Scatter-hoarding animals decide their food hoarding location by assessing food quality and pilfering risk. Previous studies have proposed two non-mutually exclusive hypotheses; the optimal density model (ODM) and the habitat structure hypothesis (HSH). The ODM proposes that animals utilize low cache density to protect their valuable caches by transporting food far from food sources. The HSH proposes that animals utilize predation risk to protect their valuable caches by hoarding food in open areas. Here, we investigated the hoarding behaviours in Eurasian red squirrels Sciurus vulgaris by experimentally providing high-quality (walnuts) and low-quality (acorns) food, to examine if they follow ODM or HSH. Compared to acorns, squirrels hoarded walnuts in places further from the area where food was provisioned and in areas with low canopy cover. These results agree with both ODM and HSH, providing the first evidence that hoarding behaviour in Eurasian red squirrels is shaped by multiple factors.
Purchase
Buy instant access (PDF download and unlimited online access):
Institutional Login
Log in with Open Athens, Shibboleth, or your institutional credentials
Personal login
Log in with your brill.com account
Bartoń, K. (2022). MuMIn: multi-model inference. R package version 1.46.00. — Available online at https://CRAN.R-project.org/package=MuMIn.
Bates, D., Mächler, M., Bolker, B.M. & Walker, S.C. (2015). Fitting linear mixed-effects models using lme4. — J. Stat. Softw. 67: 1-48.
Brodin, A. (2010). The history of scatter hoarding studies. — Phil. Trans. Roy. Soc. Lond. B: Biol. Sci. 365: 869-881.
Brooks, M.E., Kristensen, K., van Benthem, K.J., Magnusson, A., Berg, C.W., Nielsen, A., Skaug, H.J., Machler, M. & Bolker, B.M. (2017). glmmTMB balances speed and flexibility among packages for zero-inflated generalized linear mixed modeling. — R J. 9: 378-400.
Clarkson, K., Eden, S.F., Sutherland, W.J. & Houston, A.I. (1986). Density dependence and magpie food hoarding. — J. Anim. Ecol. 55: 111-121.
Dally, J.M., Emery, N.J. & Clayton, N.S. (2004). Cache protection strategies by western scrub-jays (Aphelocoma californica): hiding food in the shade. — Proc. R. Soc. Lond. B 271: S387-S390.
Dally, J.M., Emery, N.J. & Clayton, N.S. (2005). Cache protection strategies by western scrub-jays, Aphelocoma californica: implications for social cognition. — Anim. Behav. 70: 1251-1263.
Dally, J.M., Clayton, N.S. & Emery, N.J. (2006). The behavior and evolution of cache protection and pilferage. — Anim. Behav. 72: 13-23.
Delgado, M.M., Nicholas, M., Petrie, D.J. & Jacobs, L.F. (2014). Fox squirrels match food assessment and cache effort to value and scarcity. — PLoS ONE 9: e92892.
Douma, J.C. & Weedon, J.T. (2019). Analysing continuous proportions in ecology and evolution: a practical introduction to beta and Dirichlet regression. — Methods Ecol. Evol. 10: 1412-1430.
Fox, J. & Weisberg, S. (2018). An R companion to applied regression. — Sage, Los Angeles, CA.
Goto, S. & Hayashida, M. (2002). Seed dispersal by rodents and seedling establishment of walnut trees (Juglans ailanthifolia) in a riparian forest. — J. Jpn. For. Soc. 84: 1-8.
Hasegawa, S. (1984). Basic studies on the conservation of the natural coastal forests in Hokkaido: the structure and regeneration of Quercus dentata THUNB forest in Ishikari. — Bull Hokkaido Univ 41: 313-422 (in Japanese with English summary).
Havera, S.P. & Smith, K.E. (1979). A nutritional comparison of selected fox squirrel foods. — J. Wildl. Manag. 43: 691-704.
Heinrich, B. (1999). Mind of the raven. — Harper Collins, New York, NY.
Hewitt, N. (1998). Seed size and shade-tolerance: a comparative analysis of North American temperate trees. — Oecologia 114: 432-440.
Hurly, T.A. & Robertson, R.J. (1987). Scatterhoarding by territorial red squirrels: a test of the optimal density model. — Can. J. Zool. 65: 1247-1252.
