Does caching strategy vary with microclimate in endangered Mt. Graham red squirrels?

Autoři: Calebe Pereira Mendes aff001;  John Koprowski aff002
Působiště autorů: Laboratório de Biologia da Conservação, Instituto de Biociências, Universidade Estadual Paulista “Júlio Mesquita Filho” (UNESP), Rio Claro, São Paulo, Brazil aff001;  School of Natural Resources and the Environment, University of Arizona, Tucson, Arizona, United States of America aff002
Vyšlo v časopise: PLoS ONE 14(11)
Kategorie: Research Article
doi: 10.1371/journal.pone.0224947


Food hoarding is a common behavior used by a variety of animals to cope with periods of low food availability. At the retreating edge of species’ distribution, the stressful environment and unfavourable climate conditions may impose severe costs on hoarding behavior. Since relict populations are hotspots for evolution and adaptation, and considering that food hoarding behavior has a strong evolutionary basis, we decided to evaluate the occurrence of behavioral variability in the amount of food cached by the endangered Mount Graham red squirrel (Tamiasciurus fremonti grahamensis). We tested the variation in cache size in response to microclimate, soil relief, vegetation, food availability and squirrel sex. The number of pits excavated by squirrels to cache cones was used as a proxy of cache size and was affected by mountain slope aspect and density of trees. More pits were excavated in the northeast facing slopes. The density of trees negatively affects the cache volume on southwest slopes, but not on northeast slopes. The sex of the resident squirrel also affects the number of pits in the squirrel midden, with males excavating 47% more pits than females. Males and females also presented different responses to the mountain slope aspect, with females excavating more pits on northeastern slopes than on southwestern slopes, whereas male cache size did not vary with the slope aspect. Finally, the squirrel’s caching behavior did not vary in response to midden microclimate variation, a result with possible implications for the survival of the Mt Graham red squirrels, given the predicted temperature increases in the region due to climate change.

Klíčová slova:

Animal behavior – Behavior – Climate change – Conifers – Forests – Mountains – principal component analysis – Squirrels


1. Sutton AO, Strickland D, Norris DR. Food storage in a changing world: implications of climate change for food-caching species. Clim Chang Responses. 2016;3: 12. doi: 10.1186/s40665-016-0025-0

2. Wall SB Vander. Food hoarding in animals. University of Chicago Press; 1990.

3. Hadj-Chikh LZ, Steele MA, Smallwood PD. Caching decisions by grey squirrels: a test of the handling time and perishability hypotheses. Anim Behav. 1996;52: 941–948. Available:

4. Preston SD, Jacobs LF. Mechanisms of cache decision making in fox squirrels (Sciurus niger). J Mammal. 2009;90: 787–795. doi: 10.1644/08-MAMM-A-254.1

5. Tamura N, Hashimoto Y, Hayashi F. Optimal distances for squirrels to transport and hoard walnuts. Anim Behav. 1999;58: 635–642. doi: 10.1006/anbe.1999.1163 10479379

6. Smith CC. The coevolution of pine squirrels (Tamiasciurus) and conifers. Ecol Monogr. 1970;40: 349–371. doi: 10.2307/1942287

7. Cox PG, Rayfield EJ, Fagan MJ, Herrel A, Pataky TC, Jeffery N. Functional evolution of the feeding system in rodents. PLoS One. 2012;7: e36299. doi: 10.1371/journal.pone.0036299 22558427

8. Hurley T a, Robertson RJ. Variation in the food hoarding behaviour of red squirrels. Behav Ecol Sociobiol. 1990;26(2): 91–97.

