In spite of the fully-hinged shell being the defining characteristic of box turtles, few studies have quantified the behavioural use of the shell in response to predator encounters. While it is often assumed that box turtles simply withdraw into their shell in response to threats, we expected variability among individuals in shell usage and in the degree of head and limb retraction because withdrawal is likely to be costly. We tested the behavioural and physiological responses of free-ranging eastern box turtles to stimuli of varying intensity: observation only, a visual stimulus, a poke on the leg, or a pinch on the leg before being flipped. The more intense the simulated predatory stimulus, the more likely turtles were to fully close their shell. However, stimulus intensity did not affect plasma corticosterone or lactate levels. This may be due to too brief or weak of a stimulus, increased parasympathetic activity, or seasonal effects. Upon capture and during handling, almost all turtles withdrew into their shells and closed their anterior plastron, although fewer closed their posterior plastron, and a few engaged in other behaviours such as biting and urinating. Older, larger turtles were able to close their shells with greater strength than younger and smaller turtles. Our results indicate that in spite of their fully closable shell, box turtles exhibit a graded response to perceived threats. This suggests that full closure of the shell is likely to be costly and occurs only in response to the most intense stimuli.
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
Ashton, D.T., Bettaso, J.B., Welsh Jr., H.H. (2015): Changes across a decade in size, growth, and body condition of western pond turtle (Actinemys marmorata) populations on free-flowing and regulated forks of the Trinity River in northwest California. Copeia 2015: 621-633.
Bennett, A.F., Licht, P. (1972): Anaerobic metabolism during activity in lizards. J. Comp. Physiol. 81: 277-288.
Boonstra, R., Hik, D., Singleton, G.R., Tinnikov, A. (1998): The impact of predator-induced stress on the snowshoe hare cycle. Ecol. Monogr. 79: 371-394.
Bowen, M.T., McGregor, I.S. (2014): Oxytocin and vasopressin modulate the social response to threat: a preclinical study. Int. J. Neuropsychopharmacol. 17: 1621-1633.
Bramble, D.M. (1974): Emydid shell kinesis: biomechanics and evolution. Copeia 1974: 707-727.
Bramble, D.M., Hutchison, J.H. (1981): A reevaluation of plastral kinesis in African turtles of the genus Pelusios. Herpetologica 37: 205-212.
Bryan, L.K., Baldwin, C.A., Gray, M.J., Miller, D.L. (2009): Efficacy of select disinfectants at inactivating Ranavirus. Dis. Aquat. Org. 84: 89-94.
Carter, A.J., Feeney, W.E., Marshall, H.M., Cowlishaw, G., Heinsohn, R. (2013): Animal personality: what are behavioural ecologists measuring? Biol. Rev. 88: 465-475.
Cash, W.B., Holberton, R.L., Knight, S.S. (1997): Corticosterone secretion in response to capture and handling in free-living red-eared slider turtles. Gen. Comp. Endocrinol. 108: 427-433.
Cooper Jr., W.E. (2015): Reptiles. In: Escaping From Predators: an Integrative View of Escape Decisions, p. 113-151. Cooper, W.E., Blumstein, D.T., Eds, Cambridge Univ. Press, Cambridge, UK.
Cordero, G.A., Stearns, S., Quinteros, K., Berns, C.M., Binz, S.M., Janzen, F. (2019): The postembryonic transformation of the shell in emydine box turtles. Evol. Devel. 2019: e12307. DOI:10.1111/ede.12307.
Davis, D.R., Gabor, C.R. (2015): Behavioral and physiological antipredator responses of the San Marcos salamander, Eurycea nana. Physiol. Behav. 139: 145-149.
DeGregorio, B.A., Tuberville, T.D., Kennamer, R.A., Harris, B.B., Brisbin Jr., I.L. (2017): Spring emergence of eastern box turtles (Terrapene carolina): influences of individual variation and scale of temperature correlates. Can. J. Zool. 95: 23-30.
Dodd Jr., C.K. (2001): North American Box Turtles: a Natural History. University of Oklahoma Press, Norman.
Elghammer, R.W., Swan, R.O., Johnson, R.E., Murphy, D. (1979): Physical characteristics of male and female Eastern Box Turtles (Terrapene carolina carolina) found in Illinois. Trans. Ill. State Acad. Sci. 72: 1-8.
