Abstract
Abundant empirical and theoretical studies indicate that predation is a key driver of primate evolution. The Snake Detection Theory (SDT) posits that snakes have been the main predators of primates since the late Cretaceous and that they influenced the diversification and evolution of primates. Laboratory research focusing on the innate ability of primates to detect snakes amid complex visual stimuli has provided strong support for key tenets of the SDT. While this theory has greatly contributed to our knowledge of primate evolution, supporting experimental studies may have overly focused on snakes and disregarded other important predators. This potential sampling bias weakens the conclusion that primates respond with a specific (high) intensity to snakes compared to other predators. We reviewed the literature about primate-predator interactions under natural and experimental conditions. We listed the primate and predator species involved in natural versus experimental studies. Predation events on primates recorded in the field mainly involved other primates, then raptors and carnivorans. SDT-related experimental studies heavily focused on snakes as predator stimuli and did not include raptors. Other experimental studies largely used snakes and primates and to a lesser extent carnivorans. Apes were the most often tested primates in experimental studies, whereas other primate taxa were neglected. Moreover, predators used as stimuli in experimental studies were inaccurately identified, notably snakes. Altogether, our results show that SDT-related studies neglected most of the major natural predators of primates. SDT studies also focused on a handful of primate species, whereas the theory relies on comparisons among taxa. Finally, poor taxonomic information on snakes used as stimuli blurs the interpretation of their relationship with primates. We suggest that future studies test the SDT by presenting a wide range of predators to different primate species to improve our understanding of the complexity of predator–prey interactions.
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References
Adukauskienė, D., Varanauskienė, E., & Adukauskaitė, A. (2011). Venomous snakebites. Medicina, 47(8), 461. https://doi.org/10.3390/medicina47080061
Allen, W. L., Baddeley, R., Scott-Samuel, N. E., & Cuthill, I. C. (2013). The evolution and function of pattern diversity in snakes. Behavioral Ecology, 24(5), 1237–1250. https://doi.org/10.1093/beheco/art058
Altschul, D., Beran, M., Bohn, M., Caspar, K., Fichtel, C., Försterling, M., Grebe, N., Hernandez-Aguilar, R., Kwok, S. C., Llorente, M., Rodrigo, A., Proctor, D., Sánchez-Amaro, A., Simpson, E., Szabelska, A., Taylor, D., Mescht, J., Völter, C., & Watzek, J. (2019). Collaborative open science as a way to reproducibility and new insights in primate cognition research. https://doi.org/10.24602/sjpr.62.3_205
Berger, L. R., & Mcgraw, W. (2007). Further evidence for eagle predation of, and feeding damage on, the Taung child. South African Journal of Science, 103, 496–498.
Bertels, J., Bourguignon, M., de Heering, A., Chetail, F., De Tiège, X., Cleeremans, A., & Destrebecqz, A. (2020). Snakes elicit specific neural responses in the human infant brain. Scientific Reports, 10(1), 7443. https://doi.org/10.1038/s41598-020-63619-y
Bezanson, M., & McNamara, A. (2019). The what and where of primate field research may be failing primate conservation. Evolutionary Anthropology: Issues, News, and Reviews, 28(4), 166–178. https://doi.org/10.1002/evan.21790
Boesch, C., & Boesch, H. (1989). Hunting behavior of wild chimpanzees in the Taï National Park. American Journal of Physical Anthropology, 78(4), 547–573. https://doi.org/10.1002/ajpa.1330780410
Boinski, S. (1988). Use of a club by a wild white-faced capuchin (Cebus capucinus) to attack a venomous snake (Bothrops asper). American Journal of Primatology, 14(2), 177–179. https://doi.org/10.1002/ajp.1350140208
Brusatte, S. L., O’Connor, J. K., & Jarvis, E. D. (2015). The Origin and Diversification of Birds. Current Biology, 25(19), R888–R898. https://doi.org/10.1016/j.cub.2015.08.003
Butynski, T. M. (1982). Blue monkey (Cercopithecus mitis stuhlmanni) predation on galagos. Primates, 23(4), 563–566. https://doi.org/10.1007/BF02373967
