FSD 2010 - SCRAT and Relatives

5th International Symposium-Workshop on Frugivores and Seed Dispersal (1985-2010)

Seed Caching Rat (SCRAT) and Relatives

All Rodents are not Rats, but all Rats are Rodents

Rodentia comprise over 2000 living species in about 30 families, and are present almost everywhere on the planet but one continent (Antartica), New Zealand, and on some oceanic islands. They colonized almost all biomes, from desert to forest, living beneath and/or above the ground to the top of the canopy of tropical rainforests. Rodents range in size from 5 g to 70 kg. The diet of rodents is diverse, omnivorous, and they are eating invertebrates, fungi, flowers, leaves, fruit and seeds. Often, as invertebrates (ants, wasps) or other vertebrates (birds, carnivores, marsupial), rodents hoard food in the rich season and consume during the season of scarcity. The first comprehensive synthesis of the literature on food hoarding in animals was published by Stephen B. Vander Wall (1990).

Scatterhoarding Behavior

Here, a video (© The Agouti Enterprise) showing an agouti (Dasyprocta punctata) scatterhoarding fruit of Astrocaryum standleyanum palm tree at Barro Colorado island (Panama).

Hoarding behavior is when an animal store its food within a cache, in times of surplus, for times when food is less plentiful. Caches are either aggregated (larder) and/or isolated (scatter). The second type of caching is most frequent when animals do not use regular burrow or den, and when they can't defend a large concentration of stored food. Food supply is thus dispersed throughout the entire home range, generally at some distances from the sources, as a function of seed nutritional value. Since the seminal papers by Cahalane (1942) and Morris (1962) about scatterhoarding by temperate and tropical rodents, respectively, many authors (Figure below) have been documenting this scatterhoarding behavior and the consequences for seed dispersal and plant recruitment in a variety of habitats.

Since then, the number of published papers increased (Figure right), especially in the last decade as shown by the figure of the number of articles about 'scatterhoarding rodent' published by Springer (see AuthorMapper.com). A similar survey of the literature indexed by ISI, gives 129 references (pdf 1-100; 101-129) until June 2009.

Key Scatterhoarders

Herebelow illustrations of some rodent species in studies on scatterhoarding and seed dispersal in various habitats (© authors or web with link)

Desert to Mediterranean-type shrubby vegetation and rocky areas

Panamint kangaroo rat (Dipodomys panamintinus)

Mice (Acomys)

Degu (Octodon degus)

Chipmunks dispersing Manzanita seeds

Temperate forests

Squirrel (Sciurus)

Chipmunck (Tamias)

Woodmice (Apodemus)

Tropical America

Spiny rats (Proechimys sp.)© Pierre-Michel Forget

Acouchy (Myoprocta pratti)© Patrick Jansen

Agouti (Dasyprocta punctata) © Pierre-Michel Forget

Africa

Western Palm Squirrel (Epixerus ebii)

African Giant Pouched Rats (Cricetomys emini )

Red-legged Sun Squirrel (Heliosciurus rufobranchium)

Eastern Asia, New Guinea and Australia

Giant White-tailed Rat (Uromys caudimaculatus)© David & Diane Armbrust

Three-striped Ground Squirrel (Lariscus insignis)© Masatoshi Yasuda

Long-tailed Giant Rat (Leopoldamys sabanus)

Experts of Seed Dispersal by Rodents

Adler, Greg

Brewer, Stephen

Forget, Pierre-Michel

Galetti, Mauro

Hoshizaki, Kazuhiko (top, left) and Yabe, Tsuneaki (right)

Kitamura, Shumpei

Jansen, Patrick

Kuprewicz, Erin

Steele, Mike (middle, right)

Theimer, Tad (middle, left)

Midgley, Jeremy

Tamura, Noriko

Vander Wall, Stephen

Yasuda, Masatoshi (bottom, right, with Corlett, Richard, left)

Zhang, Zhibin

(Photos taken at FSD2005, Brisbane Australia.© Pierre-Michel Forget)

References (a selection) * FSD Symposium-Workshop (1985-2005)

Brewer, S. W. 2001. Predation and dispersal of large and small seeds of a tropical palm. Oikos 92:245-255.