Ewing, H.E. (1939): Growth in the Eastern Box Turtle, with special reference to the dermal shields of the carapace. Copeia 1939: 87-92.
Fonner, C.W., Woodley, S.K. (2015): Testing the predation stress hypothesis: behavioural and hormonal responses to predator cues in Allegheny Mountain dusky salamanders. Behaviour 152: 797-819.
Freeman, A.R., Hare, J.F., Anderson, W.G., Caldwell, H.K. (2018): Effects of arginine vasopressin on Richardson’s ground squirrel social and vocal behavior. Behav. Neurosci. 132: 34-50.
Gatten Jr., R.E. (1974): Effects of temperature and activity on aerobic and anaerobic metabolism and heart rate in the turtles Pseudemys scripta and Terrapene ornata. Comp. Biochem. Physiol. 48A: 619-648.
Gatten Jr., R.E. (1975): Effects of activity on blood oxygen saturation, lactate, and pH in the turtles Pseudemys scripta and Terrapene ornata. Physiol. Zool. 48: 24-35.
Germano, D.J., Bury, R.B. (1998): Age determination in turtles: evidence of annual deposition of scute rings. Chelonian Conserv. Biol. 3: 123-132.
Gilbert, S.F., Loredo, G.A., Brukman, A., Burke, A.C. (2001): Morphogenesis of the turtle shell: the development of a novel structure in tetrapod evolution. Evol. Devel. 3: 47-58.
Hawkins, S., Worthy, T.H., Bedford, S., Spriggs, M., Clark, G., Irwin, G., Best, S., Kirch, P. (2016): Ancient tortoise hunting in the southwest Pacific. Nature, Sci. Rep. 6: 38317. DOI:10.1038/srep38317.
Heatley, J.J., Russell, K.E. (2010): Box turtle (Terrapene spp.) hematology. J. Exotic Pet Med. 19: 160-164.
Herrel, A., O’Reilly, J.C. (2005): Ontogenetic scaling of biting force in lizards and turtles. Physiol. Biomech. Zool. 79: 31-42.
Hunt, K.E., Innis, C.J., Kennedy, A.E., McNally, K.L., Davis, D.G., Burgess, E.A., Merigo, C. (2015): Assessment of ground transportation stress in juvenile Kemp’s ridley sea turtles (Lepidochelys kempii). Conserv. Physiol. 4: 1-13.
Johnson, S.M., Creighton, R.J. (2005): Spinal cord injury-induced changes in breathing are not due to supraspinal plasticity in turtles (Pseudamys scripta). Amer. J. Physiol. 289: 1550-1559.
Kahn, P.F., Guyer, C., Mendonca, M.T. (2007): Handling, blood sampling, and temporary captivity do not affect plasma corticosterone or movement patterns of Gopher tortoises (Gopherus polyphemus). Copeia 2007: 614-621.
Kardong, K.V. (2015): Vertebrates Comparative Anatomy, Function, Evolution, 7th Edition. McGraw-Hill Education, New York.
Kashon, E.A.F., Carlson, B.E. (2018): Consistently bolder turtles maintain higher body temperatures in the field but may experience greater predation risk. Behav. Ecol. Sociobiol. 72: 9.
Kiester, A.R., Olson, D.H. (2011): Prime time for turtle conservation. Herpetol. Rev. 42: 198-204.
Klukowski, M. (2011): Effects of breeding season, testosterone, and ACTH on the corticosterone response of free-ranging male fence lizards (Sceloporus undulatus). Gen. Comp. Endocrinol. 173: 295-302.
Landberg, T., Mailhot, J.D., Brainerd, E.L. (2003): Lung ventilation during treadmill locomotion in a terrestrial turtle, Terrapene carolina. J. Exp. Biol. 206: 3391-3404.
Lima, S.L. (1998): Stress and decision making under the risk of predation: recent developments from behavioral, reproductive, and ecological perspectives. Adv. Study Behav. 27: 215-290.
Mateo, J.M. (2007): Ecological and hormonal correlates of antipredator behavior in adult Belding’s ground squirrels (Spermophilus beldingi). Behav. Ecol. Sociobiol. 62: 37-49.
