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Arboreal Lemur Terrestriality is Influenced by When and Where Predators are Present

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It is thought arboreal species avoid foraging on the ground due to perceived predation risk, making the study of when and where arboreal species use the ground key in understanding foraging versus safety tradeoffs. We used publicly available, opportunistic, camera-trap observations from surveys across Madagascar to examine whether arboreal lemur ground use was spatially and temporally related to fosa (Cryptoprocta ferox), a native predator, and human presence. We observed 14 species of diurnal lemur (n = 287 individual observations) and six species of nocturnal lemur (n = 105 individual observations). With static two-species occupancy models and kernel density estimation, we found diurnal and nocturnal lemur ground use was spatially and temporally related to fosa presence. Diurnal lemurs used the ground less at camera locations where fosa were present compared to camera locations where they were absent, particularly if those camera locations lacked other native carnivores. Nocturnal lemurs used the ground more at camera locations fosa were observed at within the past 5 days compared with camera locations where fosa were not observed at within the past 5 days. Despite humans and diurnal lemurs being active at the same time 80% of the diel cycle (temporal overlap Δ = 0.80; 95% confidence interval [CI]: 0.75–0.85), diurnal lemur spatial or temporal use of the ground and human presence were unrelated. Diurnal lemur temporal overlap with humans at camera locations where fosa were uncommon was higher (Δ = 0.79; 95% CI: 0.71–0.86) compared with where fosa were common (Δ = 0.57; 95% CI: 0.46–0.66). Future research on how arboreal lemurs navigate ground use in a multipredator landscape should include behavioral observations to better understand animal decision-making.

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  • Akaike, H. (1973). Information theory and an extension of the maximum likelihood principle. In B. N. Petran & F. Csaki (Eds.), Second International Symposium on Information Theory (pp. 267–281). Akademiai Kiadi.

    Google Scholar 

  • Amoroso, C. R., Kappeler, P. M., Fitchel, C., & Nunn, C. L. (2020). Temporal patterns of waterhole use as a predator avoidance strategy. Journal of Mammalogy, 101(2), 574–581.

    Article  Google Scholar 

  • Barnett, A. A., Almeida, T., Spironello, W. R., Sousa Silva, W., MacLarnon, A., & Ross, C. (2012a). Terrestrial Foraging by Cacajao melanocephalus ouakary (Primates) in Amazonian Brazil: Is Choice of Seed Patch Size and Position Related to Predation Risk? Folia Primatologica (basel), 83(2), 126–139.

    Article  Google Scholar 

  • Barnett, A. A., Boyle, S. A., Norconk, M. M., Palminteri, S., Santos, R. R., Veiga, L. M., Alvim, T. H., Bowler, M., Chism, J., A, ...., D. I. F. (2012b). Terrestrial Activity in Pitheciins (Cacajao, Chiropotes, and Pithecia). American Journal of Primatology, 74(12), 1106-1127.

  • Blanco, M. B., Dausmann, K. H., Ranaivoarisoa, J. F., & Yoder, A. D. (2013). Underground Hibernation in a Primate. Scientific Reports, 3, srep01768.

  • Borgerson, C. (2015). The Effects of Illegal Hunting and Habitat on Two Sympatric Endangered Primates. International Journal of Primatology, 36, 74–93.

    Article  Google Scholar 

  • Borgerson, C., McKean, M. A., Sutherland, M. R., & Godfrey, L. R. (2016). Who Hunts Lemurs and Why They Hunt Them. Biological Conservation, 197, 124–130.

    Article  Google Scholar 

  • Brook, C. E., Herrera, J. P., Borgerson, C., Fuller, E. C., Andriamahazoarivosoa, P., Rasolofoniaina, B. J. R., Randrianasolo, J., Rakotondrafarasata, Z. R. E., Randriamady, H. J., ...., Dobson, A. P. (2019). Population Viability and Harvest Sustainability for Madagascar Lemurs. Conservation Biology, 33(1), 99-111.

  • Burnham, K. P., & Anderson, D. R. (2002). Model Selection and Multimodel Inference. Springer-Verlag.

    Google Scholar 

  • Campbell, C. J., Aureli, F., Chapman, C. A., Ramos-Fernández, G., Matthews, K., Russo, S. E., Suarez, S., & Vick, L. (2005). Terrestrial behavior of Ateles spp. International Journal of Primatology, 26(5), 1039–1051.

    Article  Google Scholar 

  • Embar, K., Raveh, A., Hoffmann, I., & Kotler, B. P. (2014). Predator faciliation or interference: A game of vipers and owls. Oecologia, 174(4), 1301–1309.

    Article  PubMed  Google Scholar 

  • Eppley, T. M., Donati, G., & Ganzhorn, J. U. (2016a). Determinants of Terrestrial Feeding in an Arboreal Primate: The Case of the Southern Bamboo Lemur (Hapalemur meridionalis). American Journal of Physical Anthropology, 161(2), 328–342.

