Abstract
This study of California ground squirrels (Otospermophilus beecheyi) investigated the long-term effects of isolation rearing on alarm-call recognition. Six wild-caught squirrels, trapped as yearlings, and six laboratory-reared squirrels were maintained in solitary cages for approximately 3 years prior to the study. Visual searching and olfactory searching were measured as squirrels emerged from their burrow-like nest box into a laboratory room after hearing repetitive playbacks of alarm calls or control sounds consisting of pulses of white-noise or ambient laboratory sounds. Before exiting completely after hearing alarm calls, both groups exhibited similar levels of visual searching that was reliably higher than after hearing the other sounds. After exiting completely, the laboratory-reared squirrels exhibited a reliably greater amount of olfactory investigation than the wild-caught squirrels. Five laboratory-reared squirrels turned around after exiting and inspected their dark nest-box opening, three of which tail flagged repeatedly and one threw substrate into the opening. Since pups recognize snakes and engage in this behavior, this latent expression of antisnake behavior illustrates its robust organizational properties in the appropriate burrow-like context irrespective of the presumed retardation of neural development known to occur in other species of rodent subjected to similar isolation rearing.
Similar content being viewed by others
References
Andersen SL (2003) Trajectories of brain development: point of vulnerability or window of opportunity? Neurosci Biobehav Rev 27:3–18
Arenz CL, Leger DW (1997) The antipredator vigilance of adult and juvenile thirteen-lined ground squirrels (Sciuridae: Spermophilus tridecemlineatus): visual obstruction and simulated hawk attacks. Ethology 103:945–953
Barbour MA, Clark RW (2012) Ground squirrel tail-flag displays alter both predatory strike and ambush site selection behaviours of rattlesnakes. Proc R Soc B 279:3827–3833
Black JE, Greenough WT (1986) Induction of pattern in neural structure by experience: implications for cognitive development. In: Lamb ME, Brown AL, Rogoff B (eds) Advances in developmental psychology, vol 4., ErlbaumHillsdale, New Jersey, pp 1–50
Black JW, Greenough WT (1998) Developmental approaches to the memory process. In: Martinez JL Jr, Kesner RP (eds) Neurobiology of learning and memory. Academic Press, San Diego, pp 55–88
Boinski S, Kauffman L, Westoll A, Stickler CM, Cropp S, Ehm E (2003) Are vigilance, risk from avian predators and group size consequences of habitat structure? A comparison of three species of squirrel monkey (Saimiri oerstedii, S. boliviensis, and S. sciureus). Behaviour 140:1421–1467
Bryan GK, Riesen AH (1989) Deprived somatosensory-motor experience in stumptailed monkey neocortex: dendritic spine density and dendritic branching of layer IIIB pyramidal cells. J Comp Neurol 286:208–217
Burns-Cusato M, Cusato B, Glueck AC (2013) Barbados green monkeys (Chlorocebus sabaeus) recognized ancestral alarm calls after 350 years of isolation. Behav Process 100:197–199
Champagne FA, Curley JP (2005) How social experiences influence the brain. Curr Opin Neurobiol 15:704–709
Cohen J (1992) Statistical power analysis. Curr Direct Psych Sci 1:98–101
Coss RG (1979) Delayed plasticity of an instinct: recognition and avoidance of 2 facing eyes by the jewel fish. Develop Psychobiol 12:335–345
Coss RG (1991a) Context and animal behavior: III. The relationship between early development and evolutionary persistence of ground squirrel antisnake behavior. Ecol Psych 3:277–315
Coss RG (1991b) Evolutionary persistence of memory-like processes. Concepts Neurosci 2:129–168
Coss RG (1993) Evolutionary persistence of ground squirrel antisnake behavior: reflections on Burton’s commentary. Ecol Psych 2:171–194
Coss RG, Biardi JE (1997) Individual variation in the antisnake defenses of California ground squirrels (Spermophilus beecheyi). J Mammal 78:294–310
Coss RG, Globus A (1979) Social experience affects the development of dendritic spines and branches on tectal interneurons in the jewel fish. Develop Psychobiol 12:347–358
