Abstract
Models based on functional traits have limited power in predicting how animal populations respond to disturbance because they do not capture the range of demographic and biological factors that drive population dynamics, including variation in trophic interactions. I tested the hypothesis that successional changes in vegetation structure, which affected invertebrate abundance, would influence growth rates and body condition in the early-successional, insectivorous gecko Nephrurus stellatus. I captured geckos at 17 woodland sites spanning a succession gradient from 2 to 48 years post-fire. Body condition and growth rates were analysed as a function of the best-fitting fire-related predictor (invertebrate abundance or time since fire) with different combinations of the co-variates age, sex and location. Body condition in the whole population was positively affected by increasing invertebrate abundance and, in the adult population, this effect was most pronounced for females. There was strong support for a decline in growth rates in weight with time since fire. The results suggest that increased early-successional invertebrate abundance has filtered through to a higher trophic level with physiological benefits for insectivorous geckos. I integrated the new findings about trophic interactions into a general conceptual model of mechanisms underlying post-fire population dynamics based on a long-term research programme. The model highlights how greater food availability during early succession could drive rapid population growth by contributing to previously reported enhanced reproduction and dispersal. This study provides a framework to understand links between ecological and physiological traits underlying post-fire population dynamics.
Similar content being viewed by others
References
Banks SC, Blyton MDJ, Blair D, McBurney L, Lindenmayer DB (2012) Adaptive responses and disruptive effects: how major wildfire influences kinship-based social interactions in a forest marsupial. Mol Ecol 21:673–684
Bargmann T, Heegaard E, Hatteland BA, Chipperfield JD, Grytnes JA (2016) Species trait selection along a prescribed fire chronosequence. Insect Conserv Divers 9:446–455
Bates D, Maechler M, Bolker B (2013) lme4: linear mixed-effects models using S4 classes. R package, version 0.999999-2
Bowman DM, Perry GL, Higgins SI, Johnson CN, Fuhlendorf SD, Murphy BP (2016) Pyrodiversity is the coupling of biodiversity and fire regimes in food webs. Philos Trans R Soc Lond B Biol Sci 371. https://doi.org/10.1098/rstb.2015.0169
Burgess EE, Maron M (2016) Does the response of bird assemblages to fire mosaic properties vary among spatial scales and foraging guilds? Landsc Ecol 31:687–699
Campos Z, Magnusson WE, Marques V (2013) Growth rates of Paleosuchus palpebrosus at the southern limit of its range. Herpetologica 69:405–410
Caughley J (1985) Effect of fire on the reptile fauna of mallee. In: Grigg G, Shine R, Ehmann H (eds) Biology of Australasian frogs and reptiles. Royal Zoological Society of NSW and Surrey Beatty & Sons, Chipping Norton, pp 31–34
Caut S, Jowers MJ, Arnan X, Pearce-Duvet J, Rodrigo A, Cerda X, Boulay RR (2014) The effects of fire on ant trophic assemblage and sex allocation. Ecol Evol 4:35–49
Chamaillé-Jammes S, Massot M, Aragón P, Clobert J (2006) Global warming and positive fitness response in mountain populations of common lizards Lacerta vivipara. Glob Change Biol 12:392–402
Cherry MJ, Warren RJ, Mike Conner L (2016) Fear, fire, and behaviorally mediated trophic cascades in a frequently burned savanna. For Ecol Manag 368:133–139
Cox RM, Parker EU, Cheney DM, Liebl AL, Martin LB, Calsbeek R (2010) Experimental evidence for physiological costs underlying the trade-off between reproduction and survival. Funct Ecol 24:1262–1269
Cunningham HR, Rissler LJ, Apodaca JJ (2009) Competition at the range boundary in the slimy salamander: using reciprocal transplants for studies on the role of biotic interactions in spatial distributions. J Anim Ecol 78:52–62
