Skip to main content

Moving beyond the plane: measuring 3D home ranges of juvenile salamanders with passive integrated transponder (PIT) tags

Behavioral Ecology and Sociobiology volume 71, Article number: 59 (2017) Cite this article

Abstract

An individual’s home range, or how much space it requires to obtain resources and meet its needs for survival and reproduction, affects the scale of many fundamental processes in ecology and can inform the management of species. Although home range size has been described for many taxa in two dimensions (2D), for species that also have a strong vertical component to their movement, such representations can miss core components of their ecology, including the size of their home ranges and the amount of overlap, and thus competition, between individuals. Measuring three-dimensional (3D) home ranges for small-bodied life history stages and species can be particularly difficult, as they cannot tolerate high resolution tracking technologies like GPS collars. In this study, we used Passive Integrated Transponder (PIT) tags to measure the 2D and 3D home ranges of two species of fossorial juvenile salamander: the ringed salamander (Ambystoma annulatum) and the spotted salamander (A. maculatum). We also tested whether individuals modified their habitat selection or movement behavior in response to environmental variation. Salamanders in our study frequently used subterranean habitats. However, we rarely detected them more than 5 cm below ground. Additionally, the overlap among 2D and 3D home ranges, respectively, were similar. These findings indicate that these salamanders may move vertically through their habitat less than previously thought. Alternatively, salamanders may have moved into soil strata beyond the detection range of PIT telemetry. We conclude that PIT telemetry can be a suitable technique for determining the 3D home range of fossorial life-stages or species for which other tracking technologies are unsuitable.

Significance statement

When animal behavior includes movements with a vertical component, simplifying assumptions of 2D home ranges can affect ecological inferences by overestimating competition between individuals and underestimating home range size. We used Passive Integrated Transponder (PIT) tags to describe the home range of fossorial juvenile salamanders in 3D. The juvenile salamanders in this study modulated their habitat selection in response to weather, but in general remained close to the soil surface. As a result, juveniles may be more susceptible than previously thought to habitat management practices that alter the local microclimate. Because individuals moved vertically less than predicted, 2D and 3D home ranges had similar patterns. We demonstrate that PIT telemetry can facilitate subterranean tracking of a cryptic life stage. However, this technology is limited in its subterranean detection depth, and until antenna strength is improved, the resolution of 3D home ranges may be limited.

This is a preview of subscription content, access via your institution.

Access options

Buy single article

Instant access to the full article PDF.

USD 39.95

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

References

  • Amarasekare P (2003) Competitive coexistence in spatially structured environments: a synthesis. Ecol Lett 6:1109–1122

    Article  Google Scholar 

  • Baddeley A, Turner R (2005) Spatstat: an R package for analyzing spatial point patterns. J Stat Softw 12:1–42

    Article  Google Scholar 

  • Badje AF, Brandt TJ, Bergeson TL, Paloski RA, Kapfer JM, Shuurman GW (2016) Blachard’s cricket frog Acris blanchardi overwintering ecology in southwestern Wisconsin. Herpetol Conserv Biol 11:101–111

    Google Scholar 

  • Banse K, English DC (1999) Comparing phytoplankton seasonality in the eastern and western subarctic Pacific and the western Bering Sea. Prog Oceanogr 43:235–288

    Article  Google Scholar 

  • Belant JL, Millspaugh JJ, Martin JA, Gitzen RA (2012) Multi-dimensional space use: the final frontier. Front Ecol Environ 10:11–12

    Article  Google Scholar 

  • Börger L, Dalziel BD, Fryxell JM (2008) Are there general mechanisms of animal home range behaviour? A review and prospects for future research. Ecol Lett 11:637–650

    Article  PubMed  Google Scholar 

  • Bouten W, Baaij EW, Shamoun-Baranes J, Camphuysen KCJ (2013) A flexible GPS tracking system for studying bird behaviour at multiple scales. J Ornithol 154:571–580

    Article  Google Scholar 

  • Burt WH (1943) Territoriality and home range concepts as applied to mammals. J Mammal 24:346–352

    Article  Google Scholar 

  • Cardillo M, Mace GM, Gittleman JL, Jones KE, Bielby J, Purvis A (2008) The predictability of extinction: biological and external correlates of decline in mammals. Proc R Soc Lond B 275:1441–1448

    Article  Google Scholar 

  • Connette GM, Semlitsch RD (2012) Successful use of a passive integrated transponder (PIT) system for below-ground detection of plethodontid salamanders. Wildlife Res 39:1–6

    Article  Google Scholar 

  • Connior MB, Kershen AA, Medlin RE, Elrod DA, Sasse DB, Risch TS (2010) Distribution and habitat attributes of an endemic subspecies of pocket gopher. Am Midl Nat 164:217–229