    Article  PubMed  Google Scholar 

  • Eppley, T. M., Donati, G., & Ganzhorn, J. U. (2016b). Unusual Sleeping Site Selection by Southern Bamboo Lemurs. Primates, 57(2), 167–173.

    Article  PubMed  Google Scholar 

  • Eppley, T. M., Hoeks, S., Chapman, C. A., Ganzhorn, J. U., Hall, K., Owen, M. A., Adams, D. B., Allgas, N., Amato, K. R., ...., Andriamahaihavana, M. (2022). Factors influencing terrestriality in primates of the Americas and Madagascar. Proceedings of the National Academy of Sciences of the United States of America, 119(42), e2121105119.

  • Estrada, A. G., Paul, A., Rylands, A. B., Roos, C., Fernandez-Duque, E., Di Fiore, A., Nekaris, K. A., Nijman, V., Heymann, E. W., Lambert, J. E., Rovero, F., …., Barelli. (2017). Impending Extinction Crisis of the World’s Primates: Why Primates Matter. Science Advances, 3, e1600946.

  • Farris, Z. J., Karpanty, S. M., Ratelolahy, F., & Kelly, M. J. (2014). Predator-Primate Distribution, Activity, and Co-Occurrence in Relation to Habitat and Human Activity across Fragmented and Contiguous Forests in Northeastern Madagascar. International Journal of Primatology, 35(5), 859–880.

    Article  Google Scholar 

  • Farris, Z. J., Gerber, B. D., Karpanty, S., Murphy, A., Andrianjakarivelo, V., Ratelolahy, F., & Kelly, M. J. (2015a). When Carnivores Roam: Temporal Patterns and Overlap among Madagascar's Native and Exotic Carnivores. Journal of Zoology, jzo.12216.

  • Farris, Z. J., Golden, C. D., Karpanty, S., Murphy, A., Stauffer, D., Ratelolahy, F., Andrianjakarivelo, V., Holmes, C. M., & Kelly, M. J. (2015b). Hunting, Exotic Carnivores, and Habitat Loss: Anthropogenic Effects on a Native Carnivore Community, Madagascar. PLoS ONE, 10(9), e0136456.

  • Farris, Z. J., Kelly, M. J., Karpanty, S., & Ratelolahy, F. (2016). Patterns of Spatial Co-Occurrence Among Native and Exotic Carnivores in North-Eastern Madagascar. Animal Conservation, 19, 189–198.

  • Gaynor, K. M., Hojnowski, C. E., Carter, N. H., & Brashares, J. S. (2018). The Influence of Human Disturbance on Wildlife Nocturnality. Science, 360, 1232–1235.

    Article  CAS  PubMed  Google Scholar 

  • Golden, C. D. (2009). Bushmeat Hunting and Use in the Makira Forest, North-Eastern Madagascar: A Conservation and Livelihoods Issue. Oryx, 43(03), 386.

    Article  Google Scholar 

  • Goodman, S. M. (2003). Predation on lemurs. In S. M. Goodman & J. P. Benstead (Eds.), The Natural History of Madagascar (pp. 1159–1186). University of Chicago Press.

    Chapter  Google Scholar 

  • Goodman, S. M., Langrand, O., & Rasolonandrasana, B. P. N. (1997). The Food Habits of Cryptoprocta ferox in the High Mountain Zone of the Andringitra Massif, Madagascar (Carnivora, Viverridae). Mammalia, 61(2), 185–192.

    Article  Google Scholar 

  • Hawkins, C. E. (1998). Behavior and Ecology of the Fossa, Cryptoprocta Ferox (Carnivora: Viverridae) in a Dry Deciduous Forest. University of Aberdeen.

    Google Scholar 

  • Karpanty, S. M., & Wright, P. C. (2007). Predation on Lemurs in the Rainforest of Madagascar by Multiple Predator Species: Observations and Experiments. In S. L. Gursky & K. A. I. Nekaris (Eds.), Primate Anti-Predator Strategies (pp. 77–99). Springer.

    Chapter  Google Scholar 

  • LaBarge, L. R., Hill, R. A., Berman, C. M., Margulis, S. W., & Allan, A. T. L. (2020). Anthropogenic Influences on Primate Antipredator Behavior and Implications for Research and Conservation. American Journal of Primatology, 82(2), e23087.

    Article  PubMed  Google Scholar 

  • LaFleur, M., Sauther, M., Cuozzo, F., Yamashita, N., Jacky Youssouf, I. A., & Bender, R. (2014). Cathemerality in Wild Ring-Tailed Lemurs (Lemur catta) in the Spiny Forest of Tsimanampetsotsa National Park: Camera Trap Data and Preliminary Behavioral Observations. Primates, 55, 207–217.