James, P.C. & Verbeek, N.A.M. (1984). Temporal and energetic aspects of food storage in northwestern crows. — Ardea 72: 207-215.
Kenward, R.E. & Holm, J.L. (1993). On the replacement of the red squirrel in Britain: a phytotoxic explanation. — Proc. Roy. Soc. Lond. B: Biol. Sci. 251: 187-194.
Krebs, J.R. (1990). Food-storing birds: adaptive specialization in brain and behaviour? — Philos. Trans. Roy. Soc. Lond. B: Biol. Sci. 329: 153-160.
Leaver, L.A., Hopewell, L., Caldwell, C. & Mallarky, L. (2007). Audience effects on food caching in grey squirrels (Sciurus carolinensis): evidence for pilferage avoidance strategies. — Anim. Cogn. 10: 23-27.
Lichti, N.I., Steele, M.A. & Swihart, R.K. (2017). Seed fate and decision-making processes in scatter-hoarding rodents: seed fate and scatter-hoarder decision-making. — Biol. Rev. 92: 474-504.
Lichti, N.I., Dalgleish, H.J. & Steele, M.A. (2020). Interactions among shade, caching behavior, and predation risk may drive seed trait evolution in scatter-hoarded plants. — Diversity 12: 416.
Mollor, H. (1983). Foods and foraging behavior of Red (Sciurus vulgaris) and Grey (Sciurus carolinensis) squirrels. — Mammal. Rev. 13: 81-98.
Muñoz, A. & Bonal, R. (2011). Linking seed dispersal to cache protection strategies: seed dispersal and caching strategies. — J. Ecol. 99: 1016-1025.
Nakagawa, S. & Schielzeth, H. (2013). A general and simple method for obtaining R2 from generalized linear mixed-effects models. — Methods Ecol. Evol. 4: 133-142.
Obihiro City (2020). Weather data in Obihiro. — Available online at https://www15.j-server.com/LUCOBIHIRO/ns/tl.cgi/https%3a//www.city.obihiro.hokkaido.jp/seisakusuisinbu/kouhoukouchouka/c070101kisyou.html.
Preston, S.D. & Jacobs, L.F. (2005). Cache decision making: the effects of competition on cache decisions in Merriam’s kangaroo rat (Dipodomys merriami). — J. Comp. Psychol. 119: 187-196.
R Development Core Team (2022). R: a language and environment for statistical computing. — R Foundation for Statistical Computing, Vienna, Austria. Available online at http://www.r-project.org/.
Reher, S., Dausmann, K.H., Warnecke, L. & Turner, J.M. (2016). Food availability affects habitat use of Eurasian red squirrels (Sciurus vulgaris) in a semi-urban environment. — J. Mammal. 97: 1543-1554.
Shimamoto, T., Uchida, K., Koizumi, I., Matsui, M. & Yanagawa, H. (2020). No evidence of physiological stress in an urban animal: comparison of fecal cortisol metabolites between urban and rural Eurasian red squirrels. — Ecol. Res. 35: 243-251.
Smith, C.C. & Follmer, D. (1972). Food preferences of squirrels. — Ecology 53: 82-91.
Stapanian, M.A. & Smith, C.C. (1984). Survival of scatterhoarded nuts: an experimental approach. — Ecology 65: 1387-1396.
Stapanian, M.A. & Smith, C.C. (1978). A model for seed scatterhoarding: coevolution of fox squirrels and black walnuts. — Ecology 59: 884-896.
Steele, M.A., Halkin, S.L., Smallwood, P.D., Mckenna, T.J., Mitsopoulos, K. & Beam, P.D. (2008). Cache protection strategies of a scatter-hoarding rodent: do tree squirrels engage in behavioral deception?. — Anim. Behav. 75: 705-714.
Steele, M.A., Contreras, T.A., Hadj-Chikh, L.Z., Agosta, S.J., Smallwood, P.D. & Tomlinson, C.N. (2014). Do scatter hoarders trade off increased predation risks for lower rates of cache pilferage? — Behav. Ecol. 25: 206-215.
Steele, M.A., Rompré, G., Stratford, J.A., Zhang, H., Suchocki, M. & Marino, S. (2015). Scatterhoarding rodents favor higher predation risks for cache sites: the potential for predators to influence the seed dispersal process. — Integr. Zool. 10: 257-266.