9. Archibald DW, Fletcher QE, Boutin S, McAdam AG, Speakman JR, Humphries MM. Sex-specific hoarding behavior in North American red squirrels (Tamiasciurus hudsonicus). J Mammal. 2013;94: 761–770. doi: 10.1644/12-MAMM-A-213.1

10. Schauffert CA, Koprowski JL, Greer VL, Alanen MI, Hutton KA, Young PJ. Interactions between predators and Mt. Graham red squirrels (Tamiasciurus hudsonicus grahamensis). Southwest Nat. 2002;47: 498. doi: 10.2307/3672515

11. Gendron RP, Reichman OJ. Food perishability and inventory management: a comparison of three caching strategies. Am Nat. 1995;145: 948–968. Available:

12. Finley RB Jr. Cone caches and middens of Tamiasciurus in the Rocky Mountain region. Misc Publ Museum Nat Hist Univ Kansas. 1969;51: 233–273. Available:

13. Waite TA, Strickland D. Climate change and the demographic demise of a hoarding bird living on the edge. Proc R Soc B Biol Sci. 2006;273: 2809–2813. doi: 10.1098/rspb.2006.3667 17015367

14. Robertson BA, Rehage JS, Sih A. Ecological novelty and the emergence of evolutionary traps. Trends Ecol Evol. 2013;28: 552–560. doi: 10.1016/j.tree.2013.04.004 23756104

15. Gross K, Pasinelli G, Kunc HP. Behavioral plasticity allows short-term adjustment to a novel environment. Am Nat. 2010;176: 456lows s

16. Hampe A, Jump AS. Climate relicts: past, present, future. Annu Rev Ecol Evol Syst. 2011;42: 313–333. doi: 10.1146/annurev-ecolsys-102710-145015

17. Lesica P, Allendorf FW. When are peripheral populations valuable for conservation? Conserv Biol. 2015;9: 753–760.

18. Hope AG, Malaney JL, Bell KC, Salazar-Miralles F, Chavez AS, Barber BR, et al. Revision of widespread red squirrels (genus: Tamiasciurus) highlights the complexity of speciation within North American forests. Mol Phylogenet Evol. 2016;100: 170–182. doi: 10.1016/j.ympev.2016.04.014 27083861

19. Granillo KA, Froehlich GF. Mt. Graham red squirrel natural history and pre-observatory construction conservation efforts. In: Sanderson HR, Koprowski JL, editors. The last refuge of the Mt Graham red squirrel. The University of Arizona Press; 2009.

20. Goldstein EA, Merrick MJ, Koprowski JL. Functional semelparity drives population dynamics and endangers a peripheral population. Biol Conserv. 2017;205: 52–59. doi: 10.1016/j.biocon.2016.11.017

21. Koprowski JL, Doumas SL, Merrick MJ, Oleson B, Posthumus EE, Jessen TG, et al. It’s lonely at the top: biodiversity at risk to loss from climate change. Merging science and management in a rapidly changing world: Biodiversity and management of the Madrean Archipelago III and 7th Conference on Research and Resource Management in the Southwestern Deserts. Tucson, AZ, USA; 2013. pp. 53–59.

22. IPCC. Climate change 2014: Synthesis report. Contribution of working groups I, II and III to the Fifth assessment report of the Intergovernmental Panel on Climate Change. Geneva, Switzerland; 2014. doi: 10.1017/CBO9781107415324

23. Wong BBM, Candolin U. Behavioral responses to changing environments. Behav Ecol. 2015;26: 665–673. doi: 10.1093/beheco/aru183

24. Körner C. The use of “altitude” in ecological research. Trends Ecol Evol. 2007;22: 569–574. doi: 10.1016/j.tree.2007.09.006 17988759

25. Warshall P. The Madrean Sky Island Archipelago: a planetary overview. In: DeBano LH, Ffolliott PH, Ortega-Rubio A, Edminster GJG, Hamre RH, B. C, editors. Biodiversity and management of the Madrean Archipelago: The sky islands of Southwestern United States and Northwestern Mexico. Tucson, AZ, USA: Fort Collins, CO: U.S. Department of Agriculture, Forest Service, Rocky Mountain Forest and Range Experiment Station; 1995. pp. 6–18.

