Free Standard AU & NZ Shipping For All Book Orders Over $80!
Register      Login
Wildlife Research Wildlife Research Society
Ecology, management and conservation in natural and modified habitats
RESEARCH ARTICLE

Effects of gap-based silviculture on thermal biology of a terrestrial reptile

Mickey Agha A D , Brian D. Todd A , Ben Augustine B , John M. Lhotka C , Leo J. Fleckenstein C , Mariah Lewis C , Clint Patterson C , Jeffrey W. Stringer C and Steven J. Price C
+ Author Affiliations
- Author Affiliations

A Department of Wildlife, Fish, and Conservation Biology, University of California, Davis, One Shields Avenue, Davis, CA 95616, USA.

B Department of Fish and Wildlife Conservation, Virginia Tech, Blacksburg, VA 24061, USA.

C Department of Forestry and Natural Resources, University of Kentucky, Lexington, KY 40546, USA.

D Corresponding author. Email: magha@ucdavis.edu

Wildlife Research 45(1) 72-81 https://doi.org/10.1071/WR17110
Submitted: 11 March 2017  Accepted: 12 December 2017   Published: 27 March 2018

Abstract

Context: Terrestrial reptiles require varied thermal environments to promote optimal physiological performance, growth, reproduction, and survival.

Aims: Our study was designed to determine whether gap-based silvicultural practices offer suitable thermal environments for eastern box turtles (Terrapene carolina) by examining environmental temperature variation and body temperature of eastern box turtles in, and adjacent to, canopy gaps.

Methods: We recorded box turtle body temperature from 20 radio-tracked turtles and environmental temperatures (canopy gaps and undisturbed habitat) using temperature loggers from June to September 2014 in a managed forest after canopy gaps (0.28–1.13 ha gap–1) were created via gap-based silviculture.

Key results: Over the four-month study period, gap temperatures were generally higher than adjacent undisturbed microhabitats. Box turtle body temperatures were closely correlated with environmental temperatures in undisturbed habitat in June and July. Turtle body temperatures were, however, closely correlated with environmental temperatures in canopy gaps in August and September. In addition, box turtles in our study had activity areas that overlapped canopy gaps from 0 to 65%, depending on the individual. As percentage overlap of canopy gaps increased, turtle body temperatures were increasingly correlated with canopy gap temperatures. Furthermore, as percentage overlap of canopy gaps increased, daily mean body temperature records consistently stayed within the preferred box turtle body temperature range (20.2–26.2°C).

Conclusions: Our study suggests that gap-based silviculture can create thermally compatible environments for box turtles depending on the time of day and year, and that box turtles use these microhabitats to thermoregulate.

Implications: The application of relatively small-scale silvicultural practices (≤1 ha gap–1) that provide heterogeneity in forest structure, composition, and function may be a useful alternative to clearcutting and other intensive harvesting methods that are associated with declines in terrestrial reptile populations.

Additional keywords: forest dynamics, habitat modification, habitat use, radio telemetry, thermoregulation.


References

Adams, N. A., Claussen, D. L., and Skillings, J. (1989). Effects of temperature on voluntary locomotion of the Eastern Box Turtle, Terrapene carolina carolina. Copeia 1989, 905–915.
Effects of temperature on voluntary locomotion of the Eastern Box Turtle, Terrapene carolina carolina.Crossref | GoogleScholarGoogle Scholar |

Angilletta, M. J., Huey, R. B., and Frazier, M. R. (2010). Thermodynamic effects on organismal performance: is hotter better? Physiological and Biochemical Zoology 83, 197–206.
Thermodynamic effects on organismal performance: is hotter better?Crossref | GoogleScholarGoogle Scholar |

Bartsch, N. (2000). Element release in beech (Fagus sylvatica L.) forest gaps. Water, Air, and Soil Pollution 122, 3–16.
Element release in beech (Fagus sylvatica L.) forest gaps.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXlvVChsLk%3D&md5=8a829bd49ba375cdf5a63faa08c60ea2CAS |

Bauhus, J., and Bartsch, N. (1995). Mechanisms for carbon and nutrient release and retention in beech forest gaps: I. Microclimate, water balance and seepage water chemistry. Plant and Soil 168–169, 579–584.
Mechanisms for carbon and nutrient release and retention in beech forest gaps: I. Microclimate, water balance and seepage water chemistry.Crossref | GoogleScholarGoogle Scholar |

Bernstein, N. P., and Black, R. W. (2005). Thermal environment of overwintering ornate box turtles, Terrapene ornata ornata, in Iowa. American Midland Naturalist 153, 370–377.
Thermal environment of overwintering ornate box turtles, Terrapene ornata ornata, in Iowa.Crossref | GoogleScholarGoogle Scholar |

Boucher, T. P. (1999). Population, growth and thermal ecology of the eastern box turtle, Terrapene carolina carolina (L.), in Fairfax County, Virginia. Ph.D. Dissertation, George Mason University, Fairfax, VA.

