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Wildlife Research Wildlife Research Society
Ecology, management and conservation in natural and modified habitats
RESEARCH ARTICLE

Variable reptile responses to introduced predator control in southern Australia

Yang Hu https://orcid.org/0000-0002-7740-7138 A C , Graeme Gillespie B and Tim S. Jessop A
+ Author Affiliations
- Author Affiliations

A Centre for Integrative Ecology, Deakin University, Waurn Ponds, Geelong, Vic. 3216, Australia.

B Department of Environment and Natural Resources, Palmerston, NT 0830, Australia.

C Corresponding author. Email: yhu0855@yahoo.com

Wildlife Research 46(1) 64-75 https://doi.org/10.1071/WR18047
Submitted: 13 March 2018  Accepted: 24 October 2018   Published: 21 January 2019

Abstract

Context: Australia harbours an immense diversity of reptiles, which are generally expected to have frequent and diverse trophic interactions with introduced mammalian carnivores. Nevertheless, the potential for predatory or competitive interactions is likely to be contingent on multiple processes, including the importance of reptiles in the diet of introduced predators, alongside overlaps in their body sizes and ecological niches that would influence the strength of their interactions. In Australia’s temperate and relatively productive mesic environments there is little understanding of how introduced mammalian predators affect reptile assemblages.

Aims: The aim was to investigate the effects that a European red fox (Vulpes vulpes; 5–7 kg) suppression program had on the abundance and species richness of a reptile community, with species ranging in size from the largest local ectothermic predator, the lace monitor (Varanus varius; 4–7 kg), to small terrestrial reptiles (mostly 10–150 g).

Methods: We utilised two sampling designs (baited camera monitoring stations and pitfall trapping) to evaluate the effects of fox suppression and other site-level ecological covariates (fire regime and habitat vegetation characteristics) on the lace monitor and small terrestrial reptiles. Reptile abundance and richness at site level were estimated from count-related abundance models.

Key results: For lace monitors, significantly higher abundances occurred in poison-baited areas relative to control areas. This suggests that fox suppression can affect the populations of the lace monitor via mesopredator release arising from reduced competition and, possibly, predation. For small terrestrial reptiles, neither abundance nor species richness were influenced by fox suppression. Individual abundances of the three most common small reptile species matched the overall pattern, as only responses to structural parameters of the habitat were detected.

Conclusions: Fox suppression can have different impacts for different reptile taxa, pending their ecological niche, as only the largest species was affected.

Implications: Increase in lace monitor abundance may change food web dynamics in fox-suppressed sites, such as by increasing predation pressure on arboreal marsupials.

Additional keywords: exotic pest, varanid lizards, skinks, herpetofauna.


References

Amarasekare, P. (2007). Trade-offs, temporal variation, and species coexistence in communities with intraguild predation. Ecology 88, 2720–2728.
Trade-offs, temporal variation, and species coexistence in communities with intraguild predation.Crossref | GoogleScholarGoogle Scholar | 18051639PubMed |

Amarasekare, P., and Nisbet, R. M. (2001). Spatial heterogeneity, source-sink dynamics, and the local coexistence of competing species. American Naturalist 158, 572–584.
| 18707352PubMed |

Anson, J. R., Dickman, C. R., Boonstra, R., and Jessop, T. S. (2013). Stress triangle: do introduced predators exert indirect costs on native predators and prey? PLoS One 8, e60916.
Stress triangle: do introduced predators exert indirect costs on native predators and prey?Crossref | GoogleScholarGoogle Scholar | 23585861PubMed |

Anson, J. R., Dickman, C. R., Handasyde, K., and Jessop, T. S. (2014). Effects of multiple disturbance processes on arboreal vertebrates in eastern Australia: implications for management. Ecography 37, 357–366.
Effects of multiple disturbance processes on arboreal vertebrates in eastern Australia: implications for management.Crossref | GoogleScholarGoogle Scholar |

Berger, K. M., and Gese, E. M. (2007). Does interference competition with wolves limit the distribution and abundance of coyotes? Journal of Animal Ecology 76, 1075–1085.
Does interference competition with wolves limit the distribution and abundance of coyotes?Crossref | GoogleScholarGoogle Scholar | 17922704PubMed |

