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Shrinking skinks: lizard body size declines in a long-term forest fragmentation experiment

Abstract

Context

Increasing rates of habitat fragmentation globally underscore the importance of understanding the full spectrum of fragmentation’s ecological consequences. Fragmentation alters the thermal environment of fragments, which may alter the body size of ectothermic organisms and in turn impact survival and reproduction.

Objectives

To determine whether experimental habitat fragmentation alters body size in the heliothermic, ground-dwelling common garden skink (Lampropholis guichenoti).

Methods

We use body size data spanning 29 years to experimentally test the prediction that lizards will experience morphological changes in forest fragments but not in non-fragmented controls.

Results

Lizards were smaller in forest fragments relative to those in the non-fragmented controls after the fragmentation treatment was applied. For lizards within forest fragments, the greater the exposure to deforested areas, the greater the decline in body size. This pattern was strongest in the first 5 years following fragmentation and weakened or reversed over time as the pine plantation matrix surrounding the fragments matured. Using sampling site-scale temperature data for the most recent 5 years of the experiment, we show that temperature predicts lizard body size. Our findings are consistent with predictions made under the temperature-size rule that ectotherms will be smaller in fragmented landscapes because of temperature increases at newly created edges.

Conclusions

Our results raise new concerns about the effects of fragmentation on organisms in remnant patches and offer new research priorities, as more evidence is needed to determine the generality of body size declines in fragmented landscapes. Our results also highlight that body size declines, often attributed to climate change, may be amplified by habitat fragmentation, which has been global in its impact.

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References

  1. Anderson L, Burgin S (2002) Influence of woodland remnant edges on small skinks (Richmond, New South Wales). Austral Ecol 27:630–637

  2. Anderson L, Burgin S (2008) Patterns of bird predation on reptiles in small woodland remnant edges in peri-urban north-western Sydney, Australia. Landscape Ecol 23:1039–1047

  3. Angilletta MJ, Steury TD, Sears MW (2004) Temperature, growth rate, and body size in ectotherms: fitting pieces of a life-history puzzle. Integr Comp Biol 44:498–509

  4. Atkinson D (1994) Temperature and organism size—a biological law for ectotherms? Adv Ecol Res 25:1–58

  5. Austin MP, Nicholls AO (1988) Species associations within herbaceous vegetation in an Australian eucalypt forest. In: During HJ, Werger MJA, Willems JH (eds) Diversity and pattern in plant communities. SPB Academic Publishing, The Hague, pp 95–114

  6. Bates D, Maechler M, Bolker B, Walker S (2014) lme4: linear mixed-effects models using Eigen and S4. R package version 1.1-7. http://CRAN.R-project.org/package=lme4

  7. Brown JH, Marquet PA, Taper ML (1993) Evolution of body size: consequences of an energetic definition of fitness. Am Nat 142:573–584

  8. Bucher R, Entling MH (2011) Contrasting effects of habitat fragmentation, population density, and prey availability on body condition of two orb-weaving spiders. Ecol Entomol 36:680–685

  9. Caruso NM, Sears MW, Adams DC, Lips KR (2014) Widespread rapid reductions in body size of adult salamanders in response to climate change. Glob Change Biol 20:1751–1759

  10. Chen J, Saunders SC, Crow TR, Naiman RJ, Brosofske KD, Mroz GD et al (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

  11. Cogger HG (2000) Reptiles and amphibians of Australia, 6th edn. Ralph Curtis Publishing, Sanibel Island, p 808

  12. Crome B (1981) The diet of some ground-layer lizards in three woodlands of the New England Tableland of Australia. Herpetofauna 13:4–11

  13. Davies KF, Margules CR (1998) Effects of habitat fragmentation on carabid beetles: experimental evidence. J Anim Ecol 67:460–471

  14. Davies KF, Margules CR, Lawrence JF (2000) Which traits of species predict population declines in experimental forest fragments? Ecology 81:1450–1461

  15. Delgado-Acevedo J, Restrepo C (2008) The contribution of habitat loss to changes in body size, allometry, and bilateral asymmetry in two Eleutherodactylus frogs from Puerto Rico. Conserv Biol 22:773–782

  16. Downes S, Shine R (2001) Why does tail loss increase a lizard’s later vulnerability to snake predators? Ecology 82:1293–1303

  17. Ewers RM, Banks-Leite C (2013) Fragmentation impairs the microclimate buffering effect of tropical forests. PLoS ONE 8:e58093

