How to catch red foxes red handed: identifying predation of freshwater turtles and nests
Stuart J. Dawson A C , Heather M. Crawford A , Robert M. Huston B , Peter J. Adams A and Patricia A. Fleming A
+ Author Affiliations
- Author Affiliations
A Veterinary and Life Sciences, Murdoch University, Murdoch, WA 6150, Australia.
B Department of Parks and Wildlife, Perth Hills District, Nature Conservation Program, 275 Allen Road, Mundaring, WA 6073, Australia.
C Corresponding author. Email: s.dawson@murdoch.edu.au
Wildlife Research 43(8) 615-622 https://doi.org/10.1071/WR16066
Submitted: 5 April 2016 Accepted: 25 October 2016 Published: 12 December 2016
Abstract
Context: Predation is one of the key contributors to mortality in freshwater turtles. Confirming the identity of predators is an important step towards conservation management action. Throughout Australia, the red fox (Vulpes vulpes) is suspected to apply significant and unsustainable predation pressure to turtle populations, killing adults and depredating nests; however methods for confirming this are limited.
Aims: The present study used a range of methods to confirm predation of oblong turtle (Chelodina colliei) nests and adults by the introduced red fox.
Methods: First, depredated adult carapaces, and turtle egg-shell fragments from excavated nests were swabbed and analysed for trace DNA. Second, we used artificial turtle nests, monitored by camera traps, to analyse seasonal changes in the behaviour of foxes around sites where turtle nests are present, including over the nesting season. Last, we used scat analysis to identify the prevalence of turtle remains in fox diet.
Key results: Predominantly fox DNA was recovered from both adult carapaces and depredated eggs. In addition, camera traps recorded only foxes depredating artificial nests. Despite this evidence that foxes kill adults and excavated nests, we found that turtle remains were only a small part of the diet of foxes at this study site (hatchling or turtle egg shell were present in only 4% of 230 scats sampled). The diet of these foxes was largely anthropogenic-sourced foods, such as fruit (e.g. figs, grapes, melons; 81% of scats), sheep carrion (41%) and rodents (36%).
Conclusions: We conclude that DNA analysis, camera trapping and scat analysis are effective methods of identifying foxes as predators of adult turtle, and their nests. Furthermore, we found that anthropogenic foods (orchard crops, livestock or synanthropic species) may subsidise greater fox population size than might occur in their absence, thereby increasing potential pressure on these freshwater turtles.
Implications: Our findings give credence to the argument that foxes are effective predators of turtle adults and nests. In addition, the high proportion of anthropogenic food sources in the diet of foxes, and potential subsidisation, is an important consideration for land managers.
Additional keywords: anthropogenic impacts, diet, invasive species, pest ecology, urban ecology, faeces.
References
Berry, O., and Sarre, S. D. (2007). Gel-free species identification using melt-curve analysis. Molecular Ecology Notes 7, 1–4.| Gel-free species identification using melt-curve analysis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXis1Sjtb8%3D&md5=751ece1cc0b2b6bd9f6722b9f517f2c5CAS |
Brown, L., and Macdonald, D. (1995). Predation on green turtle Chelonia mydas nests by wild canids at Akyatan Beach, Turkey. Biological Conservation 71, 55–60.
| Predation on green turtle Chelonia mydas nests by wild canids at Akyatan Beach, Turkey.Crossref | GoogleScholarGoogle Scholar |
Brunner, H. and Triggs, B. (2002). ‘Hair ID: an Interactive Tool for Identifying Australian Mammal Hair.’ (CSIRO Publishing: Melbourne.)