Cahalane, V. H. 1942. Caching and recovery of food by the Western fox squirrel. Journal of Wildlife Management 6:338-352.

Chang, G., et al. 2009. Hoarding decisions by Edward's long-tailed rats (Leopoldamys edwardsi) and South China field mice (Apodemus draco): The responses to seed size and germination schedule in acorns. Behavioural Processes, In Press

Dennis, A. J. 2003. Scatter-hoarding by musky rat-kangoroos, Hypsiprymnodon moschatus, a tropical rain-forest marsupial from Australia: implications for seed dispersal. Journal of Tropical Ecology 19:619-627.

Dennis, A., G. J. Lipsett-Moore, G. Harrington, E. Collins, and D. Westcott. 2005. Seed predation, seed dispersal and habitat ragmentation: does context make a difference in tropical Australia? Pages 117-135 in P.-M. Forget, et al. CABI publishing.*

Emmons, L. H. 1980. Ecology and resource partitioning among nine species of African rain forest squirrels. Ecological Monograph 50:31-54.

Forget, P.-M. 1990. Seed-dispersal of Vouacapoua americana (Caesalpiniaceae) by caviomorph rodents in French Guiana. Journal of Tropical Ecology 6:459-468. pdf

Forget, P.-M. and T. Milleron. 1991. Evidence for secondary seed dispersal in Panama. Oecologia 87:596-599. pdf

Forget, P.-M., D. Hammond, T. Milleron, and R. Thomas. 2002. Seasonality of fruiting and food hoarding by rodents in Neotropical forests: consequences for seed dispersal and seedling recruitment. Pages 241-253 in D. J. Levey et al. CABI Publishing.*

Forget, P.-M., A. J. Dennis, S. J. Mazer, P. A. Jansen, S. Kitamura, J. E. Lambert, and W. D. A. 2007. Seed allometry and disperser assemblages in tropical rainforests: a comparison of four floras on different continents. Pages 5-36 in A. Dennis, et al. CABI Publishing.*

Forget, P. M., and S. B. V. Wall. 2001. Scatter-hoarding rodents and marsupials: convergent evolution on diverging continents. Trends in Ecology & Evolution 16:65-67.*

Hallwachs, W. 1986. Agoutis Dasyprocta punctata : the inheritors of guapinol Hymenaea courbaril (Leguminosae). Pages 119-135 in R. Estrada and T. H. Fleming, Dr. W. Junk Publishers.

Hoshizaki, K., et al. 1997. Impacts of secondary seed dispersal and herbivory on seedling survival in Aesculus turbinata. Journal of Vegetation Science 8: 735-742

Hoshizaki, K., and P. E. Hulme. 2002. Mast seeding and predator-mediated indirect interactions in a forest community: evidence from post- dispersal fate of rodent-generated caches. Pages 227-239 in D. J. Levey et al. CABI Publishing.*

Hulme, P. E. 2002. Seed eaters: seed dispersal, destruction, and demography. Pages 257-273 in D. J. Levey et al. CABI Publishing.*

Janzen, D. H. 1986. Mice, big mammals, and seeds: it matters who defecates what where. Pages 251-271 in A. Estrada and T. H. Fleming. Dr. W. Junk Publishers, Dordrecht.*

Jansen, P. A., et al. 2002. The role of seed size in dispersal by a scatter-hoarding rodent. Pages 209-225 in in D. J. Levey et al. CABI Publishing.*

Jansen, P. A., et al. 2004. Seed mass and mast seeding enhance dispersal by a neotropical scatter-hoarding rodents. Ecological Monograph 74:569-589.

Kitamura, S., et al. 2008. Rare seed-predating mammals determine seed fate of Canarium euphyllum, a large-seeded tree species in a moist evergreen forest, Thailand. Ecological Research 23: 169–177.

Midgley, J. J., Anderson, B. 2005. Scatterhoarding in mediterranean shrublands of the SW Cape, South Africa. Pages 197-204 in Forget, P. M., at al. CABI Publishing.