Camarós, E., Cueto, M., Lorenzo, C., Villaverde, V., & Rivals, F. (2015). Large carnivore attacks on hominins during the Pleistocene: A forensic approach with a Neanderthal example. Archaeological and Anthropological Sciences, 8(3), 635–646. https://doi.org/10.1007/s12520-015-0248-1
Cartmill, M. (1992). New views on primate origins. Evolutionary Anthropology: Issues, News, and Reviews, 1(3), 105–111. https://doi.org/10.1002/evan.1360010308
Cheney, D. L., Lee, P. C., & Seyfarth, R. M. (1981). Behavioral correlates of non-random mortality among free-ranging female vervet monkeys. Behavioral Ecology and Sociobiology, 9(2), 153–161. https://doi.org/10.1007/BF00293587
Choiniere, J. N., Neenan, J. M., Schmitz, L., Ford, D. P., Chapelle, K. E. J., Balanoff, A. M., Sipla, J. S., Georgi, J. A., Walsh, S. A., Norell, M. A., Xu, X., Clark, J. M., & Benson, R. B. J. (2021). Evolution of vision and hearing modalities in theropod dinosaurs. Science. https://www.science.org/doi/abs/https://doi.org/10.1126/science.abe7941
Cochran, W. G. (1954). Some Methods for Strengthening the Common χ2 Tests. Biometrics, 10(4), 417–451. https://doi.org/10.2307/3001616
Coelho, C. M., Suttiwan, P., Faiz, A. M., Ferreira-Santos, F., & Zsido, A. N. (2019). Are humans prepared to detect, fear, and avoid snakes? The mismatch between laboratory and ecological evidence. Frontiers in Psychology, 10, 2094. https://doi.org/10.3389/fpsyg.2019.02094
Da Silva, G. A. O., Falótico, T., Nash, S. D., & Valença-Montenegro, M. M. (2019). A green racer snake (Philodryas nattereri, Colubridae) killed but not eaten by a blonde capuchin monkey (Sapajus flavius, Cebidae). Primates, 60(5), 459–465. https://doi.org/10.1007/s10329-019-00738-9
Darimont, C. T., Carlson, S. M., Kinnison, M. T., Paquet, P. C., Reimchen, T. E., & Wilmers, C. C. (2009). Human predators outpace other agents of trait change in the wild. Proceedings of the National Academy of Sciences, 106(3), 952–954. https://doi.org/10.1073/pnas.0809235106
Das, C., & Jana, R. (2017). Human–crocodile conflict in the Indian Sundarban: An analysis of spatio-temporal incidences in relation to people’s livelihood. Oryx, 52, 1–8. https://doi.org/10.1017/S0030605316001502
de Moraes, P. Z., Diniz, P., Spyrides, M. H. C., & Pessoa, D. M. A. (2021). The effect of pelage, background, and distance on predator detection and the evolution of primate color vision. American Journal of Primatology, 83(2), e23230. https://doi.org/10.1002/ajp.23230
Denzer, W. (2018). Commentary: Itsy bitsy spider…: Infants react with increased arousal to spiders and snakes. Frontiers in Psychology, 9, 393. https://doi.org/10.3389/fpsyg.2018.00393
Estrada, A., Garber, P. A., Rylands, A. B., Roos, C., Fernandez-Duque, E., Fiore, A. D., Nekaris, K. A.-I., Nijman, V., Heymann, E. W., Lambert, J. E., Rovero, F., Barelli, C., Setchell, J. M., Gillespie, T. R., Mittermeier, R. A., Arregoitia, L. V., Guinea, M. de, Gouveia, S., Dobrovolski, R., …, Li, B. (2017). Impending extinction crisis of the world’s primates: Why primates matter. Science Advances. https://www.science.org/doi/abs/https://doi.org/10.1126/sciadv.1600946
Falótico, T., Verderane, M. P., Mendonça-Furtado, O., Spagnoletti, N., Ottoni, E. B., Visalberghi, E., & Izar, P. (2018). Food or threat? Wild capuchin monkeys (Sapajus libidinosus) as both predators and prey of snakes. Primates, 59(1), 99–106. https://doi.org/10.1007/s10329-017-0631-x
Ferrari, S. F. (2009). Predation Risk and Antipredator Strategies. In P. A. Garber, A. Estrada, J. C. Bicca-Marques, E. W. Heymann, & K. B. Strier (Eds.), South American primates: Comparative perspectives in the study of behavior, ecology, and conservation (pp. 251–277). Springer. https://doi.org/10.1007/978-0-387-78705-3_10
Fichtel, C. (2007). Avoiding predators at night: Antipredator strategies in red-tailed sportive lemurs (Lepilemur ruficaudatus). American Journal of Primatology, 69(6), 611–624. https://doi.org/10.1002/ajp.20363
Fichtel, C. (2012). Predation. In J. C. Mitani, J. Call, P. Kappeler, R. Palombit, & J. Silk (Eds.), The evolution of primate societies (pp. 169–194). Chicago University Press.