Brunner, H., Lloyd, J., and Coman, B. (1975). Fox scat analysis in a forest park in south-eastern Australia. Wildlife Research 2, 147–154.
| Fox scat analysis in a forest park in south-eastern Australia.Crossref | GoogleScholarGoogle Scholar |
Buhlmann, K. A., Akre, T. S. B., Iverson, J. B., Karapatakis, D., Mittermeier, R. A., Georges, A., Rhodin, A. G. J., van Dijk, P. P., and Gibbons, J. W. (2009). A global analysis of tortoise and freshwater turtle distributions with identification of priority conservation areas. Chelonian Conservation and Biology 8, 116–149.
| A global analysis of tortoise and freshwater turtle distributions with identification of priority conservation areas.Crossref | GoogleScholarGoogle Scholar |
Burger, J. (1977). Determinants of hatching success in diamondback terrapin, Malaclemys terrapin. American Midland Naturalist 97, 444–464.
| Determinants of hatching success in diamondback terrapin, Malaclemys terrapin.Crossref | GoogleScholarGoogle Scholar |
Burger, J., and Gochfeld, M. (2014). Avian predation on olive ridley (Lepidochelys olivacea) sea turtle eggs and hatchlings: avian opportunities, turtle avoidance, and human protection. Copeia 2014, 109–122.
| Avian predation on olive ridley (Lepidochelys olivacea) sea turtle eggs and hatchlings: avian opportunities, turtle avoidance, and human protection.Crossref | GoogleScholarGoogle Scholar |
Burke, V. J., Rathbun, S. L., Bodie, J. R., and Gibbons, J. W. (1998). Effect of density on predation rate for turtle nests in complex landscapes. Oikos 83, 3–11.
| Effect of density on predation rate for turtle nests in complex landscapes.Crossref | GoogleScholarGoogle Scholar |
Burke, R. L., Schneider, C. M., and Dolinger, M. T. (2005). Cues used by raccoons to find turtle nests: effects of flags, human scent, and diamond-backed terrapin sign. Journal of Herpetology 39, 312–315.
| Cues used by raccoons to find turtle nests: effects of flags, human scent, and diamond-backed terrapin sign.Crossref | GoogleScholarGoogle Scholar |
Catling, P. (1988). Similarities and contrasts in the diets of foxes, Vulpes vulpes, and cats, Felis catus, relative to fluctuating prey populations and drought. Australian 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 |
Christens, E., and Bider, J. R. (1987). Nesting activity and hatching success of the painted turtle (Chrysemys picta marginata) in southwestern Quebec. Herpetologica 43, 55–65.
Christiansen, J., and Gallaway, B. (1984). Raccoon removal, nesting success, and hatchling emergence in Iowa turtles with special reference to Kinosternon flavescens (Kinosternidae). The Southwestern Naturalist 29, 343–348.
| Raccoon removal, nesting success, and hatchling emergence in Iowa turtles with special reference to Kinosternon flavescens (Kinosternidae).Crossref | GoogleScholarGoogle Scholar |
Clay, B. T. (1981). Observations on the breeding biology and behaviour of the long-necked tortoise, Chelodina oblonga. Journal of the Royal Society of Western Australia 4, 27–32.
Coman, B. (1973). The diet of red foxes, Vulpes vulpes L., in Victoria. Australian Journal of Zoology 21, 391–401.
| The diet of red foxes, Vulpes vulpes L., in Victoria.Crossref | GoogleScholarGoogle Scholar |
Congdon, J. D., Tinkle, D. W., Breitenbach, G. L., and Sels, R. C. L. (1983). Nesting ecology and hatching success in the turtle Emydoidea blandingi. Herpetologica 39, 417–429.
Congdon, J. D., Breitenbach, G. L., Sels, R. C. L., and Tinkle, D. W. (1987). Reproduction and nesting ecology of snapping turtles (Chelydra serpentina) in Southeastern Michigan. Herpetologica 43, 39–54.
Crawford, H. (2010). A comparison of red fox (Vulpes vulpes) and feral cat (Felis catus) diets in the south west region of Western Australia. Ph.D. Thesis, Murdoch University, Perth.