26. Correa-Metrio A, Bush M, Lozano-García S, Sosa-Nájera S. Millennial-scale temperature change velocity in the continental northern neotropics. PLoS One. 2013;8: 1–11. doi: 10.1371/journal.pone.0081958 24312614

27. Gurnell J. Home range, territoriality, caching behaviour and food supply of the red squirrel (Tamiasciurus hudsonicus fremonti) in a subalpine lodgepole pine forest. Anim Behav. 1984;32: 1119–1131. doi: 10.1016/S0003-3472(84)80228-6

28. Mery F, Burns JG. Behavioural plasticity: an interaction between evolution and experience. Evol Ecol. 2010;24: 571–583. doi: 10.1007/s10682-009-9336-y

29. Abudu S, Sheng Z ping, Cui C liang, Saydi M, Sabzi HZ, King JP. Integration of aspect and slope in snowmelt runoff modeling in a mountain watershed. Water Sci Eng. 2016;9: 265–273. doi: 10.1016/j.wse.2016.07.002

30. Hendricks P, Hendricks LM. Use of conifers by red squirrels (Tamiasciurus hudsonicus) in Montana for drying and caching mushrooms. Northwest Nat. 2015;96: 240–242.

31. Koprowski JL, Greer VL, Merrick MJ. Mt. Graham red squirrel monitoring program—2015 Annual report. Tucson, AZ, USA; 2015.

32. Pewsey A, Neuhäuser M, Ruxton GD. Circular statistics in R. Oxford University Press; 2013.

33. Jolliffe IT. Principal Component Analysis [Internet]. 2nd ed. New York: Springer-Verlag; 2002. doi: 10.1007/b98835

34. Burnham KP, Anderson DR. Model selection and multi-model inference: a practical information-theoretic approach. 2nd ed. Springer; 2010.

35. R Development Core Team. R: A language and environment for statiscal computing [Internet]. Vienna, Austria: R Foundation for Statistical Computing; 2016. Available:

36. Agostinelli C, Lund U. R package “circular”: circular statistics [Internet]. 2011. Available:

37. Bolker B R Development Core Team. bbmle: tools for general maximum likelihood estimation. R package version 1.0.20. 2017.

38. Le S, Josse J, Husson F. FactoMineR: an R package for multivariate analysis. J Stat Softw. 2008;25: 1–18. doi: 10.18637/jss.v025.i01

39. Akima H, Gebhardt A. akima: interpolation of irregularly and regularly spaced data. R package version 0.6–2. 2016.

40. Lemon J. Plotrix: a package in the red light district of R. R-News. 2016. p. R-News, 6(4): 8–12.

41. Paradis E, Schliep K. ape 5.0: an environment for modern phylogenetics and evolutionary analyses in R. Bioinformatics; 2018.

42. Smith AA, Mannan RW. Distinguishing characteristics of Mount Graham red squirrel midden sites. J Wildl Manage. 1994;58: 437–445.

43. Courbaud B, De Coligny F, Cordonnier T. Simulating radiation distribution in a heterogeneous Norway spruce forest on a slope. Agric For Meteorol. 2003;116: 1–18. doi: 10.1016/S0168-1923(02)00254-X

44. Elgar M. Predator vigilance and group size in mammals and birds: a critical review of the empirical evidence. Biol Rev. 1989;64: 13–33. doi: 10.1111/j.1469-185x.1989.tb00636.x 2655726

45. Verdolin JL. Meta-analysis of foraging and predation risk trade-offs in terrestrial systems. Behav Ecol Sociobiol. 2006;60: 457–464. doi: 10.1007/s00265-006-0172-6

46. Ecological Parmesan C. and evolutionary responses to recent climate change. Annu Rev Ecol Evol Syst. 2006;37: 637–669. doi: 10.1146/annurev.ecolsys.37.091305.110100

Článek vyšel v časopise


2019 Číslo 11