Brown, G. W. (2001). The influence of habitat disturbance on reptiles in a box–ironbark eucalypt forest of south-eastern Australia. Biodiversity and Conservation 10, 161–176.
The influence of habitat disturbance on reptiles in a box–ironbark eucalypt forest of south-eastern Australia.Crossref | GoogleScholarGoogle Scholar |

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

Catling, P. C. (1988). Similarities and contrasts in the diets of foxes, Vulpes vulpes, and cats, Felis catus, relative to fluctuating prey populations and drought. Wildlife Research 15, 307–317.
Similarities and contrasts in the diets of foxes, Vulpes vulpes, and cats, Felis catus, relative to fluctuating prey populations and drought.Crossref | GoogleScholarGoogle Scholar |

Claridge, A. W., Cunningham, R. B., Catling, P. C., and Reid, A. M. (2010). Trends in the activity levels of forest-dwelling vertebrate fauna against a background of intensive baiting for foxes. Forest Ecology and Management 260, 822–832.
Trends in the activity levels of forest-dwelling vertebrate fauna against a background of intensive baiting for foxes.Crossref | GoogleScholarGoogle Scholar |

Cogger, H. (2014). ‘Reptiles and Amphibians of Australia.’ (CSIRO Publishing: Melbourne.)

Creel, S., and Christianson, D. (2008). Relationships between direct predation and risk effects. Trends in Ecology & Evolution 23, 194–201.
Relationships between direct predation and risk effects.Crossref | GoogleScholarGoogle Scholar |

Croll, D. A., Maron, J. L., Estes, J. A., Danner, E. M., and Byrd, G. V. (2005). Introduced predators transform subarctic islands from grassland to tundra. Science 307, 1959–1961.
Introduced predators transform subarctic islands from grassland to tundra.Crossref | GoogleScholarGoogle Scholar | 15790855PubMed |

Cupples, J. B., Crowther, M. S., Story, G., and Letnic, M. (2011). Dietary overlap and prey selectivity among sympatric carnivores: could dingoes suppress foxes through competition for prey? Journal of Mammalogy 92, 590–600.
Dietary overlap and prey selectivity among sympatric carnivores: could dingoes suppress foxes through competition for prey?Crossref | GoogleScholarGoogle Scholar |

Dexter, N., and Murray, A. (2009). The impact of fox control on the relative abundance of forest mammals in East Gippsland, Victoria. Wildlife Research 36, 252–261.
The impact of fox control on the relative abundance of forest mammals in East Gippsland, Victoria.Crossref | GoogleScholarGoogle Scholar |

Dickman, C. R. (1996). Impact of exotic generalist predators on the native fauna of Australia. Wildlife Biology 2, 185–195.
Impact of exotic generalist predators on the native fauna of Australia.Crossref | GoogleScholarGoogle Scholar |

Donadio, E., and Buskirk, S. W. (2006). Diet, morphology and interspecific killing in Carnivora. American Naturalist 167, 524–536.
Diet, morphology and interspecific killing in Carnivora.Crossref | GoogleScholarGoogle Scholar | 16670995PubMed |

Glen, A. S., Fay, A. R., and Dickman, C. R. (2006). Diets of sympatric red foxes Vulpes vulpes and wild dogs Canis lupus in the Northern Rivers Region, New South Wales. Australian Mammalogy 28, 101–104.
Diets of sympatric red foxes Vulpes vulpes and wild dogs Canis lupus in the Northern Rivers Region, New South Wales.Crossref | GoogleScholarGoogle Scholar |

Guarino, F. (2001). Diet of a large carnivorous lizard, Varanus varius. Wildlife Research 28, 627–630.
Diet of a large carnivorous lizard, Varanus varius.Crossref | GoogleScholarGoogle Scholar |

Guarino, F. (2002). Spatial ecology of a large carnivorous lizard, Varanus varius (Squamata: Varanidae). Journal of Zoology 258, 449–457.
Spatial ecology of a large carnivorous lizard, Varanus varius (Squamata: Varanidae).Crossref | GoogleScholarGoogle Scholar |

Heatwole, H., and Taylor, J. A. (1987). ‘Ecology of Reptiles,’ 2nd edn. (Surrey Beatty and Sons: Sydney.)