Morris, D. O. 1962. The behavior of the green acouchi (Myoprocta pratti) with special reference to scatterhoarding. Proceedings of the Royal Zoological Society 139: 701-732.

Smythe, N. 1978. The natural history of the Central American agouti (Dasyprocta punctata). Smithsonian Contribution to Zoology 257: 1-52.

Stapanian, M. A. 1986. Seed dispersal by birds and squirrels in the deciduous forests of the United States. Pages 225-236 in A. Estrada and T. H. Fleming, Dr. W. Junk Publishers, The Hagues.*

Stapanian, M. A. and C. C. Smith. 1978. A model for seed scatterhoarding: coevolution of fox squirrels and black walnuts. Ecology 59:884-896.

Stapanian, M. A. and C. C. Smith. 1986. How fox squirrels influence the invasion of prairies by nut-bearing trees. Journal of Mammalogy 67:326-332.

Steele, M. A., et al. 1996. Caching and feeding decisison by Sciurus carolinensis: responses to weevil-infested acorns. Journal of Mammalogy 77:305-314.

Steele, M. A., et al. 1993. Tannins and partial consumption of acorns: implications for dispersal of oaks by seed predators. Midl. Nat. 130:229-238.

Theimer, T. C. 2001. Seed scatterhoarding by white-tailed rats: consequences for seedling recruitment by an Australian rain forest tree. Journal of Tropical Ecology 17:177-189.

Vander Wall, S. B. 1990. Food Hoarding in Animals. Chicago University Press, Chicago.

Vander Wall, S. B. 1991. Mechanisms of cache recovery by yellow pine Chipmunk. Animal Behavior 41:851-863.

Vander Wall, S. B. 1993. Cache site selection by Chipmunk (Tamias spp.) and its influence on the effectiveness of seed dispersal in jeffrey pine (Pinus jeffreyi). Oecologia 96:246-252.

Vander Wall, S. B. 2002. Secondary dispersal of Jeffrey pine seeds by rodent scatter hoarders: the roles of pilfering, recaching, and a variable environment. Pages 193-208 in D. J. Levey et al. CABI Publishing.*

Wenny, D. G. 1999. Two-stage dispersal of Guarea glabra and G. kunthiana (Meliaceae) in Monteverde, Costa Rica. Journal of Tropical Ecology 15:481-496.

Xiao, Z.-S. and Z.-B. Zhang. 2003. How to trace seeds and fruits dispersed by frugivorous animals: a review. Biodiversity Science 11:248-255. (in Chinese with English summary).

Yasuda, M., et al. 2000. Evidence for hoarding behaviour in terrestrial rodents in Pasoh Forest reserve, a Malaysian lowland rain forest. Journal of Tropical Forest Science 12:164-173.

Wang, W and Ma, Ke-Ping. 1998. Predation and dispersal of Quercus liatungensis by Chinese rock Squirrels and Eurasian jay. Acta Botanica Sinica 41: 1142-1144.

Zhang, H. et al. 2008. Effects of seed abundance on seed scatter-hoarding of Edward’s rat (Leopoldamys edwardsi Muridae) at the individual level. Oecologia 158:57–63.

Zhang, Z, et al. 2005. Impact of small rodents on tree seeds in temperate and subtropical forests, China. Page 269-2282 in P.-M. Forget, et al. CABI Publishing.

Websites

The role of scatterhoarding in the regeneration of rodent-dispersed rainforest trees in French Guiana

Carapa.org - Seed dispersal by rodents

About Agouti and Brazil nut The agouti's nutty friend

The agouti enterprise

Agoutis and Seed Dispersal in Tropical Rainforest

Sciuridae.org (Sciurus - Tamiasciurus - Spermophilus - Cynomys)

Smithsonian Institution - Sciuridae - Muridae

Lodgepole Chipmunk Tamias speciosus

Chipmunks disperse Manzanita seeds

Tree-rodent interactions in Kanumazawa Riparian Forest, northern Japan