    Article  PubMed  Google Scholar 

  • Leblond, M., Dussault, C., Ouellet, J. P., St. Laurent, M. H., & Singh, N. (2016). Caribou Avoiding Wolves Face Increased Predation by Bears-Caught Between Scylla and Charybdis. Journal of Applied Ecology, 53(4), 1078-1087.

  • Lührs, M.-L., & Dammhahn, M. (2009). An Unusual Case of Cooperative Hunting in a Solitary Carnivore. Journal of Ethology, 28(2), 379–383.

    Article  Google Scholar 

  • MacKenzie, D. I., & Hines, J. E. (2022). RPresence: R Interface for Program PRESENCE. R package version 2.13.41.

  • MacKenzie, D. I., Nichols, J. D., Lachman, G. B., Droege, S., Royle, J. A., & Langtimm, C. A. (2002). Estimating Site Occupancy Rates When Detection Probabilities Are Less Than One. Ecology, 83(8), 2248–2255.

    Article  Google Scholar 

  • McComb, K., Shannon, G., Durant, S. M., Sayialel, K., Slotow, R., Poole, J., & Moss, C. (2011). Leadership in Elephants: The Adaptive Value of Age. Proceedings of the Royal Society b: Biological Sciences, 278(1722), 3270–3276.

    Article  PubMed Central  Google Scholar 

  • McComb, K., Shannon, G., Sayialel, K. N., & Moss, C. (2014). Elephants Can Determine Ethnicity, Gender, and Age from Acoustic Cues in Human Voices. Proceedings of the National Academy of Sciences of the United States of America, 111(14), 5433–5438.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Merson, S. D., Dollar, L. J., Tan, C. K. W., & Macdonald, D. W. (2019). Effects of Habitat Alteration and Disturbance by Humans and Exotic Species on Fosa Cryptoprocta ferox Occupancy in Madagascar’s Deciduous Forests. Oryx, 54(6), 828–836.

    Article  Google Scholar 

  • Merson, S. D., Dollar, L. J., Tan, C. K. W., & Macdonald, D. W. (2018). Activity Patterns of Sympatric Living Exotic and Endemic Carnivores (the Fosa) in Western Madagascar’s Deciduous Forests. Journal of Zoology, 307(3), 186–194.

    Article  Google Scholar 

  • Mittermeier, R. A., Louis Jr., E. E., Richardson, M., Schwitzer, C., Langrand, O., Rylands, A. B., Hawkins, F., Rajaobelina, S., Ratsimbazafy, J., …., Rasoloarison, R. (2010). Lemurs of Madagascar, Third Edition. Conservation International.

  • Nowak, K., le Roux, A., Richards, S. A., Scheijen, C. P. J., & Hill, R. A. (2014). Human Observers Impact Habituated Samango Monkeys’ Perceived Landscape of Fear. Behavioral Ecology, 25(5), 1199–1204.

    Article  Google Scholar 

  • R Core Team. (2021). R: A Language and Environment for Statistical Computing. (Version 4.1.2). R Foundation for Statistical Computing.

  • Ramananjato, V., Randimbiarison, F., Rabarijaonina, T., & Razafindratsima, O. H. (2022). Arboreal Mouse Lemurs Discovered Sleeping in a Burrow on the Ground. Ecology and Evolution, 12(12), e9543.

    Article  PubMed  PubMed Central  Google Scholar 

  • Richmond, O. M. W., Hines, J. E., & Beissinger, S. R. (2010). Two-Species Occupancy Models: A New Parameterization Applied to Co-Occurrence of Secretive Rails. Ecological Applications, 20(7), 2036–2046.

    Article  PubMed  Google Scholar 

  • Ridout, M., & Linkie, M. (2009). Estimating Overlap of Daily Activity Patterns from Camera Trap Data. Journal of Agricultural, Biological, and Environmental Statistics, 14(3), 322–337.

    Article  Google Scholar 

  • Rivera, K., Fidino, M., Farris, Z. J., Magle, S. B., Murphy, A., & Gerber, B. D. (2022). Rethinking Habitat Occupancy Modeling and the Role of Diel Activity in an Anthropogenic World. The American Naturalist, 200(4), 720714.

    Article  Google Scholar 

  • Rowcliffe, M. (2021). activity: Animal Activity Statistics. R package version 1.3.1.

  • Samson, D. R., & Hunt, K. D. (2012). A Thermodynamic Comparison of Arboreal and Terrestrial Sleeping Sites for Dry-Habitat Chimpanzees (Pan troglodytes schweinfurthii) at the Toro-Semliki Wildlife Reserve, Uganda. American Journal of Primatology, 74(9), 811–818.

