Predictions of Seed Shadows Generated by Common Brown Lemurs (Eulemur fulvus) and Their Relationship to Seasonal Behavioral Strategies
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Frugivorous primates in the family Lemuridae, the largest seed dispersers in Madagascar, often modify their behavior dramatically to cope with seasonal fluctuations in food availability and climate. Such behavioral strategies influence seed dispersal distances and seed shadows, which determine seed fate, gene flow, and the geographical range expansion of plant populations. To examine seasonal variation in seed shadows generated by the common brown lemur (Eulemur fulvus), I combined data on movements of a wild group of lemurs in northwestern Madagascar from full-day observations made twice weekly for 1 year and full-night observations made once a fortnight during the dry season, with gut passage times for three captive individuals in a Malagasy zoo. During the rainy season, brown lemurs increased traveling effort (mean daily path lengths: 1172 ± SE 59 m), adopting a high-cost/high-yield foraging strategy to maximize harvest under periods of fruit abundance; this resulted in long seed dispersal distances (median: 170 ± MAD 77 m). During the dry season, daily path lengths (mean: 469 ± SE 30 m) were shorter owing to midday resting and consumption of water-rich succulent leaves, probably to avoid overheating and dehydration. These behaviors led to short-distance seed dispersal (median: 75 ± MAD 47 m). Although brown lemurs moved nocturnally during the dry season (mean nightly path lengths: 304 ± SE 58 m), nocturnal seed dispersal distances were short (median: 34 ± MAD 21 m). This seasonal variation in seed shadows might cause different population dynamics for rainy- and dry-season-fruiting species of large-seeded plants that depend on brown lemurs for seed dispersal. Additionally, lemur-facilitated seed dispersal distances were shorter than those of large frugivores elsewhere in the world. Therefore, lemur-mediated seed dispersal systems are likely to be vulnerable to forest fragmentation, which can isolate new recruits and prevent gene flow among plant metapopulations.
KeywordsLarge frugivores Madagascar Movement patterns Seasonality Seed dispersal distance
The author is grateful to A. Mori, H. F. Rakotomanana, F. Rakotondraparany, and all members of the Antananarivo-Kyoto University research team for their support in carrying out fieldwork; to G. Yamakoshi, A. Mori, and N. Nakagawa for their research guidance; and to all of the staff at Ankarafantsika National Park and Tsimbazaza Botanical and Zoological Park for giving permission to conduct this research. I thank O. Razafindratsima, Y. Tsuji, and L. Culot for co-organizing the special issue “Advances and Frontiers in Primate Seed Dispersal” in the International Journal of Primatology. I also thank J. M. Setchell, the editor-in-chief, and the three anonymous reviewers for their constructive comments and useful suggestions to improve my manuscript. This work was supported by the Japan Society for the Promotion of Science (JSPS) Grants-in-Aid for Scientific Research (Nos. 17405008 and 21-3399).
- Andresen, E. (1999). Seed dispersal by monkeys and the fate of dispersed seeds in a Peruvian rain forest. Biotropica, 31, 145–158.Google Scholar
- Campera, M., Serra, V., Balestri, M., Barresi, M., Ravaolahy, M., Randriatafika, F., & Donati, G. (2014). Effects of habitat quality and seasonality on ranging patterns of collared brown lemur (Eulemur collaris) in littoral forest fragments. International Journal of Primatology, 35, 957–975.CrossRefGoogle Scholar
- Comita, L. S., Queenborough, S. A., Murphy, S. J., Eck, J. L., Xu, K., Krishnadas, M., Beckman, N., Zhu, Y., & Gómez-Aparicio, L. (2014). Testing predictions of the Janzen-Connell hypothesis: A meta-analysis of experimental evidence for distance and density-dependent seed and seedling survival. Journal of Ecology, 102, 845–856.PubMedCrossRefGoogle Scholar
- Connell, J. H. (1971). On the role of natural enemies in preventing competitive exclusion in some marine animals and in rain forest trees. In P. J. Den Boer & G. Gradwell (Eds.), Dynamics of populations (pp. 298–312). Wageningen: PUDOC.Google Scholar
- Estrada, A., Garber, P. A., Rylands, A. B., Roos, C., Fernandez-Duque, E., di Fiore, A., 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., de Guinea, M., Gouveia, S., Dobrovolski, R., Shanee, S., Shanee, N., Boyle, S. A., Fuentes, A., MacKinnon, K. C., Amato, K. R., Meyer, A. L. S., Wich, S., Sussman, R. W., Pan, R., Kone, I., & Li, B. (2017). Impending extinction crisis of the world's primates: Why primates matter. Science Advances, 3, e1600946.PubMedPubMedCentralCrossRefGoogle Scholar
- Federman, S., Dornburg, A., Daly, D. C., Downie, A., Perry, G. H., et al. (2016). Implications of lemuriform extinctions for the Malagasy flora. Proceedings of the National Academy of Sciences of the USA, 113, 5041–5046.Google Scholar
- Godfrey, L. R., Jungers, W. L., Schwartz, G. T., & Irwin, M. T. (2008). Ghosts and orphans: Madagascar’s vanishing ecosystems. In J. G. Fleagle, & C. C. Gilbert (Eds.), Elwyn Simons: A research for origins (pp. 361–395). Developments in primatology: Progress and prospects. New York: Springer science+business media.Google Scholar
- Holbrook, K. M., & Loiselle, B. A. (2007). Using toucan-generated dispersal models to estimate seed dispersal in Amazonian Ecuador. In A. J. Dennis, E. W. Schupp, R. J. Green, & D. A. Westcott (Eds.), Seed dispersal: Theory and its application in a changing world (pp. 300–321). Wallingford: CAB International.CrossRefGoogle Scholar
- Jordano, P., Garcia, C., Godoy, J. A., & Garcia-Castano, J. L. (2007). Differential contribution of frugivores to complex seed dispersal patterns. Proceedings of the National Academy of Sciences of the USA, 104, 3278–3282.Google Scholar
- Jury, M. R. (2003). The climate of Madagascar. In S. M. Goodman & J. P. Benstead (Eds.), The natural history of Madagascar (pp. 75–87). Chicago: University of Chicago Press.Google Scholar
- Koike, S., Masaki, T., Nemoto, Y., Kozakai, C., Yamazaki, K., Kasai, S., Nakajima, A., & Kaji, K. (2011). Estimate of the seed shadow created by the Asiatic black bear Ursus thibetanus and its characteristics as a seed disperser in Japanese cool-temperate forest. Oikos, 120, 280–290.CrossRefGoogle Scholar
- Kutner, M., Nachtsheim, C., Neter, J., & Wasserman, W. (2004). Applied linear statistical model, 5th ed. New York: McGraw-Hill/Irwin.Google Scholar
- McConkey, K. R. (2018). Seed dispersal by primates in Asian habitats: From species, to communities, to conservation. International Journal of Primatology. https://doi.org/10.1007/s10764-017-0013-7.
- Milton, K. (1984). The role of food-processing factors in primate food choice. In P. S. Rodman & J. G. H. Cant (Eds.), Adaptations of foraging in nonhuman primates (pp. 249–279). New York: Columbia University Press.Google Scholar
- Rasmussen, M. A. (1999). Ecological influences on activity cycle in two cathemeral primates, the mongoose lemur (Eulemur mongoz) and the common brown lemur (Eulemur fulvus fulvus). Ph.D. thesis, Duke University.Google Scholar