    Article  Google Scholar 

  • Cunha AA, Vieira MV (2004) Two bodies cannot occupy the same place at the same time, or the importance of space in the ecological niche. Bull Ecol Soc Am 85:25–26

    Article  Google Scholar 

  • Curry JP (1994) Grassland invertebrates: ecology, influence on soil fertility and effects on plant growth. Chapman and Hall, London

    Google Scholar 

  • Duong T (2007) Ks: kernel density estimation and kernel discriminant analysis for multivariate data in R. J Stat Softw 21:1–16

    Article  Google Scholar 

  • Earl JE, Zollner PA (2014) Effects of animal movement strategies and costs on the distribution of active subsidies across simple landscapes. Ecol Model 283:45–52

    Article  Google Scholar 

  • Fournier D, Skaug H, Ancheta J, Ianelli J, Magnusson A, Maunder M, Nielsen A, Sibert J (2012) AD model builder: using automatic differentiation for statistical inference of highly parameterized complex nonlinear models. Optim Methods Softw 27:233–249

    Article  Google Scholar 

  • Gibbons JW, Andrews KM (2004) PIT tagging: simple technology at its best. Bioscience 54:447–454

    Article  Google Scholar 

  • Greene KM, Pittman SE, Dorcas ME (2016) The effects of conspecifics on burrow selection in juvenile spotted salamanders (Ambystoma maculatum). J Ethol 34:309–314

    Article  Google Scholar 

  • Grover MC (2000) Determinants of salamander distributions along moisture gradients. Copeia 2000:156–168

    Article  Google Scholar 

  • Hebblewhite M, Haydon DT (2010) Distinguishing technology from biology: a critical review of the use of GPS telemetry data in ecology. Philos T Roy Soc B 365:2303–2312

    Article  Google Scholar 

  • Heemeyer JL, Williams PJ, Lannoo MJ (2012) Obligate crayfish burrow use and core habitat requirements of crawfish frogs. J Wildlife Manage 76:1081–1091

    Article  Google Scholar 

  • Hocking DJ, Rittenhouse TAG, Rothermel BB, Johnson JR, Conner CA, Harper EB, Semlitsch RD (2008) Breeding and recruitment phenology of amphibians in Missouri oak-hickory forests. Am Midl Nat 160:41–60

    Article  Google Scholar 

  • Jacobs KA, Nix B, Scharenbroch BC (2015) The effects of prescribed burning on soil and litter invertebrate diversity and abundance in an Illinois oak woodland. Nat Area J 36:318–327

    Article  Google Scholar 

  • Johnson JR, Mahan RD, Semlitsch RD (2008) Seasonal terrestrial microhabitat use by gray treefrogs (Hyla versicolor) in Missouri oak-hickory forests. Herpetologica 64:259–269

    Article  Google Scholar 

  • Kane DL, Hinkel KM, Goering DJ, Hinzman LD, Outcalt SI (2001) Non-conductive heat transfer associated with frozen soils. Glob Planet Chang 29:275–292

    Article  Google Scholar 

  • Kleeberger SR (1985) Influence of intraspecific density and cover on home range of a plethodontid salamander. Oecologia 66:404–410

    Article  PubMed  Google Scholar 

  • Kleeberger SR, Werner JK (1982) Home range and homing behavior in Plethodon cinereus in northern Michigan. Copeia 1982:409–415

    Article  Google Scholar 

  • Kleeberger SR, Werner JK (1983) Post-breeding migration and summer movement of Ambystoma maculatum. J Herpetol 17:176–177

    Article  Google Scholar 

  • Laundré JW, Reynolds TD (1993) Effects of soil structure on burrow characteristics of five small mammal species. West N Am Naturalist 53:358–366

    Google Scholar 

  • Laver PN, Kelly MJ (2008) A critical review of home range studies. J Wildlife Manage 72:290–298

    Article  Google Scholar 

  • Liebgold EB, Jaeger RG (2007) Juvenile movements and potential inter-age class associations of red-backed salamanders. Herpetologica 63:51–55

    Article  Google Scholar 

  • Lindstedt SL, Miller BJ, Buskirk SW (1986) Home range, time, and body size in mammals. Ecology 67:413–418

    Article  Google Scholar 

  • Loredo I, Van Vuren D, Morrison ML (1996) Habitat use and migration behavior of the California tiger salamander. J Herpetol 30:282–285

    Article  Google Scholar 

  • Marzluff JM, Millspaugh JJ, Hurvitz P, Handcock MS (2004) Relating resources to a probabalistic measure of space use: forest fragments and Steller’s jays. Ecology 85:1411–1427

    Article  Google Scholar 

  • Middleton AD, Kauffman MJ, Mcwhirter DE, Cook JG, Cook RC, Nelson AA, Jimenez MD, Klaver RW (2013) Animal migration amid shifting patterns of phenology and predation: lessons from a Yellowstone elk herd. Ecology 94:1245–1256

