A. (2011). Primate locomotor positional behavior and ecology. In C. J. Campbell, A. Fuentes, K. C. MacKinnon, S. K. Bearder, and R. M. Stumpf (Eds.), Primates in Perspective (pp. 548 – 563). New York, NY: Oxford University Press.

3.) Emmons, L. H., & Gentry, A. H. (1983). Tropical forest structure and the distribution of gliding and prehensile-tailed vertebrates. The American Naturalist, 121, 513-524. https://doi.org/10.1086/284079

4.) Schneider, H., & Sampaio, I. (2015). The systematics and evolution of New World primates – A review. Molecular Phylogenetics and Evolution, 82, 348 – 357. https://doi.org/10.1016/j.ympev.2013.10.017

5.) Rosenberger, A. L. (1983). Tale of tails: Parallelism and prehensility. American Journal of Physical Anthropology, 60, 103 – 107. https://doi.org/10.1002/ajpa.1330600114

6.) Organ, J. M., Teaford, M. F., & Taylor, A. B. (2009). Functional correlates of fiber architecture of the lateral caudal musculature in prehensile and nonprehensile tails of the Platyrrhini (Primates) and Procyonidae (Carnivora). The Anatomical Record, 292, 827 – 841. https://doi.org/10.1002/ar.20886

7.) Organ, J. M., Muchlinski, M. N., & Deane, A. S. (2011). Mechanoreceptivity of prehensile tail skin varies between ateline and cebine primates. The Anatomical Record, 294, 2064-2072. https://doi.org/10.1002/ar.21505.

8.) Cant, J. G. H. (1986). Locomotion and feeding postures of spider and howling monkeys: Field study and evolutionary interpretation. Folia Primatologica, 46, 1-14. https://doi.org/10.1159/000156232

9.) Fleagle, J. G. & Mittermeier, R. A. (1980). Locomotor behavior, body size, and comparative ecology of seven Surinam monkeys. American Journal of Physical Anthropology, 52, 301-314. https://doi.org/10.1002/ajpa.1330520302

10.) Youlatos, D. (2008). Locomotion and positional behavior of spider monkeys. In C.J. Campbell (Ed.), Spider Monkeys: Behavior, Ecology, and Evolution of the Genus Ateles (pp. 185-219). Cambridge, UK: Cambridge University Press.

11.) Garber, P. A. & Rehg, J. A. (1999). The ecological role of the prehensile tail in white-faced capuchins (Cebus capucinus). American Journal of Physical Anthropology, 110, 325-339. https://doi.org/10.1002/(SICI)1096-8644(199911)110:3<325::AID-AJPA5>3.0.CO;2-D

12.) Melin, A. D., Young, H. C., Mosdossy, K. N., & Fedigan, L. M. (2014). Seasonality, extractive foraging and the evolution of primate sensorimotor intelligence. Journal of Human Evolution, 71, 77-86. https://doi.org/10.1016/j.jhevol.2014.02.009

13.) Bergeson, D. J. (1998). Patterns of suspensory feeding in Alouatta palliata, Ateles geoffroyi, and Cebus capuchinus. In E. Strasser, J. Fleagle, A. Rosenberger, and H. McHenry (Eds.), Primate Locomotion: Recent Advances (pp. 45-60). New York, NY: Plenum Press.

A Trick of the Tail: Prehensile Tails and Primate Evolution