  18. Ewers RM, Didham RK (2005) Confounding factors in the detection of species responses to habitat fragmentation. Biol Rev Camb Philos Soc 81:117–142

  19. Fahrig L (2013) Rethinking patch size and isolation effects: the habitat amount hypothesis. J Biogeogr 40:1649–1663

  20. Fietz J, Weis-Dootz T (2012) Stranded on an island: consequences of forest fragmentation for body size variations in an arboreal mammal, the edible dormouse (Glis glis). Popul Ecol 54:313–320

  21. Forsman A, Merilä J, Ebenhard T (2011) Phenotypic evolution of dispersal-enhancing traits in insular voles. Proc R Soc B 278:225–232

  22. Forster J, Hirst AG, Woodward G (2011) Growth and development rates have different thermal responses. Am Nat 178:668–678

  23. Forster J, Hirst AG, Atkinson D (2012) Warming-induced reductions in body size are greater in aquatic than terrestrial species. PNAS 109:19310–19314

  24. Gardner JL, Peters A, Kearney MR, Joseph L, Heinsohn R (2011) Declining body size: a third universal response to warming? Trends Ecol Evol 26:285–291

  25. Haddad NM, Brudvig LA, Clobert J, Davies KF, Gonzalez A, Holt RD, Lovejoy TE, Sexton JO, Austin MP, Collins CD, Cook WM (2015) Habitat fragmentation and its lasting impact on Earth’s ecosystems. Sci Adv 1(2):e1500052

  26. Heidinger IMM, Hein S, Bonte D (2010) Patch connectivity and sand dynamics affect dispersal-related morphology of the blue-winged grasshopper Oedipoda caerulescens in coastal grey dunes. Insect Conserv Divers 3:205–212

  27. Henríquez P, Donoso DS, Grez AA (2009) Population density, sex ratio, body size and fluctuating asymmetry of Ceroglossus chilensis (Carabidae) in the fragmented Maulino forest and surrounding pine plantations. Acta Oecol 35:811–818

  28. Hill JK, Gray MA, Khen CV, Benedick S, Tawatao N, Hamer KC (2011) Ecological impacts of tropical forest fragmentation: how consistent are patterns in species richness and nestedness? Philos Trans R Soc B 366:3265–3276

  29. Hutchinson MN (1993) Fauna of Australia 2A, 31: Scincidae. AGPS, Canberra

  30. Kingsolver JG, Huey RB (2008) Size, temperature, and fitness: three rules. Evol Ecol Res 10:251–268

  31. Lomolino MV, Perault DR (2007) Body size variation of mammals in a fragmented, temperate rainforest. Conserv Biol 21:1059–1069

  32. Lunney D, Ashby E, Grigg J, O’Connell M (1989) Diets of scincid lizards Lampropholis guichenoti (Dumeril & Bibron) and L. delicata (De Vis) in Mumbulla State forest on the south coast of New South Wales. Aust Wildl Res 16:307–312

  33. Mantle BL, La Salle J, Fisher N (2012) Whole-drawer imaging for digital management and curation of a large entomological collection. ZooKeys 209:147–163

  34. Margules C (1992) The Wog Wog habitat fragmentation experiment. Environ Conserv 19:316–325

  35. Mathis A (1990) Territoriality in a terrestrial salamander: the influence of resource quality and body size. Behaviour 112:162–175

  36. Murcia C (1995) Edge effects in fragmented forests: implications for conservation. Trends Ecol Evol 10:58–62

  37. Norberg U, Leimar O (2002) Spatial and temporal variation in flight morphology in the butterfly Melitaea cinxia (Lepidoptera: Nymphalidae). Biol J Lin Soc 77:445–453

  38. Nowakowski AJ, Watling JI, Thompson ME, Brusch GA IV, Catenazzi A, Whitfield SM, Kurz DJ, Suárez-Mayorga Á, Aponte-Gutiérrez A, Donnelly MA, Todd BD (2018) Thermal biology mediates responses of amphibians and reptiles to habitat modification. Ecol Lett 21:345–355

  39. Nowakowski AJ, Watling JI, Whitfield SM, Todd BD, Kurz DJ, Donnelly MA (2017) Tropical amphibians in shifting thermal landscapes under land-use and climate change. Conserv Biol 31:96–105