Burke, R. L., Calle, P. P., Figueras, M. P., and Green, T. M. (2016). Internal body temperatures of an overwintering adult Terrapene carolina (eastern box turtle). Northeastern Naturalist 23, 364–366.
Internal body temperatures of an overwintering adult Terrapene carolina (eastern box turtle).Crossref | GoogleScholarGoogle Scholar |

Burnham, K. P., and Anderson, D. R. (2002). ‘Model Selection and Multi-model Inference: a Practical Information-theoretic Approach.’ (Springer: New York.)

Cagle, F. R. (1939). A system of marking turtles for future identification. Copeia 1939, 170–173.
A system of marking turtles for future identification.Crossref | GoogleScholarGoogle Scholar |

Cantrell, A. W., Wang, Y., Schweitzer, C. J., and Greenberg, C. H. (2013). Short term response of herpetofauna to oak regeneration treatments on the mid-Cumberland Plateau of southern Tennessee. Forest Ecology and Management 295, 239–247.
Short term response of herpetofauna to oak regeneration treatments on the mid-Cumberland Plateau of southern Tennessee.Crossref | GoogleScholarGoogle Scholar |

Carlson, D. W., and Groot, A. (1997). Microclimate of clear-cut, forest interior, and small openings in trembling aspen forest. Agricultural and Forest Meteorology 87, 313–329.
Microclimate of clear-cut, forest interior, and small openings in trembling aspen forest.Crossref | GoogleScholarGoogle Scholar |

Chen, J., Saunders, S. C., Crow, T. R., Naiman, R. J., Brosofske, K. D., Mroz, G. D., Brookshire, B. L., and Franklin, J. F. (1999). Microclimate in forest ecosystem and landscape ecology variations in local climate can be used to monitor and compare the effects of different management regimes. Bioscience 49, 288–297.
Microclimate in forest ecosystem and landscape ecology variations in local climate can be used to monitor and compare the effects of different management regimes.Crossref | GoogleScholarGoogle Scholar |

Chen, T.-H., and Lue, K.-Y. (2008). Thermal preference of the yellow-margined box turtle (Cuora flavomarginata) (Testudines: Geoemydidae) inhabiting a mesic lowland, northern Taiwan. Amphibia-Reptilia 29, 513–522.
Thermal preference of the yellow-margined box turtle (Cuora flavomarginata) (Testudines: Geoemydidae) inhabiting a mesic lowland, northern Taiwan.Crossref | GoogleScholarGoogle Scholar |

Craig, J. M., Lhotka, J. M., and Stringer, J. W. (2014). Evaluating initial responses of natural and underplanted oak reproduction and a shade-tolerant competitor to midstory removal. Forest Science 60, 1164–1171.
Evaluating initial responses of natural and underplanted oak reproduction and a shade-tolerant competitor to midstory removal.Crossref | GoogleScholarGoogle Scholar |

Cunnington, G. M., Schaefer, J., Cebek, J. E., and Murray, D. (2008). Correlations of biotic and abiotic variables with ground surface temperature: an ectothermic perspective. Ecoscience 15, 472–477.
Correlations of biotic and abiotic variables with ground surface temperature: an ectothermic perspective.Crossref | GoogleScholarGoogle Scholar |

Currylow, A. F., MacGowan, B. J., and Williams, R. N. (2012). Short-term forest management effects on a long-lived ectotherm. PLoS One 7, e40473.
Short-term forest management effects on a long-lived ectotherm.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhtVemsr3P&md5=01a0111ac0502bb09f1e17b78db3e2dbCAS |

Currylow, A. F., Macgowan, B. J., and Williams, R. N. (2013). Hibernal thermal ecology of eastern box turtles within a managed forest landscape. Journal of Wildlife Management 77, 326–335.
Hibernal thermal ecology of eastern box turtles within a managed forest landscape.Crossref | GoogleScholarGoogle Scholar |

do Amaral, J. P. S., Marvin, G. A., and Hutchison, V. H. (2002). Thermoregulation in the box turtles Terrapene carolina and Terrapene ornata. Canadian Journal of Zoology 80, 934–943.
Thermoregulation in the box turtles Terrapene carolina and Terrapene ornata.Crossref | GoogleScholarGoogle Scholar |

Dodd, C. K. (2001). ‘North American Box Turtles: A Natural History.’ (University of Oklahoma Press: USA.)