Hines, J. E. (2014). PRESENCE – Software to estimate patch occupancy and related parameters. U.S. Geological Survey–Patuxent Wildlife Research Center, Laurel, MD. Available at http://www.mbr-pwrc.usgs.gov/software/presence.html [Verified December 2018]

Hu, Y., Urlus, J., Gillespie, G., Letnic, M., and Jessop, T. S. (2013a). Evaluating the role of fire disturbance in structuring small reptile communities in temperate forests. Biodiversity and Conservation 22, 1949–1963.
Evaluating the role of fire disturbance in structuring small reptile communities in temperate forests.Crossref | GoogleScholarGoogle Scholar |

Hu, Y., Magaton, S., Gillespie, G., and Jessop, T. S. (2013b). Small reptile community responses to rotational logging. Biological Conservation 166, 76–83.
Small reptile community responses to rotational logging.Crossref | GoogleScholarGoogle Scholar |

Hu, Y., Kelly, L. T., Gillespie, G. R., and Jessop, T. S. (2016). Lizard responses to forest fire and timber harvesting: complementary insights from species and community approaches. Forest Ecology and Management 379, 206–215.
Lizard responses to forest fire and timber harvesting: complementary insights from species and community approaches.Crossref | GoogleScholarGoogle Scholar |

Jellinek, S., Driscoll, D. A., and Kirkpatrick, J. B. (2004). Environmental and vegetation variables have a greater influence than habitat fragmentation in structuring lizard communities in remnant urban bushland. Austral Ecology 29, 294–304.
Environmental and vegetation variables have a greater influence than habitat fragmentation in structuring lizard communities in remnant urban bushland.Crossref | GoogleScholarGoogle Scholar |

Jessop, T. S., Lockwood, T., Urlus, J., and Gillespie, G. (2010). Preying possum: assessing the diet of V. varius from forest of South Eastern Australia. Biawak 4, 59–66.

Jessop, T. S., Smissen, P., Scheelings, F., and Dempster, T. (2012). Demographic and phenotypic effects of human mediated trophic subsidy on a large Australian lizard (Varanus varius): meal ticket or last supper?. PLoS one 7, e34069.
| 23028983PubMed |

Jessop, T. S., Anson, J. R., Narayan, E., and Lockwood, T. (2015). An introduced competitor elevates corticosterone responses of a native lizard (Varanus varius). Physiological and Biochemical Zoology 88, 237–245.
An introduced competitor elevates corticosterone responses of a native lizard (Varanus varius).Crossref | GoogleScholarGoogle Scholar | 25860823PubMed |

Jessop, T. S., Gillespie, G. R., and Letnic, M. (2016). Examining multi-scale effects of the invasive fox on a large varanid (Varanus varius White, 1790) mesopredator. In ‘Proceedings of the 2015 Interdisciplinary World Conference on Monitor Lizards’, 12 July 2015, Bangkok, Thailand. (Ed. M. Cota), pp. 221–236. (Institute for Research and Development, Suan Sunandha Rajabhat University: Bangkok.)

Kéry, M., and Schmidt, B. (2008). Imperfect detection and its consequences for monitoring for conservation. Community Ecology 9, 207–216.
Imperfect detection and its consequences for monitoring for conservation.Crossref | GoogleScholarGoogle Scholar |

Kinnear, J. E., Sumner, N. R., and Onus, M. L. (2002). The red fox in Australia—an exotic predator turned biocontrol agent. Biological Conservation 108, 335–359.
The red fox in Australia—an exotic predator turned biocontrol agent.Crossref | GoogleScholarGoogle Scholar |

Laurie, W. A., and Brown, D. (1990). Population biology of marine iguanas (Amblyrhynchus cristatus). III. Factors affecting survival. Journal of Animal Ecology 59, 545–568.
Population biology of marine iguanas (Amblyrhynchus cristatus). III. Factors affecting survival.Crossref | GoogleScholarGoogle Scholar |