Davies AB, Eggleton P, van Rensburg BJ, Parr CL (2012) The pyrodiversity–biodiversity hypothesis: a test with savanna termite assemblages. J Appl Ecol 49:422–430
Di Stefano J, Ashton A, York A (2014) Diet of the silky mouse (Pseudomys apodemoides) and the heath rat (P. shortridgei) in a post-fire environment. Int J Wildland Fire 23:746–753
Driscoll DA, Henderson MK (2008) How many common reptile species are fire specialists? A replicated natural experiment highlights the predictive weakness of a fire succession model. Biol Conserv 141:460–471
Driscoll DA, Lindenmayer DB, Bennett AF, Bode M, Bradstock RA, Cary GJ, Clarke MF, Dexter N, Fensham R, Friend G, Gill AM, James S, Kay G, Keith DA, MacGregor C, Russell-Smith J, Salt D, Watson JEM, Williams RJ, York A (2010) Fire management for biodiversity conservation: key research questions and our capacity to answer them. Biol Conserv 143:1928–1939
Driscoll DA, Smith AL, Blight SR, Maindonald J (2012) Reptile responses to fire and the risk of post-disturbance sampling bias. Biodivers Conserv 21:1607–1625
Ferran A, Vallejo VR (1992) Litter dynamics in post-fire successional forests of Quercus ilex. Vegetatio 99(100):239–246
Forero MG, Tella JL, Hobson KA, Bertellotti M, Blanco G (2002) Conspecific food competition explains variability in colony size: a test in magellanic penguins. Ecology 83:3466–3475
Fox BJ (1982) Fire and mammalian secondary succession in an Australian coastal heath. Ecology 63:1332–1341
García Y, Castellanos MC, Pausas JG (2016) Fires can benefit plants by disrupting antagonistic interactions. Oecologia 182:1165–1173
Gascoigne J, Berec L, Gregory S, Courchamp F (2009) Dangerously few liaisons: a review of mate-finding Allee effects. Popul Ecol 51:355–372
Gibson RK, Bradstock RA, Penman T, Keith DA, Driscoll DA (2015) Climatic, vegetation and edaphic influences on the probability of fire across mediterranean woodlands of south-eastern Australia. J Biogeogr 42:1750–1760
Greenville AC, Wardle GM, Nguyen V, Dickman CR (2016) Spatial and temporal synchrony in reptile population dynamics in variable environments. Oecologia 182:475–485
Hawlena D, Saltz D, Abramsky Z, Bouskila A (2010) Ecological trap for desert lizards caused by anthropogenic changes in habitat structure that favor predator activity. Conserv Biol 24:803–809
Hegyi G, Garamszegi L (2011) Using information theory as a substitute for stepwise regression in ecology and behavior. Behav Ecol Sociobiol 65:69–76
Hodges KE, Boonstra R, Krebs CJ (2006) Overwinter mass loss of snowshoe hares in the Yukon: starvation, stress, adaptation or artefact? J Anim Ecol 75:1–13
Hossack BR, Eby LA, Guscio CG, Corn PS (2009) Thermal characteristics of amphibian microhabitats in a fire-disturbed landscape. For Ecol Manag 258:1414–1421
Hu Y, Urlus J, Gillespie G, Letnic M, Jessop TS (2013) Evaluating the role of fire disturbance in structuring small reptile communities in temperate forests. Biodivers Conserv 22:1949–1963
Jarvie S, Senior AM, Adolph SC, Seddon PJ, Cree A (2015) Captive rearing affects growth but not survival in translocated juvenile tuatara. J Zool 297:184–193
Joern A, Provin T, Behmer ST (2012) Not just the usual suspects: insect herbivore populations and communities are associated with multiple plant nutrients. Ecology 93:1002–1015
Keith DA, Holman L, Rodoreda S, Lemmon J, Bedward M (2007) Plant functional types can predict decade-scale changes in fire-prone vegetation. J Ecol 95:1324–1337
Kelly LT, Nimmo DG, Spence-Bailey LM, Haslem A, Watson SJ, Clarke MF, Bennett AF (2011) Influence of fire history on small mammal distributions: insights from a 100-year post-fire chronosequence. Divers Distrib 17:462–473
Leahy L, Legge SM, Tuft K, McGregor HW, Barmuta LA, Jones ME, Johnson CN (2016) Amplified predation after fire suppresses rodent populations in Australia’s tropical savannas. Wildl Res 42:705–716
Letnic M, Dickman CR (2010) Resource pulses and mammalian dynamics: conceptual models for hummock grasslands and other Australian desert habitats. Biol Rev 85:501–521