Dodd, C. K., Rolland, V., and Oli, M. K. (2016). Consequences of individual removal on persistence of a protected population of long‐lived turtles. Animal Conservation 19, 369–379.
Consequences of individual removal on persistence of a protected population of long‐lived turtles.Crossref | GoogleScholarGoogle Scholar |

Dubois, Y., Blouin-Demers, G., Shipley, B., and Thomas, D. (2009). Thermoregulation and habitat selection in wood turtles Glyptemys insculpta: chasing the sun slowly. Journal of Animal Ecology 78, 1023–1032.
| 1:STN:280:DC%2BD1MrlsFWlsw%3D%3D&md5=139adafdda56a28add83a926cb18b499CAS |

Elliott, K. J., Hitchcock, S. L., and Krueger, L. (2002). Vegetation response to large scale disturbance in a southern Appalachian forest: Hurricane Opal and salvage logging. The Journal of the Torrey Botanical Society 129, 48–59.
Vegetation response to large scale disturbance in a southern Appalachian forest: Hurricane Opal and salvage logging.Crossref | GoogleScholarGoogle Scholar |

Ernst, C. H., and Lovich, J. E. (Eds) (2009). ‘Turtles of the United States and Canada.’ (The Johns Hopkins University Press: Baltimore, MD.)

ESRI (2014). ‘ArcGIS Desktop 10.1.1.’ (Environmental Systems Research Institute, Inc.: Redlands, CA.)

Faccio, S. D. (2003). Effects of ice storm-created gaps on forest breeding bird communities in central Vermont. Forest Ecology and Management 186, 133–145.
Effects of ice storm-created gaps on forest breeding bird communities in central Vermont.Crossref | GoogleScholarGoogle Scholar |

Faraway, J. J. (2005). ‘Extending the Linear Model with R: Generalized Linear, Mixed Effects and Nonparametric Regression Models.’ (CRC Press: Boca Raton, FL.)

Felix, Z., Wang, Y., Czech, H., and Schweitzer, C. J. (2008). Abundance of juvenile eastern box turtles relative to canopy cover in managed forest stands in Alabama. Chelonian Conservation and Biology 7, 128–130.
Abundance of juvenile eastern box turtles relative to canopy cover in managed forest stands in Alabama.Crossref | GoogleScholarGoogle Scholar |

Greenberg, C. H. (2001). Response of reptile and amphibian communities to canopy gaps created by wind disturbance in the southern Appalachians. Forest Ecology and Management 148, 135–144.
Response of reptile and amphibian communities to canopy gaps created by wind disturbance in the southern Appalachians.Crossref | GoogleScholarGoogle Scholar |

Greenberg, C. H., and Lanham, J. D. (2001). Breeding bird assemblages of hurricane-created gaps and adjacent closed canopy forest in the southern Appalachians. Forest Ecology and Management 154, 251–260.
Breeding bird assemblages of hurricane-created gaps and adjacent closed canopy forest in the southern Appalachians.Crossref | GoogleScholarGoogle Scholar |

Hashimoto, S., and Suzuki, M. (2004). The impact of forest clear-cutting on soil temperature: a comparison between before and after cutting, and between clear-cut and control sites. Journal of Forest Research 9, 125–132.
The impact of forest clear-cutting on soil temperature: a comparison between before and after cutting, and between clear-cut and control sites.Crossref | GoogleScholarGoogle Scholar |

Huey, R. B., and Stevenson, R. D. (1979). Integrating thermal physiology and ecology of ectotherms: a discussion of approaches. American Zoologist 19, 357–366.
Integrating thermal physiology and ecology of ectotherms: a discussion of approaches.Crossref | GoogleScholarGoogle Scholar |

Hutchison, V. H., Vinergar, A., and Kosh, R. J. (1966). Critical thermal maxima in turtles. Herpetologica 22, 32–41.