    Article  PubMed  Google Scholar 

  • Schnoell, A. V., & Fichtel, C. (2011). Predation on Redfronted Lemurs (Eulemur rufifrons) by Fossas (Cryptoprocta ferox). Lemur News, 16, 30–32.

    Google Scholar 

  • Smith, J. A., Suraci, J. P., Clinchy, M., Crawford, A., Roberts, D., Zanette, L. Y., & Wilmers, C. C. (2017). Fear of the Human “Super Predator” Reduces Feeding Time in Large Carnivores. Proceedings of the Royal Society B: Biological Sciences, 284(1857), 20170433.

    Article  PubMed Central  Google Scholar 

  • Souza-Alves, J. P., Baccaro, F. B., Fontes, I. P., Oliveira, M. A., Silva, N. M. O., & Barnett, A. A. (2021). For Emergency Only: Terrestrial Feeding in Coimbra-Filho’s Titis Reflects Seasonal Arboreal Resource Availability. Primates, 62(1), 199–206.

    Article  PubMed  Google Scholar 

  • Souza-Alves, J. P., Mourthe, I., Hilário, R. R., Bicca-Marques, J. C., Rehg, J., Gestich, C. C., Acero-Murcia, A. C., Adret, P., Aquino, R., ...., Berthet, M. (2019). Terrestrial Behavior in Titi Monkeys (Callicebus, Cheracebus, and Plecturocebus): Potential Correlates, Patterns, and Differences between Genera. International Journal of Primatology, 40(4-5), 553-572.

  • Suraci, J. P., Clinchy, M., Zanette, L. Y., & Wilmers, C. C. (2019). Fear of Humans as Apex Predators Has Landscape-Scale Impacts from Mountain Lions to Mice. Ecology Letters, 22(10), 1578–1586.

    Article  PubMed  Google Scholar 

  • Tucker, M. A., Bohning-Gaese, K., Fagan, W. F., Fryxell, J. M., Van Moorter, B., Alberts, S. C., Ali, A. H., Allen, A. M., Attias, N., ...., Avgar, T. (2018). Moving in the Anthropocene: Global reductions in terrestrial mammalian movements. Science, 359(6374), 466-469.

  • Vazquez, C., Rowcliffe, J. M., Spoelstra, K., & Jansen, P. A. (2019). Comparing diel activity patterns of wildlife across latitudes and seasons: time transformations using day length. Methods in Ecology and Evolution, 10, 2057–2066.

  • Wampole, E. M., Gerber, B. D., Farris, Z. J., Razafimahaimodison, J. C., Andrianarisoa, M. H., Ralazampirenena, C. J., Wright, P. C., Rasamisoa, C. D., Gibson, D., ...., Tobler, M. W. (2022). Madagascar terrestrial camera survey database 2021: A collation of protected forest camera surveys from 2007-2021. Ecology, 103(6), e3687.

  • Widén, A., Clinchy, M., Felton, A. M., Hofmeester, T. R., Kuijper, D. P. J., Singh, N. J., Widemo, F., Zanette, L. Y., & Cromsigt, J. P. G. M. (2022). Playbacks of predator vocalizations reduce crop damage by ungulates. Agriculture, Ecosystems & Environment, 328, j.agee.2022.107853.

  • Williamson, R. E., Webb, S. E., Dubreuil, C., Lopez, R., Cheves Hernandez, S., Fedigan, L. M., & Melin, A. D. (2021). Sharing Spaces: Niche Differentiation in Diet and Substrate Use among Wild Capuchin Monkeys. Animal Behaviour, 179, 317–338.

    Article  Google Scholar 

  • Wyza, E., Dollar, L., Rahajanirina, L. P., Popescu, V., & Stevens, N. J. (2020). Spatial Dynamics and Activity Patterns of the Fosa Cryptoprocta ferox in Ankarafantsika National Park, Madagascar: Carnivores Navigating a Human-Influenced Landscape. Oryx, 54(6), 837–846.

    Article  Google Scholar 

  • Zanette, L. Y., & Clinchy, M. (2020). Ecology and Neurobiology of Fear in Free-Living Wildlife. Annual Review of Ecology, Evolution, and Systematics, 51(1), 297–318.

    Article  Google Scholar 

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The authors thank Wampole et al. (2022) for providing open access to the camera trap surveys across Madagascar and the Malagasy researchers who helped to collect the data. They also thank the UC Santa Cruz Science Internship Program for connecting the two authors and providing the funding to conduct the analyses.

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K.G. conceived the project and hypotheses and wrote the first draft of the manuscript. A.M. ran the analyses and revised the manuscript.

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Correspondence to Asia Murphy.

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Handling Editor: Onja H. Razafindratsima

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Garg, K., Murphy, A. Arboreal Lemur Terrestriality is Influenced by When and Where Predators are Present. Int J Primatol 44, 1166–1181 (2023).

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