Letnic, M., Koch, F., Gordon, C., Crowther, M. S., and Dickman, C. R. (2009). Keystone effects of an alien top predator stem extinctions of native mammals. Proceedings of the Royal Society of London. Series B, Biological Sciences 276, 3249–3256.
Keystone effects of an alien top predator stem extinctions of native mammals.Crossref | GoogleScholarGoogle Scholar |

Letnic, M., Ritchie, E. G., and Dickman, C. R. (2012). Top predators as biodiversity regulators: the dingo Canis lupus dingo as a case study. Biological Reviews of the Cambridge Philosophical Society 87, 390–413.
Top predators as biodiversity regulators: the dingo Canis lupus dingo as a case study.Crossref | GoogleScholarGoogle Scholar | 22051057PubMed |

Levin, S. A. (1974). Dispersion and population interactions. American Naturalist 108, 207–228.
Dispersion and population interactions.Crossref | GoogleScholarGoogle Scholar |

Lunney, D., Triggs, B., Eby, P., and Ashby, A. (1990). Analysis of scats of dogs Canis-familiaris and foxes Vulpes vulpes (Canidae, Carnivora) in coastal forests near Bega, New-South-Wales. Australian Wildlife Research 17, 61–68.
Analysis of scats of dogs Canis-familiaris and foxes Vulpes vulpes (Canidae, Carnivora) in coastal forests near Bega, New-South-Wales.Crossref | GoogleScholarGoogle Scholar |

Mahon, P. S. (2009). Targeted control of widespread exotic species for biodiversity conservation: the red fox (Vulpes vulpes) in New South Wales, Australia. Ecological Management & Restoration 10, S59–S69.
Targeted control of widespread exotic species for biodiversity conservation: the red fox (Vulpes vulpes) in New South Wales, Australia.Crossref | GoogleScholarGoogle Scholar |

May, S. A., and Norton, T. W. (1996). Influence of fragmentation and disturbance on the potential impact of feral predators on native fauna in Australian forest ecosystems. Wildlife Research 23, 387–400.
Influence of fragmentation and disturbance on the potential impact of feral predators on native fauna in Australian forest ecosystems.Crossref | GoogleScholarGoogle Scholar |

McIlroy, J., King, D. R., and Oliver, A. J. (1985). The sensitivity to Australian animals to 1080 poison VIII. Amphibians and reptiles. Australian Wildlife Research 12, 113–118.
The sensitivity to Australian animals to 1080 poison VIII. Amphibians and reptiles.Crossref | GoogleScholarGoogle Scholar |

Melis, C., Jędrzejewska, B., Apollonio, M., Bartoń, K. A., Jędrzejewski, W., Linnell, J. D., Kojola, I., Kusak, J., Adamic, M., Ciuti, S., and Delehan, I. (2009). Predation has a greater impact in less productive environments: variation in roe deer, Capreolus capreolus, population density across Europe. Global Ecology and Biogeography 18, 724–734.
Predation has a greater impact in less productive environments: variation in roe deer, Capreolus capreolus, population density across Europe.Crossref | GoogleScholarGoogle Scholar |

Mitchell, B. D, and Banks, P. B. (2005). Do wild dogs exclude foxes? Evidence for competition from dietary and spatial overlaps. Austral Ecology 30, 581–591.
Do wild dogs exclude foxes? Evidence for competition from dietary and spatial overlaps.Crossref | GoogleScholarGoogle Scholar |

Molsher, R. L., Gifford, E. J., and McIlroy, J. C. (2000). Temporal, spatial and individual variation in the diet of red foxes (Vulpes vulpes) in central New South Wales. Wildlife Research 27, 593–601.
Temporal, spatial and individual variation in the diet of red foxes (Vulpes vulpes) in central New South Wales.Crossref | GoogleScholarGoogle Scholar |

Moseby, K. E., Hill, B. M., and Read, J. L. (2009). Arid recovery–a comparison of reptile and small mammal populations inside and outside a large rabbit, cat and fox‐proof exclosure in arid South Australia. Austral Ecology 34, 156–169.
Arid recovery–a comparison of reptile and small mammal populations inside and outside a large rabbit, cat and fox‐proof exclosure in arid South Australia.Crossref | GoogleScholarGoogle Scholar |

Murray, A. J., Poore, R. N., and Dexter, N. (2006). Project Deliverance: the response of ‘critical weight range’ mammals to effective fox control in mesic forest habitats in far East Gippsland, Victoria. Department of Sustainability and Environment, Melbourne.