Kern, C. C., D’Amato, A. W., and Strong, T. F. (2013). Diversifying the composition and structure of managed, late-successional forests with harvest gaps: what is the optimal gap size? Forest Ecology and Management 304, 110–120.
Diversifying the composition and structure of managed, late-successional forests with harvest gaps: what is the optimal gap size?Crossref | GoogleScholarGoogle Scholar |

Kittredge, D. B., Finley, A. O., and Foster, D. R. (2003). Timber harvesting as ongoing disturbance in a landscape of diverse ownership. Forest Ecology and Management 180, 425–442.
Timber harvesting as ongoing disturbance in a landscape of diverse ownership.Crossref | GoogleScholarGoogle Scholar |

Lhotka, J. M. (2013). Effect of gap size on mid-rotation stand structure and species composition in a naturally regenerated mixed broadleaf forest. New Forests 44, 311–325.
Effect of gap size on mid-rotation stand structure and species composition in a naturally regenerated mixed broadleaf forest.Crossref | GoogleScholarGoogle Scholar |

Lindenmayer, D. B., Hunter, M. L., Burton, P. J., and Gibbons, P. (2009). Effects of logging on fire regimes in moist forests. Conservation Letters 2, 271–277.
Effects of logging on fire regimes in moist forests.Crossref | GoogleScholarGoogle Scholar |

Littell, R. C., Pendergast, J., and Natarajan, R. (2000). Tutorial in biostatistics: modeling covariance structure in the analysis of repeated measures data. Statistics in Medicine 19, 1793–1819.
Tutorial in biostatistics: modeling covariance structure in the analysis of repeated measures data.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD3M7islemtQ%3D%3D&md5=dcef7605cf7c05c16be4ff6342ddc12fCAS |

Martín-Queller, E., Diez, J. M., Ibanez, I., and Saura, S. (2013). Effects of silviculture on native tree species richness: interactions between management, landscape context and regional climate. Journal of Applied Ecology 50, 775–785.
Effects of silviculture on native tree species richness: interactions between management, landscape context and regional climate.Crossref | GoogleScholarGoogle Scholar |

Masek, J. G., Cohen, W. B., Leckie, D., Wulder, M. A., Vargas, R., de Jong, B., Healey, S., Law, B., Birdsey, R., Houghton, R. A., Mildrexler, D., Goward, S., and Smith, W. B. (2011). Recent rates of forest harvest and conversion in North America. Journal of Geophysical Research. Biogeosciences 116, G00K03.

Matlack, G. R. (1993). Microenvironment variation within and among forest edge sites in the eastern United States. Biological Conservation 66, 185–194.
Microenvironment variation within and among forest edge sites in the eastern United States.Crossref | GoogleScholarGoogle Scholar |

Messere, M., and Ducey, P. K. (1998). Forest floor distribution of northern redback salamanders, Plethodon cinereus, in relation to canopy gaps: first year following selective logging. Forest Ecology and Management 107, 319–324.
Forest floor distribution of northern redback salamanders, Plethodon cinereus, in relation to canopy gaps: first year following selective logging.Crossref | GoogleScholarGoogle Scholar |

Mitchell, R. J., Franklin, J. F., Palik, B. J., Kirkman, L. K., Smith, L. L., Engstrom, R. T., and Hunter Jr., M. L. (2005). Natural disturbance-based silviculture for restoration and maintenance of biological diversity. Final report to the National Commission on Science for Sustainable Forestry No. 120.

O’Bryan, C. (2014). Persistence of a vulnerable semi-aquatic turtle in an intensively-managed forest landscape. M.S. Thesis, Clemson University, Clemson, SC.

Patterson, C., and Karcher, S. (2013). Berea College forest management plan. Available at: http://www.berea.edu/forestry/files/2013/04/2013-forest-management-plan.pdf [accessed 6 March 2015].

Perison, D., Phelps, J., Pavel, C., and Kellison, R. (1997). The effects of timber harvest in a South Carolina blackwater bottomland. Forest Ecology and Management 90, 171–185.
The effects of timber harvest in a South Carolina blackwater bottomland.Crossref | GoogleScholarGoogle Scholar |

Peterson, C. R., Gibson, A. R., and Dorcas, M. E. (1993). Snake thermal ecology: the causes and consequences of body-temperature variation. In ‘Snakes: Ecology and Behavior’. (Eds R. A. Seigel, and J. T. Collins.) pp. 240–267. (McGraw Hill: New York.)

Pike, D. A., Webb, J. K., and Shine, R. (2011a). Removing forest canopy cover restores a reptile assemblage. Ecological Applications 21, 274–280.
Removing forest canopy cover restores a reptile assemblage.Crossref | GoogleScholarGoogle Scholar |

Pike, D. A., Webb, J. K., and Shine, R. (2011b). Chainsawing for conservation: ecologically informed tree removal for habitat management. Ecological Management & Restoration 12, 110–118.
Chainsawing for conservation: ecologically informed tree removal for habitat management.Crossref | GoogleScholarGoogle Scholar |

Pinheiro, J., Bates, D., DebRoy, S., and Sarkar, D. (2013). R Development Core Team (2012) nlme: linear and nonlinear mixed effects models. R package version 3.1–103. R Foundation for Statistical Computing, Vienna.