Liebhold A, Sharov A (1998) Testing for correlation in the presence of spatial autocorrelation in insect count data. In: Baumgartner J (ed) Population and community ecology for insect management and conservation. A.A. Balkema, Rotterdam, pp 111–117
MacGregor HEA, While GM, Uller T (2017) Comparison of reproductive investment in native and non-native populations of common wall lizards reveals sex differences in adaptive potential. Oikos 126:1564–1574
Mazerolle MJ (2012) AICcmodavg. R package, version 1.26
McCoy ED, Styga JM, Rizkalla CE, Mushinsky HR (2012) Time since fire affects ectoparasite prevalence on lizards in the Florida scrub ecosystem. Fire Ecol 8:32–40
McGregor HW, Legge S, Jones ME, Johnson CN (2014) Landscape management of fire and grazing regimes alters the fine-scale habitat utilisation by feral cats. PLoS ONE 9:e109097
Meiri S (2010) Length–weight allometries in lizards. J Zool 281:218–226
Moritz MA, Parisien M-A, Batllori E, Krawchuk MA, Van Dorn J, Ganz DJ, Hayhoe K (2012) Climate change and disruptions to global fire activity. Ecosphere 3:art49
Naulleau G, Bonnet X (1996) Body condition threshold for breeding in a viviparous snake. Oecologia 107:301–306
Nimmo DG, Kelly LT, Spence-Bailey LM, Watson SJ, Haslem A, White JG, Clarke MF, Bennett AF (2012) Predicting the century-long post-fire responses of reptiles. Glob Ecol Biogeogr 21:1062–1073
Nimmo DG, Kelly LT, Farnsworth LM, Watson SJ, Bennett AF (2014) Why do some species have geographically varying responses to fire history? Ecography 37:805–813
Pausas JG (2015) Bark thickness and fire regime. Funct Ecol 29:315–327
Phillips BL (2009) The evolution of growth rates on an expanding range edge. Biol Lett 5:802–804
Pianka ER (1969) Habitat specificity, speciation, and species density in Australian desert lizards. Ecology 50:498–502
R Core Team (2017) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna. http://www.R-project.org
Radchuk V, Ims RA, Andreassen HP (2016) From individuals to population cycles: the role of extrinsic and intrinsic factors in rodent populations. Ecology 97:720–732
Ribeiro PJ Jr, Diggle PJ (2001) geoR: a package for geostatistical analysis. R News 1:14–18
Ruffino L, Salo P, Koivisto E, Banks PB, Korpimäki E (2014) Reproductive responses of birds to experimental food supplementation: a meta-analysis. Front Zool 11:80
Santos X, Mateos E, Bros V, Brotons L, De Mas E, Herraiz JA, Herrando S, Miño À, Olmo-Vidal JM, Quesada J, Ribes J, Sabaté S, Sauras-Yera T, Serra A, Vallejo VR, Viñolas A (2014) Is response to fire influenced by dietary specialization and mobility? A comparative study with multiple animal assemblages. PLoS ONE 9:e88224
Sanz-Aguilar A, Anadón JD, Giménez A, Ballestar R, Graciá E, Oro D (2011) Coexisting with fire: the case of the terrestrial tortoise Testudo graeca in mediterranean shrublands. Biol Conserv 144:1040–1049
Silvério DV, Brando PM, Balch JK, Putz FE, Nepstad DC, Oliveira-Santos C, Bustamante MM (2013) Testing the Amazon savannization hypothesis: fire effects on invasion of a neotropical forest by native cerrado and exotic pasture grasses. Philos Trans R Soc Lond B Biol Sci 368. https://doi.org/10.1098/rstb.2012.0427
Smith AL, Bull CM, Driscoll DA (2012) Post-fire succession affects abundance and survival but not detectability in a knob-tailed gecko. Biol Conserv 145:139–147
Smith AL, Bull CM, Driscoll DA (2013a) Skeletochronological analysis of age in three ‘fire-specialist’ lizard species. S Aust Nat 87:6–17
Smith AL, Bull CM, Driscoll DA (2013b) Successional specialization in a reptile community cautions against widespread planned burning and complete fire suppression. J Appl Ecol 50:1178–1186
Smith AL, Blanchard W, Blair D, McBurney L, Banks SC, Driscoll DA, Lindenmayer DB (2016a) The dynamic regeneration niche of a forest following a rare disturbance event. Divers Distrib 22:457–467