Olsson, M., Wapstra, E., Swan, G., Snaith, E., Clarke, R., and Madsen, T. (2005). Effects of long-term fox baiting on species composition and abundance in an Australian lizard community. Austral Ecology 30, 899–905.
Effects of long-term fox baiting on species composition and abundance in an Australian lizard community.Crossref | GoogleScholarGoogle Scholar |

Paltridge, R. (2002). The diets of cats, foxes and dingoes in relation to prey availability in the Tanami Desert, Northern Territory. Wildlife Research 29, 389–403.
The diets of cats, foxes and dingoes in relation to prey availability in the Tanami Desert, Northern Territory.Crossref | GoogleScholarGoogle Scholar |

Paltridge, R. M. (2005). Predator–prey interactions in the spinifex grasslands of central Australia. Ph.D dissertation, School of Biological Sciences, University of Wollongong, Wollongong, NSW.

Pianka, E. R. (1969). Habitat specificity, speciation, and species density in Australian desert lizards. Ecology 50, 498–502.
Habitat specificity, speciation, and species density in Australian desert lizards.Crossref | GoogleScholarGoogle Scholar |

Ramsey, D. S., Barclay, C., Campbell, C. D., Dewar, E., MacDonald, A. J., Modave, E., Quasim, S., and Sarre, S. D. (2018). Detecting rare carnivores using scats: Implications for monitoring a fox incursion into Tasmania. Ecology and Evolution 8, 732–743.
Detecting rare carnivores using scats: Implications for monitoring a fox incursion into Tasmania.Crossref | GoogleScholarGoogle Scholar | 29321909PubMed |

Rayner, M. J., Hauber, M. E., Imber, M. J., Stamp, R. K., and Clout, M. N. (2007). Spatial heterogeneity of mesopredator release within an ocean island system. Proceedings of the National Academy of Sciences of the United States of America 104, 20862–20865.
Spatial heterogeneity of mesopredator release within an ocean island system.Crossref | GoogleScholarGoogle Scholar | 18083843PubMed |

Read, J., and Bowen, Z. (2001). Population dynamics, diet and aspects of the biology of feral cats and foxes in arid South Australia. Wildlife Research 28, 195–203.
Population dynamics, diet and aspects of the biology of feral cats and foxes in arid South Australia.Crossref | GoogleScholarGoogle Scholar |

Read, J. L., and Scoleri, V. (2015). Ecological implications of reptile mesopredator release in arid South Australia. Journal of Herpetology 49, 64–69.
Ecological implications of reptile mesopredator release in arid South Australia.Crossref | GoogleScholarGoogle Scholar |

Reddiex, B., Forsyth, D. M., McDonald-Madden, E., Einoder, L. D., Griffioen, P. A., Chick, R. R., and Robley, A. J. (2006). Control of pest mammals for biodiversity protection in Australia. I. Patterns of control and monitoring. Wildlife Research 33, 691–709.
Control of pest mammals for biodiversity protection in Australia. I. Patterns of control and monitoring.Crossref | GoogleScholarGoogle Scholar |

Risbey, D. A., Calver, M. C., Short, J., Bradley, J. S., and Wright, I. W. (2000). The impact of cats and foxes on the small vertebrate fauna of Heirisson Prong, Western Australia. II. A field experiment. Wildlife Research 27, 223–235.
The impact of cats and foxes on the small vertebrate fauna of Heirisson Prong, Western Australia. II. A field experiment.Crossref | GoogleScholarGoogle Scholar |

Ritchie, E. G., and Johnson, C. N. (2009). Predator interactions, mesopredator release and biodiversity conservation. Ecology Letters 12, 982–998.
Predator interactions, mesopredator release and biodiversity conservation.Crossref | GoogleScholarGoogle Scholar | 19614756PubMed |