    Article  PubMed  Google Scholar 

  • Morales JM, Moorcroft PR, Matthiopoulos J, Frair JL, Kie JG, Powell RA, Merrill EH, Haydon DT (2010) Building the bridge between animal movement and population dynamics. Philos T Roy Soc B 365:2289–2301

    Article  Google Scholar 

  • Nussbaum SE, Ousterhout BH, Semlitsch RD (2016) Agonistic behavior and resource defense among sympatric juvenile pond-breeding salamanders. J Herpetol 50:388–393

    Article  Google Scholar 

  • O’Donnell KM, Semlitsch RD (2015) Advancing terrestrial salamander population ecology: the central role of imperfect detection. J Herpetol 49:533–540

    Article  Google Scholar 

  • O’Donnell KM, Thompson FR, Semlitsch RD (2015) Partitioning detectability components in populations subject to within-season temporary emigration using binomial mixture models. PLoS One 10:e0117216

    Article  PubMed  PubMed Central  Google Scholar 

  • O’Donnell KM, Thompson FR, Semlitsch RD (2016) Prescribed fire alters surface activity and movement behavior of a terrestrial salamander. J Zool 298:303–309

    Article  Google Scholar 

  • Osbourn MS, Connette GM, Semlitsch RD (2014) Effects of fine-scale forest habitat quality on movement and settling decisions in juvenile pond-breeding salamanders. Ecol Appl 24:1719–1729

    Article  Google Scholar 

  • Ousterhout BH, Liebgold EB (2010) Dispersal versus site tenacity of adult and juvenile red-backed salamanders (Plethodon cinereus). Herpetologica 66:269–275

    Article  Google Scholar 

  • Ousterhout BH, Semlitsch RD (2014) Measuring terrestrial movement behavior using passive integrated transponder (PIT) tags: effects of tag size on detection, movement, survival, and growth. Behav Ecol Sociobiol 68:343–350

    Article  Google Scholar 

  • Ousterhout BH, Semlitsch RD (2016) Non-additive response of larval ringed salamanders to intraspecific density. Oecologia 180:1137–1145

    Article  PubMed  Google Scholar 

  • Peterman WE, Locke JL, Semlitsch RD (2013) Spatial and temporal patterns of water loss in heterogeneous landscapes: using plaster models as amphibian analogues. Can J Zool 140:135–140

    Article  Google Scholar 

  • Petranka JW (1998) Salamanders of the United States and Canada. Smithsonian Institution Press, Washington, DC

    Google Scholar 

  • Pittman SE, Osbourn MS, Semlitsch RD (2014) Movement ecology of amphibians: a missing component for understanding population declines. Biol Conserv 169:44–53

    Article  Google Scholar 

  • Powell RA, Mitchell MS (2012) What is a home range? J Mammal 93:948–958

    Article  Google Scholar 

  • R Core Team (2016) R: a language and environment for statistical computing, version 3.3.0. R Foundation for Statistical Computing, Vienna http://www.R-project.org

    Google Scholar 

  • Reichman OJ, Smith SC (1990) Burrows and burrowing behavior by mammals. In: Genoways HH (ed) Current Mammology. Plenum Press, New York, pp 197–244

    Google Scholar 

  • Rosenberg DK, Noon BR, Megahan JW, Meslow EC (1998) Compensatory behavior of Ensatina eschscholtzii in biological corridors: a field experiment. Can J Zool 76:117–133

    Article  Google Scholar 

  • Rothermel BB, Luhring TM (2005) Burrow availability and desiccation risk of mole salamanders (Ambystoma talpoideum) in harvested versus unharvested forest stands. J Herpetol 39:619–626

    Article  Google Scholar 

  • Rothermel BB, Semlitsch RD (2002) An experimental investigation of landscape resistance of forest versus old-field habitats to emigrating juvenile amphibians. Conserv Biol 16:1324–1332

    Article  Google Scholar 

  • Rothermel BB, Semlitsch RD (2006) Consequences of forest fragmentation for juvenile survival in spotted (Ambystoma maculatum) and marbled (Ambystoma opacum) salamanders. Can J Zool 84:797–807

    Article  Google Scholar 

  • Ryan KJ, Calhoun AJK (2014) Postbreeding habitat use of the rare, pure-diploid blue-spotted salamander (Ambystoma laterale). J Herpetol 48:556–566

    Article  Google Scholar 

  • Schabetsberger R, Jehle R, Maletzky A, Pesta J, Sztatecsny M (2004) Delineation of terrestrial reserves for amphibians: post-breeding migrations of Italian crested newts (Triturus C. carnifex) at high altitude. Biol Conserv 117:95–104