Fichtel, C., & Kappeler, P. M. (2002). Anti-predator behavior of group-living Malagasy primates: Mixed evidence for a referential alarm call system. Behavioral Ecology and Sociobiology, 51(3), 262–275. https://doi.org/10.1007/s00265-001-0436-0
Foerster, S. (2008). Two incidents of venomous snakebite on juvenile blue and Sykes monkeys (Cercopithecus mitis stuhlmanni and C. m. Albogularis). Primates, 49(4), 300–303. https://doi.org/10.1007/s10329-008-0098-x
Fukuda, Y., Manolis, C., & Appel, K. (2014). Featured article: Management of human-crocodile conflict in the Northern Territory, Australia: Review of crocodile attacks and removal of problem crocodiles. The Journal of Wildlife Management, 78(7), 1239–1249. https://doi.org/10.1002/jwmg.767
García-Grajales, J., & Buenrostro-Silva, A. (2019). Assessment of human–crocodile conflict in Mexico: Patterns, trends and hotspots areas. Marine and Freshwater Research, 70(5), 708–720. https://doi.org/10.1071/MF18150
Gašperšič, M., & Pruetz, J. (2004). Predation on a monkey by Savanna Chimpanzees at Fongoli, Senegal. Pan Africa News, 11, 8–10. https://doi.org/10.5134/143443
Gayet, S., Stein, T., & Peelen, M. V. (2019). The danger of interpreting detection differences between image categories: A brief comment on “Mind the snake: Fear detection relies on low spatial frequencies” (Gomes, Soares, Silva, & Silva, 2018). Emotion, 19(5), 928–932. https://doi.org/10.1037/emo0000550
Gil-da-Costa, R., Palleroni, A., Hauser, M. D., Touchton, J., & Kelley, J. P. (2003). Rapid acquisition of an alarm response by a neotropical primate to a newly introduced avian predator. Proceedings of the Royal Society of London Series B: Biological Sciences, 270(1515), 605–610. https://doi.org/10.1098/rspb.2002.2281
Glaudas, X., & Winne, C. T. (2007). Do warning displays predict striking behavior in a viperid snake, the cottonmouth (Agkistrodon piscivorus)? Canadian Journal of Zoology, 85(4), 574–578. https://doi.org/10.1139/Z07-025
Gomes, N., Soares, S., Silva, S., & Silva, C. (2017). Mind the snake: Fear detection relies on low spatial frequencies. Emotion, 18(6), 886. https://doi.org/10.1037/emo0000391
Goodman, S. M., O’Connor, S., & Langrand, O. (1993). A Review of predation on lemurs: Implications for the evolution of social behavior in small, nocturnal primates. In P. M. Kappeler & J. U. Ganzhorn (Eds.), Lemur social systems and their ecological basis (pp. 51–66). Springer US. https://doi.org/10.1007/978-1-4899-2412-4_5
Grigg, G., & Kirshner, D. S. (2015). Biology and Evolution of Crocodylians. Csiro Publishing.
Gursky-Doyen, S., & Nekaris, K. A. I. (2007). Primate anti-predator strategies. Springer Science & Business Media.