Roberts, S. L., van Wagtendonk, J. W., Miles, A. K., and Kelt, D. A. (2011). Effects of fire on spotted owl site occupancy in a late-successional forest. Biological Conservation 144, 610–619.
Effects of fire on spotted owl site occupancy in a late-successional forest.Crossref | GoogleScholarGoogle Scholar |

Royle, J. A. (2004). N‐mixture models for estimating population size from spatially replicated counts. Biometrics 60, 108–115.
N‐mixture models for estimating population size from spatially replicated counts.Crossref | GoogleScholarGoogle Scholar | 15032780PubMed |

Royle, J. A., and Nichols, J. D. (2003). Estimating abundance from repeated presence–absence data or point counts. Ecology 84, 777–790.
Estimating abundance from repeated presence–absence data or point counts.Crossref | GoogleScholarGoogle Scholar |

Salo, P., Korpimäki, E., Banks, P. B., Nordström, M., and Dickman, C. R. (2007). Alien predators are more dangerous than native predators to prey populations. Proceedings of the Royal Society of London. Series B, Biological Sciences 274, 1237–1243.
Alien predators are more dangerous than native predators to prey populations.Crossref | GoogleScholarGoogle Scholar |

Saunders, G. R., Gentle, M. N., and Dickman, C. R. (2010). The impacts and management of foxes Vulpes vulpes in Australia. Mammal Review 40, 181–211.
The impacts and management of foxes Vulpes vulpes in Australia.Crossref | GoogleScholarGoogle Scholar |

Shine, R., and Madsen, T. (1997). Prey abundance and predator reproduction: rats and pythons on a tropical Australian floodplain. Ecology 78, 1078–1086.

Sutherland, D. R., Glen, A. S., and de Tores, P. J. (2011). Could controlling mammalian carnivores lead to mesopredator release of carnivorous reptiles? Proceedings. Biological Sciences 278, 641–648.
Could controlling mammalian carnivores lead to mesopredator release of carnivorous reptiles?Crossref | GoogleScholarGoogle Scholar | 21123272PubMed |

Thompson, M. B. (1983). Populations of the Murray River tortoise, Emydura (Chelodina): the effect of egg predation by the red fox, Vulpes vulpes. Australian Wildlife Research 10, 363–372.
Populations of the Murray River tortoise, Emydura (Chelodina): the effect of egg predation by the red fox, Vulpes vulpes.Crossref | GoogleScholarGoogle Scholar |

Triggs, B. H., Brunner, H., and Cullen, J. M. (1984). The food of the fox, dog and cat in Croajingalong National Park, southeastern Victoria. Australian Wildlife Research 11, 491–499.
The food of the fox, dog and cat in Croajingalong National Park, southeastern Victoria.Crossref | GoogleScholarGoogle Scholar |

Twigg, L. E., and King, D. R. (1991). The impact of fluoroacetate-bearing vegetation on native Australian fauna: a review. Oikos 61, 412–430.
The impact of fluoroacetate-bearing vegetation on native Australian fauna: a review.Crossref | GoogleScholarGoogle Scholar |

Urlus, J. (2009). The influence of vegetation structure and land management on East Gippsland reptile communities. Honours Thesis, Deakin University, Victoria.

Weavers, B. (1989). Diet of the lace monitor lizard (Varanus vadus) in south-eastern Australia. Australian Zoologist 25, 83–85.
Diet of the lace monitor lizard (Varanus vadus) in south-eastern Australia.Crossref | GoogleScholarGoogle Scholar |

Wilson, G. J., and Delahay, R. J. (2001). A review of methods to estimate the abundance of terrestrial carnivores using field signs and observation. Wildlife Research 28, 151–164.
A review of methods to estimate the abundance of terrestrial carnivores using field signs and observation.Crossref | GoogleScholarGoogle Scholar |

Wilson, S., and Swan, G. (2008). ‘A Complete Guide to Reptiles of Australia,’ 2nd edn. (New Holland Publishers: Sydney.)