Dawson, S. J., Adams, P. J., Huston, R., and Fleming, P. A. (2014). Environmental factors influence nest excavation by foxes. Journal of Zoology 294, 104–113.
| Environmental factors influence nest excavation by foxes.Crossref | GoogleScholarGoogle Scholar |
De Barba, M., Miquel, C., Boyer, F., Mercier, C., Rioux, D., Coissac, E., and Taberlet, P. (2014). DNA metabarcoding multiplexing and validation of data accuracy for diet assessment: application to omnivorous diet. Molecular Ecology Resources 14, 306–323.
| DNA metabarcoding multiplexing and validation of data accuracy for diet assessment: application to omnivorous diet.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXjt1Sksbg%3D&md5=127727acc6d8fc7965023fc13bf9bf07CAS |
Doody, J. S., Green, B., Sims, R., Rhind, D., West, P., and Steer, D. (2006). Indirect impacts of invasive cane toads (Bufo marinus) on nest predation in pig-nosed turtles (Carettochelys insculpta). Wildlife Research 33, 349–354.
| Indirect impacts of invasive cane toads (Bufo marinus) on nest predation in pig-nosed turtles (Carettochelys insculpta).Crossref | GoogleScholarGoogle Scholar |
Escalona, T., and Fa, J. E. (1998). Survival of nests of the terecay turtle (Podocnemis unifilis) in the Nichare–Tawadu rivers, Venezuela. Journal of Zoology 244, 303–312.
| Survival of nests of the terecay turtle (Podocnemis unifilis) in the Nichare–Tawadu rivers, Venezuela.Crossref | GoogleScholarGoogle Scholar |
Feinberg, J. A., and Burke, R. L. (2003). Nesting ecology and predation of diamondback terrapins, Malaclemys terrapin, in Gateway National Recreation Area, New York. Journal of Herpetology 37, 517–526.
| Nesting ecology and predation of diamondback terrapins, Malaclemys terrapin, in Gateway National Recreation Area, New York.Crossref | GoogleScholarGoogle Scholar |
Fowler, L. E. (1979). Hatching success and nest predation in the green sea turtle, Chelonia mydas, at Tortuguero, Costa Rica. Ecology 60, 946–955.
| Hatching success and nest predation in the green sea turtle, Chelonia mydas, at Tortuguero, Costa Rica.Crossref | GoogleScholarGoogle Scholar |
Giles, J., Kuchling, G., and Davis, J. A. (2008). Populations of the snake-necked turtle Chelodina oblonga in three suburban lakes of Perth, Western Australia. In ‘Urban Herpetoplogy’. (Eds J. C. Mitchell, R. E. Jung and B. Bartholomew.) pp. 275–283. (Society for the Study of Amphibians and Reptiles: Salt Lake City, UT.)
Hamilton, A. M., Freedman, A. H., and Franz, R. (2002). Effects of deer feeders, habitat, and sensory cues on predation rate on artificial turtle nests. American Midland Naturalist 147, 123–134.
| Effects of deer feeders, habitat, and sensory cues on predation rate on artificial turtle nests.Crossref | GoogleScholarGoogle Scholar |
Johnson, C. (2006). ‘Australia’s Mammal Extinction.’ (Cambridge University Press: Melbourne.)
King, R. A., Read, D. S., Traugott, M., and Symondson, W. O. C. (2008). Invited review: molecular analysis of predation: a review of best practice for DNA-based approaches. Molecular Ecology 17, 947–963.
| Invited review: molecular analysis of predation: a review of best practice for DNA-based approaches.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXktVajurw%3D&md5=d362072afa1bb341eaa2415287d497eeCAS |
Leighton, P. A., Horrocks, J. A., and Kramer, D. L. (2011). Predicting nest survival in sea turtles: when and where are eggs most vulnerable to predation? Animal Conservation 14, 186–195.