Hauke, T. J., & Herzig, V. (2017). Dangerous arachnids—Fake news or reality? Toxicon, 138, 173–183. https://doi.org/10.1016/j.toxicon.2017.08.024
Hernández Tienda, C., Beltrán Francés, V., Majolo, B., Romero, T., Illa Maulany, R., Oka Ngakan, P., & Amici, F. (2021). Reaction to snakes in wild moor Macaques (Macaca maura). International Journal of Primatology, 42(4), 528–532. https://doi.org/10.1007/s10764-021-00230-6
Hoehl, S., Hellmer, K., Johansson, M., & Gredebäck, G. (2017). Itsy bitsy spider… : Infants react with increased arousal to spiders and snakes. Frontiers in Psychology, 8, 1710. https://doi.org/10.3389/fpsyg.2017.01710
Hohmann, G., & Fruth, B. (2007). New records on prey capture and meat eating by Bonobos at Lui Kotale, Salonga National Park, Democratic Republic of Congo. Folia Primatologica, 79(2), 103–110. https://doi.org/10.1159/000110679
Hopper, L. M., Allritz, M., Egelkamp, C. L., Huskisson, S. M., Jacobson, S. L., Leinwand, J. G., & Ross, S. R. (2021). A comparative perspective on three primate species’ responses to a pictorial emotional stroop task. Animals, 11(3), 588. https://doi.org/10.3390/ani11030588
Isbell, L. A. (1994). Predation on primates: Ecological patterns and evolutionary consequences. Evolutionary Anthropology: Issues, News, and Reviews, 3(2), 61–71. https://doi.org/10.1002/evan.1360030207
Isbell, L. A. (2006). Snakes as agents of evolutionary change in primate brains. Journal of Human Evolution, 51(1), 1–35. https://doi.org/10.1016/j.jhevol.2005.12.012
Isbell, L. A. (2009). The Fruit, the Tree, and the Serpent: Why We See So Well. Harvard University Press.
Isbell, L. A., & Etting, S. F. (2017). Scales drive detection, attention, and memory of snakes in wild vervet monkeys (Chlorocebus pygerythrus). Primates, 58(1), 121–129. https://doi.org/10.1007/s10329-016-0562-y
Jolly, A., Caless, S., Cavigelli, S., Gould, L., Pereira, M. E., Pitts, A., Pride, R. E., Rabenandrasana, H. D., Walker, J. D., & Zafison, T. (2000). Infant killing, wounding and predation in Eulemur and Lemur. International Journal of Primatology, 21(1), 21–40. https://doi.org/10.1023/A:1005467411880
Kawai, N. (2019). The fear of snakes: Evolutionary and psychobiological perspectives on our innate fear. Springer Singapore. https://doi.org/10.1007/978-981-13-7530-9
Le, Q. V., Isbell, L. A., Matsumoto, J., Le, V. Q., Hori, E., Tran, A. H., Maior, R. S., Tomaz, C., Ono, T., & Nishijo, H. (2014). Monkey pulvinar neurons fire differentially to snake postures. PLoS One, 9(12), e114258. https://doi.org/10.1371/journal.pone.0114258
Lobue, V., & Deloache, J. S. (2011). What’s so special about slithering serpents? Children and adults rapidly detect snakes based on their simple features. Visual Cognition, 19(1), 129–143. https://doi.org/10.1080/13506285.2010.522216
Lorenz, R. (1971). Goeldi’s monkey callimico goeldii Thomas 1904 preying on snakes. Folia Primatologica, 15(1–2), 133–142. https://doi.org/10.1159/000155372
Mcgraw, W. S., & Berger, L. R. (2013). Raptors and primate evolution. Evolutionary Anthropology: Issues, News, and Reviews, 22(6), 280–293. https://doi.org/10.1002/evan.21378
McGraw, W. S., Cooke, C., & Shultz, S. (2006). Primate remains from African crowned eagle (Stephanoaetus coronatus) nests in Ivory Coast’s Tai Forest: Implications for primate predation and early hominid taphonomy in South Africa. American Journal of Physical Anthropology, 131(2), 151–165. https://doi.org/10.1002/ajpa.20420
Miller, L. E., & Treves, A. (2011). Predation on primates predation on primates past studies, current challenges, and directions for the future. In primates in perspective. Oxford University Press.