Pich, J.M., Belden, A.J., Carlson, B.E. (2019): Individual variation in boldness in turtles is consistent across assay conditions and behavioural measures. Behaviour 156: 1039-1056.
Pritchard, P.C.H. (2008): Evolution and structure of the turtle shell. In: Biology of Turtles, p. 45-83. Wyneken, J., Godfrey, M.H., Bels, V., Eds, CRC Press, Boca Raton.
Randall, D., Burggren, W., French, K. (2001): Eckert Animal Physiology: Mechanisms and Adaptations, 5th Edition. W.H. Freeman and Company, New York.
Schramm, B.G., Casares, M., Lance, V.A. (1999): Steroid levels and reproductive cycle of the Galápagos tortoise, Geochelone nigra, living under seminatural conditions on Santa Cruz Island (Galápagos). Gen. Comp. Endocrinol. 114: 108-120.
Smith, E.N., De Carvalho Jr., M.C. (1985): Heart rate response to threat and diving in the ornate box turtle, Terrapene ornata. Physiol. Zool. 58: 236-241.
Thaker, M., Lima, S.L., Hews, D.K. (2009): Acute corticosterone elevation enhances antipredator behaviors in male tree lizard morphs. Horm. Behav. 56: 51-57.
Vannatta, J.M., Klukowski, M., Wright, S. (2016): Prevalence of ranavirus infection in the Eastern Box Turtle, Terrapene carolina carolina, in an isolated, suburban wetland habitat of middle Tennessee. Herpetol. Rev. 47: 55-56.
Vera, F., Zenuto, R., Antenucci, C.D. (2017): Expanding the actions of cortisol and corticosterone in wild vertebrates: a necessary step to overcome the emerging challenges. Gen. Comp. Endocrinol. 246: 337-353.
West, J.M., Klukowski, M. (2016): Demographic characteristics of the Eastern Box Turtle, Terrapene carolina carolina, in a relictual, suburban, wetland habitat of middle Tennessee, USA. Herpetol. Conserv. Biol. 11: 459-466.
West, J.M., Klukowski, M. (2018): Seasonal changes in baseline corticosterone, association with innate immunity, and effects of confinement in free-ranging Eastern Box Turtles, Terrapene carolina carolina. Gen. Comp. Endocrinol. 262: 71-80.
Winterhalder, B. (1983): Opportunity-cost foraging models for stationary and mobile predators. Am. Nat. 122: 73-84.
| All Time | Past 365 days | Past 30 Days | |
|---|---|---|---|
| Abstract Views | 1065 | 335 | 34 |
| Full Text Views | 314 | 12 | 1 |
| PDF Views & Downloads | 316 | 23 | 0 |
In spite of the fully-hinged shell being the defining characteristic of box turtles, few studies have quantified the behavioural use of the shell in response to predator encounters. While it is often assumed that box turtles simply withdraw into their shell in response to threats, we expected variability among individuals in shell usage and in the degree of head and limb retraction because withdrawal is likely to be costly. We tested the behavioural and physiological responses of free-ranging eastern box turtles to stimuli of varying intensity: observation only, a visual stimulus, a poke on the leg, or a pinch on the leg before being flipped. The more intense the simulated predatory stimulus, the more likely turtles were to fully close their shell. However, stimulus intensity did not affect plasma corticosterone or lactate levels. This may be due to too brief or weak of a stimulus, increased parasympathetic activity, or seasonal effects. Upon capture and during handling, almost all turtles withdrew into their shells and closed their anterior plastron, although fewer closed their posterior plastron, and a few engaged in other behaviours such as biting and urinating. Older, larger turtles were able to close their shells with greater strength than younger and smaller turtles. Our results indicate that in spite of their fully closable shell, box turtles exhibit a graded response to perceived threats. This suggests that full closure of the shell is likely to be costly and occurs only in response to the most intense stimuli.
| All Time | Past 365 days | Past 30 Days | |
|---|---|---|---|
| Abstract Views | 1065 | 335 | 34 |
| Full Text Views | 314 | 12 | 1 |
| PDF Views & Downloads | 316 | 23 | 0 |