    Article  Google Scholar 

  • Seaman DE, Millspaugh JJ, Kernohan BJ, Brundige GC, Raedeke KJ, Gitzen RA (1999) Effects of sample size on kernel home range estimates. J Wildlife Manage 63:739–747

    Article  Google Scholar 

  • Semlitsch RD (1981) Terrestrial activity and summer home range of the mole salamander (Ambystoma talpoideum). Can J Zool 59:315–322

    Article  Google Scholar 

  • Semlitsch RD (1983) Burrowing ability and behavior of salamanders of the genus Ambystoma. Can J Zool 61:616–620

    Article  Google Scholar 

  • Semlitsch RD, Bodie JR (1998) Are small, isolated wetlands expendable? Conserv Biol 12:1129–1133

    Article  Google Scholar 

  • Semlitsch RD, Pechmann JHK (1985) Diel pattern of migratory activity for several species of pond-breeding salamanders. Copeia 1985:86–91

    Article  Google Scholar 

  • Semlitsch RD, Anderson TL, Osbourn MS, Ousterhout BH (2014) Structure and dynamics of ringed salamander (Ambystoma annulatum) populations in Missouri. Herpetologica 7:14–22

    Article  Google Scholar 

  • Simpfendorfer CA, Olsen EM, Heupel MR, Moland E (2012) Three-dimensional kernel utilization distributions improve estimates of space use in aquatic animals. Can J Fish Aquat Sci 69:565–572

    Article  Google Scholar 

  • Skaug H, Fournier D, Bolker BM, Magnusson A, Nielsen A (2016) Generalized linear mixed models using AD Model Builder. R package version 0.8.3.3, http://glmmadmb.r-forge.r-project.org/

  • Spotila JR, Berman EN (1976) Determination of skin resistance and the role of the skin in controlling water loss in amphibians and reptiles. Comp Biochem Physiol 55:407–411

    Article  CAS  Google Scholar 

  • Tilzer MM (1973) Diurnal periodicity in the phytoplankton assemblage of a high mountain lake. Limnol Oceanogr 18:15–30

    Article  Google Scholar 

  • Tracey JA, Sheppard J, Zhu J, Wei F, Swaisgood RR, Fisher RN (2014) Movement-based estimation and visualization of space use in 3D for wildlife ecology and conservation. PLoS One 9:e101205

    Article  PubMed  PubMed Central  Google Scholar 

  • Trenham PC (2001) Terrestrial habitat use by adult California tiger salamanders. J Herpetol 35:343–346

    Article  Google Scholar 

  • Valenzuela-Sánchez A, Harding G, Cunningham AA, Chirgwin C, Soto-Azat C (2014) Home range and social analyses in a mouth brooding frog: testing the coexistence of paternal care and male territoriality. J Zool 294:215–223

    Article  Google Scholar 

  • Wells KD (2007) The ecology and behavior of amphibians. University of Chicago Press, Chicago

    Book  Google Scholar 

  • Williams PK (1973) Seasonal movements and population dynamics of four sympatric mole salamanders, genus Ambystoma. PhD-thesis. Indiana University, Bloomington

Download references

Acknowledgements

Comments from the Semlitsch lab and three reviewers greatly improved this manuscript. We thank K. Lohraff and J. Matta for allowing us to conduct this research at Fort Leonard Wood. This work was supported by the Department of Defense (SERDP RC-2155), NSF DEB-1620046, and a Life Sciences Fellowship (BHO).

Author information

Author notes

  1. Brittany H. Ousterhout

    Present address: Department of Biological Sciences, University of Arkansas, Fayetteville, AR, 72701, USA

Authors and Affiliations

  1. Division of Biological Sciences, University of Missouri, Columbia, MO, 65211, USA

    Brittany H. Ousterhout & Jacob J. Burkhart

Authors
  1. Brittany H. Ousterhout
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Jacob J. Burkhart
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Brittany H. Ousterhout.

Ethics declarations

This research complies with the current laws of the USA and was conducted under Missouri Department of Conservation Permits 14922 and 15186 and approved by the University of Missouri Animal Care and Use Committee (7403).

Additional information

Communicated by L. Z. Garamszegi

Brittany H. Ousterhout and Jacob J. Burkhart contributed equally to this work

Electronic supplementary material

ESM 1

(PDF 655 kb)

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Ousterhout, B.H., Burkhart, J.J. Moving beyond the plane: measuring 3D home ranges of juvenile salamanders with passive integrated transponder (PIT) tags. Behav Ecol Sociobiol 71, 59 (2017). https://doi.org/10.1007/s00265-017-2284-6

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s00265-017-2284-6

Keywords

  • Ambystoma spp.
  • Core area
  • Kernel density estimation
  • Minimum convex polygon
  • Ringed salamander
  • Spotted salamander