Mittermeier, R. A., Wilson, D. E., & Rylands, A. B. (2013). Handbook of the mammals of the world: Primates. Lynx Edicions.
National Geographic News. (2017). Are we born fearing spiders and snakes? Retrieved August 9, 2020, from https://www.nationalgeographic.com/news/2017/10/infant-fear-phobia-science-snakes-video-spd/
Newton-Fisher, N., Notman, H., & Reynolds, V. (2002). Hunting of mammalian prey by Budongo Forest Chimpanzees. Folia Primatologica. International Journal of Primatology, 73, 281–283. https://doi.org/10.1159/000067454
Ohman, A., & Mineka, S. (2001). Fears, phobias, and preparedness: Toward an evolved module of fear and fear learning. Psychological Review, 108(3), 483–522. https://doi.org/10.1037/0033-295x.108.3.483
Page, M. J., McKenzie, J. E., Bossuyt, P. M., Boutron, I., Hoffmann, T. C., Mulrow, C. D., Shamseer, L., Tetzlaff, J. M., Akl, E. A., Brennan, S. E., Chou, R., Glanville, J., Grimshaw, J. M., Hróbjartsson, A., Lalu, M. M., Li, T., Loder, E. W., Mayo-Wilson, E., McDonald, S., …, & Moher, D. (2021a). The PRISMA 2020 statement: An updated guideline for reporting systematic reviews. BMJ, 372, n71. https://doi.org/10.1136/bmj.n71
Page, M. J., Moher, D., Bossuyt, P. M., Boutron, I., Hoffmann, T. C., Mulrow, C. D., Shamseer, L., Tetzlaff, J. M., Akl, E. A., Brennan, S. E., Chou, R., Glanville, J., Grimshaw, J. M., Hróbjartsson, A., Lalu, M. M., Li, T., Loder, E. W., Mayo-Wilson, E., McDonald, S., …, & McKenzie, J. E. (2021b). PRISMA 2020 explanation and elaboration: Updated guidance and exemplars for reporting systematic reviews. BMJ, 372, n160. https://doi.org/10.1136/bmj.n160
Pessoa, D. M. A., Maia, R., de Albuquerque Ajuz, R. C., De Moraes, P. Z. P. M. R., Spyrides, M. H. C., & Pessoa, V. F. (2014). The adaptive value of primate color vision for predator detection. American Journal of Primatology, 76(8), 721–729. https://doi.org/10.1002/ajp.22264
R Core Team. (2022). R: A language and environment for statistical computing. (4.0.2). R foundation for statistical computing. Retrieved June 25, 2020, from http://www.R-project.org/
RStudio Team. (2022). RStudio: Integrated development environment for R (2022.2.3.492). RStudio, PBC. Retrieved May 17, 2022, from http://www.rstudio.com/
Shine, R., Harlow, P. S., Keogh, J. S., & Boeadi. (1998). The influence of sex and body size on food habits of a giant tropical snake, Python reticulatus. Functional Ecology, 12(2), 248–258https://doi.org/10.1046/j.1365-2435.1998.00179.x
Silcox, M. T., & López-Torres, S. (2017). Major Questions in the Study of Primate Origins. Annual Review of Earth and Planetary Sciences, 45(1), 113–137. https://doi.org/10.1146/annurev-earth-063016-015637
Soares, S. C., Lindström, B., Esteves, F., & Öhman, A. (2014). The Hidden Snake in the Grass: Superior Detection of Snakes in Challenging Attentional Conditions. PLoS ONE, 9(12), e114724. https://doi.org/10.1371/journal.pone.0114724
Stanford, C. B., Wallis, J., Matama, H., & Goodall, J. (1994). Patterns of predation by chimpanzees on red colobus monkeys in gombe national park, 1982–1991. American Journal of Physical Anthropology, 94(2), 213–228. https://doi.org/10.1002/ajpa.1330940206
Sussman, R. W. (2017). Angiosperm radiation theory. In The international encyclopedia of primatology (pp. 1–3). American Cancer Society. https://doi.org/10.1002/9781119179313.wbprim0097
Utami, S. S., & Van Hooff, J. A. R. A. M. (1997). Meat-eating by adult female Sumatran orangutans (Pongo pygmæus abelii). American Journal of Primatology, 43(2), 159–165. https://doi.org/10.1002/(SICI)1098-2345(1997)43:2%3c159::AID-AJP5%3e3.0.CO;2-W