Raymond, P., Bédard, S., Roy, V., Larouche, C., and Tremblay, S. (2009). The irregular shelterwood system: review, classification, and potential application to forests affected by partial disturbances. Journal of Forestry 107, 405–413.

Renken, R. B., Gram, W. K., Fantz, D. K., Richter, S. C., Miller, T. J., Ricke, K. B., Russell, B., and Wang, X. (2004). Effects of forest management on amphibians and reptiles in Missouri Ozark forests. Conservation Biology 18, 174–188.
Effects of forest management on amphibians and reptiles in Missouri Ozark forests.Crossref | GoogleScholarGoogle Scholar |

Ritter, E., and Bjørnlund, L. (2005). Nitrogen availability and nematode populations in soil and litter after gap formation in a semi-natural beech-dominated forest. Applied Soil Ecology 28, 175–189.
Nitrogen availability and nematode populations in soil and litter after gap formation in a semi-natural beech-dominated forest.Crossref | GoogleScholarGoogle Scholar |

Roe, J. H., Wild, K. H., and Hall, C. A. (2017). Thermal biology of eastern box turtles in a longleaf pine system managed with prescribed fire. Journal of Thermal Biology 69, 325–333.
Thermal biology of eastern box turtles in a longleaf pine system managed with prescribed fire.Crossref | GoogleScholarGoogle Scholar |

Ross, C., Simcock, R., Williams, P., Toft, R., Flynn, S., Birchfield, R., and Comeskey, P. (2000). Salvage and direct transfer for accelerating restoration of native ecosystems on mine sites in New Zealand. In ‘New Zealand Miner & Mine Conference Proceedings’, pp. 29–31.

Sims, C. (2013). Influencing natural forest disturbance through timber harvesting: tradeoffs among disturbance processes, forest values, and timber condition. American Journal of Agricultural Economics 95, 992–1008.
Influencing natural forest disturbance through timber harvesting: tradeoffs among disturbance processes, forest values, and timber condition.Crossref | GoogleScholarGoogle Scholar |

Stringer, J. W. (2006). Oak shelterwood: a technique to improve oak regeneration. University of Kentucky Cooperative Extension Publication FOR-100, Lexington, KY: 8.

Sturbaum, B. A. (1981). Responses of the three-toed box turtle, Terrapene carolina triunguis, to heat stress. Comparative Biochemistry and Physiology. Part A, Physiology 70, 199–204.
Responses of the three-toed box turtle, Terrapene carolina triunguis, to heat stress.Crossref | GoogleScholarGoogle Scholar |

Todd, B. D., and Andrews, K. M. (2008). Response of a reptile guild to forest harvesting. Conservation Biology 22, 753–761.
Response of a reptile guild to forest harvesting.Crossref | GoogleScholarGoogle Scholar |

Todd, B. D., Willson, J. D., and Gibbons, J. W. (2010). The global status of reptiles and causes of their decline. In ‘Ecotoxicology of Amphibians and Reptiles’. 2nd edn. (Eds D. W. Sparling, G. Linder, C. A. Bishop, and S. Krest.) pp. 47–67. (CRC Press: Pensacola, FL.)

Todd, B. D., Blomquist, S. M., Harper, E. B., and Osbourn, M. S. (2014). Effects of timber harvesting on terrestrial survival of pond-breeding amphibians. Forest Ecology and Management 313, 123–131.
Effects of timber harvesting on terrestrial survival of pond-breeding amphibians.Crossref | GoogleScholarGoogle Scholar |

Vitt, L. J., Avila‐Pires, T., Caldwell, J. P., and Oliveira, V. R. (1998). The impact of individual tree harvesting on thermal environments of lizards in Amazonian rain forest. Conservation Biology 12, 654–664.
The impact of individual tree harvesting on thermal environments of lizards in Amazonian rain forest.Crossref | GoogleScholarGoogle Scholar |

Walker, R. C. (2012). A critical evaluation of field survey methods for establishing the range of a small, cryptic tortoise (Pyxis arachnoides). The Herpetological Journal 22, 7–12.

Webster, C. R., and Lorimer, C. G. (2005). Minimum opening sizes for canopy recruitment of midtolerant tree species: a retrospective approach. Ecological Applications 15, 1245–1262.
Minimum opening sizes for canopy recruitment of midtolerant tree species: a retrospective approach.Crossref | GoogleScholarGoogle Scholar |