Coss RG, Goldthwaite RO (1995) The persistence of old designs for perception. In: Thompson NS (ed) Perspectives in ethology, vol 11. Plenum Press, New York, pp 83–148
Coss RG, Owings DH (1985) Restraints on ground squirrel antipredator behavior: adjustments over multiple time scales. In: Johnston TD, Pietrewicz AT (eds) Issues in the ecological study of learning. Erlbaum, Hillsdale, pp 167–200
Coss RG, Owings DH (1989) Rattler battlers. Nat Hist 5:30–35
Coss RG, McCowan B, Ramakrishnan U (2007) Threat-related acoustical differences in alarm calls by wild bonnet macaques (Macaca radiata) elicited by python and leopard models. Ethology 113:352–367
Davies NB, Madden JR, Butchart SHM (2004) Learning fine-tunes a specific response of nestlings to the parental alarm calls of their own species. Proc R Soc Lond B 271:2297–2304
Dukes WF (1965) N = 1. Psychol Bull 64:74–79
Fitch HS (1948) Ecology of the California ground squirrel on grazing lands. Amer Midl Nat 39:513–596
Fitch HS (1949) Study of snake populations in central California. Amer Midl Nat 41:513–579
Fitch HS, Swenson F, Tillotson DF (1946) Behavior and food habits of the red-tailed hawk. Condor 48:205–237
Gould JL, Marler P (1987) Learning by instinct. Sci Am 256:74–85
Green EJ, Greenough WT, Schlumpf BE (1983) Effects of complex or isolated environments on cortical dendrites of middle-aged rats. Brain Res 264:233–240
Greenough WT, Volkmar FR (1973) Pattern of dendritic branching in occipital cortex of rats reared in complex environments. Exper Neurol 40:491–504
Griffin AS (2004) Social learning about predators: a review and prospectus. Learn Behav 32:131–140
Hanson MT, Coss RG (1997) Age differences in the response of California ground squirrels (Spermophilus beecheyi) to avian and mammalian predators. J Comp Psychol 111:174–184
Hanson MT, Coss RG (2001a) Age differences in arousal and vigilance in California ground squirrels (Spermophilus beecheyi). Develop Psychobiol 39:199–206
Hanson MT, Coss RG (2001b) Age differences in the response of California ground squirrels (Spermophilus beecheyi) to conspecific alarm calls. Ethology 107:259–275
Helmeke C, Poeggel G, Braun K (2001) Differential emotional experience induces elevated spine densities on basal dendrites of pyramidal neurons in the anterior cingulate cortex of Octodon degus. Neuroscience 104:927–931
Hennessy DF, Owings DH, Rowe MP, Coss RG, Leger DW (1981) The information afforded by a variable signal: constraints on snake-elicited tail flagging by California ground squirrels. Behaviour 78:188–226
Hersek MJ, Owings DH (1993) Tail flagging by adult California ground squirrels: a tonic signal that serves different functions for males and females. Anim Behav 46:129–138
Heth G, Frankenberg E, Nevo E (1986) Adaptive optimal sound for vocal communication in tunnels of a subterranean mammal (Spalax ehrenbergi). Experientia 42:1287–1289
Heyes CM (1994) Social learning in animals: categories and mechanisms. Biol Rev 69:207–231
Ikemoto S, Panksepp J (1992) The effects of early social isolation on the motivation for social play in juvenile rats. Develop Psychobiol 25:261–274
Lea AJ, Barrera JP, Tom LM, Blumstein DT (2008) Heterospecific eavesdropping in a nonsocial species. Behav Ecol 19:1041–1046
Leger DW, Owings DH (1978) Responses to alarm calls by California ground squirrels: effects of call structure and maternal status. Behav Ecol Sociobiol 3:177–186
Leger DW, Owings DH, Boal LM (1979) Contextual information and differential responses to alarm whistles in California ground squirrels. Z Tierpsychol 49:142–155
Loughry WJ, McDonough CM (1989) Calling and vigilance in California ground squirrels: age, sex, and seasonal differences in responses to vocalizations. Am Midl Nat 121:312–321
Mateo JM (1996a) Development of alarm response behavior in free-living Belding’s ground squirrels. Anim Behav 52:89–105
Mateo JM (1996b) Early auditory experience and the ontogeny of alarm call discrimination in Belding’s ground squirrels (Spermophilus beldingi). J Comp Psychol 110:115–124