Smith AL, Landguth EL, Bull CM, Banks SC, Gardner MG, Driscoll DA (2016b) Dispersal responses override density effects on genetic diversity during post-disturbance succession. Proc R Soc Lond B 283:20152934
St. Clair SB, O’Connor R, Gill R, McMillan B (2016) Biotic resistance and disturbance: rodent consumers regulate post-fire plant invasions and increase plant community diversity. Ecology 97:1700–1711
Teasdale LC, Smith AL, Thomas M, Whitehead CA, Driscoll DA (2013) Detecting invertebrate responses to fire depends on sampling method and taxonomic resolution. Austral Ecol 38:874–883
Templeton AR, Brazeal H, Neuwald JL (2011) The transition from isolated patches to a metapopulation in the eastern collared lizard in response to prescribed fires. Ecology 92:1736–1747
Therrien JF, Gauthier G, Korpimäki E, Bêty J (2014) Predation pressure by avian predators suggests summer limitation of small-mammal populations in the Canadian Arctic. Ecology 95:56–67
Vernes K, Haydon DT (2001) Effect of fire on northern bettong (Bettongia tropica) foraging behaviour. Austral Ecol 26:649–659
Wang Y, Zeng Z-G, Ma L, Li S-R, Du W-G (2017) Food restriction affects maternal investment but not neonate phenotypes in a viviparous lizard. Zool Res 38:81–87
Webb JK, Shine R (1998) Ecological characteristics of a threatened snake species, Hoplocephalus bungaroides (Serpentes, Elapidae). Anim Conserv 1:185–193
Westgate MJ, Driscoll DA, Lindenmayer DB (2012) Can the intermediate disturbance hypothesis and information on species traits predict anuran responses to fire? Oikos 121:1516–1524
Wikelski M, Wrege PH (2000) Niche expansion, body size, and survival in Galápagos marine iguanas. Oecologia 124:107–115
Wright AN, Piovia-Scott J, Spiller DA, Takimoto G, Yang LH, Schoener TW (2013) Pulses of marine subsidies amplify reproductive potential of lizards by increasing individual growth rate. Oikos 122:1496–1504
Zuur AF, Ieno EN, Walker NJ, Saveliev AA, Smith GM (2009) Mixed effects models and extensions in ecology with R. Springer, New York
Acknowledgements
This paper is dedicated to the memory of Professor C. Michael Bull (1947–2016) and Mr Dale Burzacott (1958–2017) who ran a productive, honest and friendly research laboratory together for over 30 years. They made substantial contributions to lizard population ecology and will be missed as mentors and friends. Don Driscoll and C. Michael Bull were involved in the design of a broader project during which data for this project were collected. Over 40 volunteers were involved in field work, particularly Samantha Blight, Simone Dalgairns, Juliana Lazzari, Kevin Mayes and Catherine Whitehead. Joe Tilley and the South Australian Department of Environment, Water and Natural Resources (DEWNR) provided field support. The research was funded by the Australian Research Council (LP0776604), Native Vegetation Council of South Australia, DEWNR, Wildlife Conservation Fund, Sir Mark Mitchell Research Foundation, Lirabenda Endowment Fund, Ecological Society of Australia and Australian National University.
Author information
Authors and Affiliations
Contributions
ALS conceived, designed and executed this study and wrote the manuscript. No other person is entitled to authorship.
Corresponding author
Ethics declarations
Ethical approval
All applicable institutional and national guidelines for the care and use of animals were followed. I followed the Australian code for the care and use of animals for scientific purposes and worked under scientific (S25589 Government of South Australian) and animal ethics (E256 Flinders University) permits.
Data accessibility
Data supporting this article have been uploaded as part of the Electronic Supplementary Material.
Additional information
Communicated by Jean-François Le Galliard.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Smith, A.L. Successional changes in trophic interactions support a mechanistic model of post-fire population dynamics. Oecologia 186, 129–139 (2018). https://doi.org/10.1007/s00442-017-4016-z
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00442-017-4016-z