Sundaram, M., Lichti, N.I., Widmar, N.J.O. & Swihart, R.K. (2018). Eastern gray squirrels are consistent shoppers of seed traits: insights from discrete choice experiments. — Integr. Zool. 13: 280-296.
Sundaram, M., Higdon, A.E., Wood, K.V., Bonham, C.C. & Swihart, R.K. (2020). Mechanisms underlying detection of seed dormancy by a scatter-hoarding rodent. — Integr. Zool. 15: 89-102.
Uchida, K., Suzuki, K., Shimamoto, T., Yanagawa, H. & Koizumi, I. (2016). Seasonal variation of flight initiation distance in Eurasian red squirrels in urban versus rural habitat. — J. Zool. 298: 225-231.
Uchida, K., Suzuki, K., Shimamoto, T., Yanagawa, H. & Koizumi, I. (2019). Decreased vigilance or habituation to humans? Mechanisms on increased boldness in urban animals. — Behav. Ecol. 30: 1583-1590.
Uchida, K., Shimamoto, T., Yanagawa, H. & Koizumi, I. (2020). Comparison of the multiple behavioral traits between urban and rural squirrels. — Urban Ecosyst. 23: 745-754.
Van Horik, J. & Burns, K.C. (2007). Cache spacing patterns and reciprocal cache theft in New Zealand robins. — Anim. Behav. 73: 1043-1049.
Vander Wall, S.B. (2001). The evolutionary ecology of nut dispersal. — Bot. Rev. 67: 74-117.
Vander Wall, S.B. & Jenkins, S.H. (2003). Reciprocal pilfering and the evolution of food-hoarding behavior. — Behav. Ecol. 14: 656-667.
Waite, T.A. (1990). Effects of caching supplemental food on induced feather regeneration in wintering gray jays Perisoreus canadensis: a ptilochronology study. — Ornis Scand. 21: 122-128.
Wang, B. (2020). Neighbour effects do not always show consistent patterns, contrast of seed trait matters: evidence from a seed-rodent mutualism study. — Behav. Ecol. Sociobiol. 74: 119.
Wauters, L.A. & Casale, P. (1996). Long-term scatterhoarding by Eurasian red squirrels (Sciurus vulgaris). — J. Zool. 238: 195-207.
Wauters, L.A., Suhonen, J. & Dhondt, A.A. (1995). Fitness consequences of hoarding behavior in the Eurasian red squirrel. — Proc. Roy. Soc. Lond. B: Biol. Sci. 262: 277-281.
Wauters, L.A., Gurnell, J., Martinoli, A. & Tosi, G. (2001). Does interspecific competition with introduced grey squirrels affect foraging and food choice of Eurasian red squirrels?. — Anim. Behav. 61: 1079-1091.
Xiao, Z., Holyoak, M., Krebs, C.J. & Huang, X. (2022). Palatability and profitability of co-occurring seeds alter indirect interactions among rodent-dispersed trees. — Integr. Zool. 17: 206-216.
| All Time | Past 365 days | Past 30 Days | |
|---|---|---|---|
| Abstract Views | 1385 | 342 | 18 |
| Full Text Views | 340 | 18 | 1 |
| PDF Views & Downloads | 595 | 38 | 2 |
Scatter-hoarding animals decide their food hoarding location by assessing food quality and pilfering risk. Previous studies have proposed two non-mutually exclusive hypotheses; the optimal density model (ODM) and the habitat structure hypothesis (HSH). The ODM proposes that animals utilize low cache density to protect their valuable caches by transporting food far from food sources. The HSH proposes that animals utilize predation risk to protect their valuable caches by hoarding food in open areas. Here, we investigated the hoarding behaviours in Eurasian red squirrels Sciurus vulgaris by experimentally providing high-quality (walnuts) and low-quality (acorns) food, to examine if they follow ODM or HSH. Compared to acorns, squirrels hoarded walnuts in places further from the area where food was provisioned and in areas with low canopy cover. These results agree with both ODM and HSH, providing the first evidence that hoarding behaviour in Eurasian red squirrels is shaped by multiple factors.
| All Time | Past 365 days | Past 30 Days | |
|---|---|---|---|
| Abstract Views | 1385 | 342 | 18 |
| Full Text Views | 340 | 18 | 1 |
| PDF Views & Downloads | 595 | 38 | 2 |