McAdam AG, Kramer DL (1998) Vigilance as a benefit of intermittent locomotion in small mammals. Anim Behav 55:109–117
Morton ES (1977) On the occurrence and significance of motivation-structural rules in some bird and mammal sounds. Amer Nat 111:855–869
Owings DH, Coss RG (2008) Hunting California ground squirrels: constraints and opportunities for northern Pacific rattlesnakes. In: Hayes WK, Beaman KR, Cardwell MD, Bush SP (eds) The biology of rattlesnakes. Loma Linda University Press, Loma, pp 155–167
Owings DH, Hennessy DF (1984) The importance of variation in sciurid visual and vocal communication. In: Murie JA, Michener GR (eds) The biology of ground-dwelling squirrels: annual cycles, behavioral ecology, and sociality. University of Nebraska Press, Lincoln, pp 169–200
Owings DH, Leger DW (1980) Chatter vocalizations of California ground squirrels: predator- and social-role specificity. Z Tierpsychol 54:163–184
Owings DH, Virginia RA (1978) Alarm calls of California ground squirrels (Spermophilus beecheyi). Z Tierpsychol 46:58–70
Owings DH, Hennessy DF, Leger DW, Gladney AB (1986) Different functions of alarm calling for different time scales: a preliminary report on ground squirrels. Behaviour 99:101–116
Owren MJ, Rendall DD (1997) An affect conditioning model of non-human primate vocal signaling. In: Beecher MD, Owings DH (eds) Perspectives in ethology, vol 12. Plenum Press, New York, pp 299–346
Palleroni A, Hauser M, Marler P (2005) Do responses of galliform birds vary adaptively with predator size? Anim Cog 8:200–210
Poran NS, Coss RG (1990) Development of antisnake defenses in California ground squirrels (Spermophilus beecheyi): I. Behavioral and immunological correlates. Behaviour 112:222–245
Quenette P-Y (1990) Functions of vigilance behaviour in mammals: a review. Acta Oecolog 11:801–818
Rendall D, Owren MJ (2013) Communication without meaning or information: abandoning language-based and informational constructs in animal communication theory. In: Stegmann UE (ed) animal communication theory. Cambridge University Press, New York, pp 151–182
Seyfarth RM, Cheney DL (1980) The ontogeny of vervet monkey alarm calling behavior: a preliminary report. Z Tierpsychol 54:37–45
Seyfarth RM, Cheney DL, Marler P (1980) Monkey responses to three different alarm calls: evidence for predator classification and semantic communication. Science 210:801–803
Stegmann UE (2013) Introduction: a primer on information and influence in animal communication. In: Stegmann UE (ed) Animal communication theory. Cambridge University Press, New York, pp 1–39
Strusaker TP (1967) Auditory communication among vervet monkeys (Cercopithecus aethiops). In: Altmann SA (ed) Social communication among primates. University of Chicago Press, Chicago, pp 281–384
Treves A (2000) Theory and method in studies of vigilance and aggregation. Anim Behav 60:711–722
Tromborg CT (1998) Figure and ground squirrels. Ph.D. Dissertation, University of California, Davis. AAT 9925761
Tromborg CT, Coss RG (1995) Denizens, decibels, and dens. Ann Proc Am Assoc Zoos Aquariums, Seattle, pp 521–528
Winer BJ (1962) Statistical principles in experimental design. McGraw-Hill Book Co., New York, p 208
Woodward JA, Bonett DG, Brecht M-L (1990) Introduction to linear models and experimental design. Harcourt, Brace, Jovanovich, San Diego, p 173
Acknowledgments
The authors wish to thank Dr. Mark Hanson for recording ground squirrel alarm calls in the field and Nancy Bacon for her behavioral observations during animal care. Professor Donald H. Owings provided important insight in the development of this study for which we are grateful. This research was supported by University of California Research Grant 1016 to CT and Faculty Research Grant 3079 to RGC.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Tromborg, C.T., Coss, R.G. Isolation rearing reveals latent antisnake behavior in California ground squirrels (Otospermophilus becheeyi) searching for predatory threats. Anim Cogn 18, 855–865 (2015). https://doi.org/10.1007/s10071-015-0853-5
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10071-015-0853-5