Van Strien, J. W., & Isbell, L. A. (2017). Snake scales, partial exposure, and the Snake Detection Theory: A human event-related potentials study. Scientific Reports, 7(1), 46331. https://doi.org/10.1038/srep46331
Wallace, K. M., Leslie, A. J., & Coulson, T. (2012). Living with predators: A focus on the issues of human–crocodile conflict within the lower Zambezi valley. Wildlife Research, 38(8), 747–755. https://doi.org/10.1071/WR11083
Watts, D. P., & Amsler, S. J. (2013). Chimpanzee-red colobus encounter rates show a red colobus population decline associated with predation by chimpanzees at Ngogo. American Journal of Primatology, 75(9), 927–937. https://doi.org/10.1002/ajp.22157
Weiss, L., Brandl, P., & Frynta, D. (2015). Fear reactions to snakes in naïve mouse lemurs and pig-tailed macaques. Primates, 56(3), 279–284. https://doi.org/10.1007/s10329-015-0473-3
Westoll, A., Boinski, S., Stickler, C., Cropp, S., Ehmke, E., & Kauffman, L. (2003). Are vigilance, risk from avian predators and group size consequences of habitat structure? A comparison of three species of squirrel monkey (Saimiri oerstedii, S. boliviensis, and S. sciureus). Behaviour, 140(11–12), 1421–1467. https://doi.org/10.1163/156853903771980666
Wheeler, B. (2010). Snakes! The unified theory of everything about primates? Evolutionary Anthropology: Issues, News, and Reviews, 19(1), 37–38. https://doi.org/10.1002/evan.20244
Wheeler, B., Bradley, B. J., & Kamilar, J. M. (2011). Predictors of orbital convergence in primates: A test of the snake detection hypothesis of primate evolution. Journal of Human Evolution, 61(3), 233–242. https://doi.org/10.1016/j.jhevol.2011.03.007
Wilson, G. P., Ekdale, E. G., Hoganson, J. W., Calede, J. J., & Vander Linden, A. (2016). A large carnivorous mammal from the Late Cretaceous and the North American origin of marsupials. Nature Communications, 7(1), 13734. https://doi.org/10.1038/ncomms13734
Wrangham, R., & Riss, E. (1990). Rates of predation on mammals by Gombe chimpanzees, 1972–1975. Primates, 31(2), 157–170. https://doi.org/10.1007/BF02380938
Zuberbühler, K., & Jenny, D. (2002). Leopard predation and primate evolution. Journal of Human Evolution, 43(6), 873–886. https://doi.org/10.1006/jhev.2002.0605
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The authors thank Benoit Van Der Zyppe for help setting up the bibliographic analysis grid, reading publications, and data collection. We are grateful to Sandrine Prat for her insightful comments and suggestions on the manuscript. We thank the Muséum national d'Histoire naturelle (MNHN) for allocating a Master’s grant to Karl Zeller. We thank anonymous reviewers and the editor for their constructive comments that helped improving the manuscript.
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This work was financially supported by the Museum national d’Histoire naturelle (France) to C.G and K.Z.
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Original idea: XB. Conceptualization and writing of first version of the manuscript: KZ. Data collection, data management and statistical analyses: KZ. All authors contributed to the elaboration of the research questions and to the methodology. All authors contributed to writing, improvements and approved the submitted version.
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Zeller, K., Garcia, C., Maille, A. et al. Primate–Predator Interactions: Is There a Mismatch Between Laboratory and Ecological Evidence?. Int J Primatol 44, 258–281 (2023). https://doi.org/10.1007/s10764-022-00331-w
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DOI: https://doi.org/10.1007/s10764-022-00331-w