  40. Parsons H (2007) Caring for Australian native birds. Kangaroo Press, New South Wales

  41. Peters RH (1983) The ecological implications of body size. Cambridge University Press, Cambridge

  42. Rasband, W. (2011). Image J 1.44o. National Institute of Health, USA. http://imagej.nih.gov

  43. R Development Core Team (2008) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. http://www.R-project.org

  44. Resasco J, Tuff KT, Cunningham SA, Melbourne BA, Hicks AL, Newsome SD, Davies KF (2017) Generalist predator’s niche shifts reveal ecosystem changes in an experimentally fragmented landscape. Ecography 41:1209–1219

  45. Salvidio S, Crovetto F, Adams DC (2015) Potential rapid evolution of foot morphology in Italian plethodontid salamanders (Hydromantes strinatii) following the colonization of an artificial cave. J Evol Biol 28:1403–1409

  46. Sample BE, Cooper RJ, Greer RD, Whitmore RC (1993) Estimation of insect biomass by length and width. Am Midl Nat 129(2):234–240

  47. Secretariat of the Convention on Biological Diversity (CBD) (2010) Global Biodiversity Outlook 3. CBD

  48. Sheridan JA, Bickford D (2011) Shrinking body size as an ecological response to climate change. Nat Clim Change 1:401–406

  49. Simbotwem MP (1985) Sexual dimorphism and reproduction of Lampropholis guichenoti (Lacertilia: Scincidae). In: Grigg G, Shine R, Ehmann HW (eds) The biology of Australasian frogs and reptiles. Royal Zoological Society of New South Wales, Sydney, pp 11–16

  50. Sinervo B, Adolph SC (1989) Thermal sensitivity of growth rate in hatchling Sceloporus lizards: environmental, behavioral and genetic aspects. Oecologia 78:411–419

  51. Slater P, Slater P, Slater R (2006) The slater field guide to Australian birds. New Holland Publishers, Sydney

  52. Standfuss M (1895) On causes of variation and aberration in the imago stage of butterflies, with suggestions on the establishment of new species. The Entomologist 28:69–76

  53. Stuart YE, Campbell TS, Hohenlohe PA, Reynolds RG, Revell LJ, Losos JB (2014) Rapid evolution of a native species following invasion by a congener. Science 346:463–466

  54. Sumner J, Moritz C, Shine R (1999) Shrinking forest shrinks skink: morphological change in response to rainforest fragmentation in the prickly forest skink (Gnypetoscincus queenslandiae). Biol Conserv 91:159–167

  55. Torr GA, Shine R (1993) Experimental analysis of thermally dependent behavior patterns in the Scincid lizard Lampropholis guichenoti. Copeia 3(3):850–854

  56. Tuff KT, Tuff T, Davies KF (2016) A framework for integrating thermal biology into fragmentation research. Ecol Lett 19:361–374

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Acknowledgements

We greatly appreciate the technical support and expertise of Dr. Beth Mantle, Nicole Fischer, and Robyn Meier of the Australian National Insect Collection, particularly for their use of the SatScan machine that made this study possible. We also thank Dr. Leo Joseph of the CSIRO Australian National Wildlife Collection for providing us access to the historic skink specimens and to Mr. John Wombey for identifying, aging, and processing skink specimens. The successful translation of the Wog Wog bird data was made possible by the generosity of Mrs. Katherine Nix, who graciously hosted KTT throughout the data entry and validation process. Funding was provided by the National Science Foundation (DEB 0841892 to KFD and BAM; and DEB 1350872 to KFD) and the University of Colorado’s Undergraduate Research Opportunity Program (UROP). Finally, we are grateful to Dr. Deahn Donner, Dr. Craig Moritz, and four reviewers whose comments greatly improved the manuscript. Finally, we are very grateful to Forestry Corportation of NSW and the NSW National Parks and Wildlife Service for permission to sample and for continued support for the experiment.

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Correspondence to Kendi F. Davies.

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Tuff, K.T., Glidden, C.K., Melbourne, B.A. et al. Shrinking skinks: lizard body size declines in a long-term forest fragmentation experiment. Landscape Ecol 34, 1395–1409 (2019). https://doi.org/10.1007/s10980-019-00853-4

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Keywords

  • Deforestation
  • Habitat fragmentation
  • Thermal biology
  • Temperature-size rule
  • Temperature
  • Morphometrics
  • Climate change
  • Ectotherms
  • Lampropholis guichenoti
  • Wog Wog