| Predicting nest survival in sea turtles: when and where are eggs most vulnerable to predation?Crossref | GoogleScholarGoogle Scholar |
Macdonald, D. W. (1976). Food caching by red foxes and some other carnivores. Zeitschrift für Tierpsychologie 42, 170–185.
| Food caching by red foxes and some other carnivores.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaE2s%2Fotl2ntg%3D%3D&md5=566bfa0a18acd90e4506d119b72e0200CAS |
Marchand, M. N., and Litvaitis, J. A. (2004). Effects of landscape composition, habitat features, and nest distribution on predation rates of simulated turtle nests. Biological Conservation 117, 243–251.
| Effects of landscape composition, habitat features, and nest distribution on predation rates of simulated turtle nests.Crossref | GoogleScholarGoogle Scholar |
Marchand, M. N., Litvaitis, J. A., Maier, T. J., and DeGraaf, R. M. (2002). Use of artificial nests to investigate predation on freshwater turtle nests. Wildlife Society Bulletin 30, 1092–1098.
McCutcheon, R. H. J. (1985). Observation on the breeding of the oblong turtle (Chelodina oblonga). Western Australian Naturalist (Perth) 16, 40.
Oskam, C. L., Haile, J., McLay, E., Rigby, P., Allentoft, M. E., Olsen, M. E., Bengtsson, C., Miller, G. H., Schwenninger, J.-L., and Jacomb, C. (2010). Fossil avian eggshell preserves ancient DNA. Proceedings of the Royal Society of London. Series B. Biological Sciences 277, 1991–2000.
| Fossil avian eggshell preserves ancient DNA.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXpvFaisrs%3D&md5=e359e9374fbcf9dccb8bf84051190429CAS |
Pedler, R. D., Brandle, R., Read, J. L., Southgate, R., Bird, P., and Moseby, K. E. (2016). Rabbit biocontrol and landscape‐scale recovery of threatened desert mammals. Conservation Biology 30, 774–782.
| Rabbit biocontrol and landscape‐scale recovery of threatened desert mammals.Crossref | GoogleScholarGoogle Scholar |
Scott, T. G. (1943). Some food coactions of the northern plains red fox. Ecological Monographs 13, 427–479.
| Some food coactions of the northern plains red fox.Crossref | GoogleScholarGoogle Scholar |
Short, J., Calver, M. C., and Risbey, D. A. (1999). The impact of cats and foxes on the small vertebrate fauna of Heirisson Prong, Western Australia. I. Exploring potential impact using diet analysis. Wildlife Research 26, 621–630.
| The impact of cats and foxes on the small vertebrate fauna of Heirisson Prong, Western Australia. I. Exploring potential impact using diet analysis.Crossref | GoogleScholarGoogle Scholar |
Spencer, R.-J. (2002). Experimentally testing nest site selection: fitness trade-offs and predation risk in turtle. Ecology 83, 2136–2144.
| Experimentally testing nest site selection: fitness trade-offs and predation risk in turtle.Crossref | GoogleScholarGoogle Scholar |
Spencer, R.-J., and Thompson, M. B. (2003). The significance of predation in nest site selection of turtles: an experimental consideration of macro- and microhabitat preferences. Oikos 102, 592–600.
| The significance of predation in nest site selection of turtles: an experimental consideration of macro- and microhabitat preferences.Crossref | GoogleScholarGoogle Scholar |
Spencer, R.-J., and Thompson, M. B. (2005). Experimental analysis of the impact of foxes on freshwater turtle populations. Conservation Biology 19, 845–854.
| Experimental analysis of the impact of foxes on freshwater turtle populations.Crossref | GoogleScholarGoogle Scholar |
StatSoft Inc (2007). ‘STATISTICA (data analysis software system), version 8.0.’ (StatSoft, Inc.: Tulsa OK.)
Stickney, A. (1991). Seasonal patterns of prey availability and the foraging behavior of arctic foxes (Alopex lagopus) in a waterfowl nesting area. Canadian Journal of Zoology 69, 2853–2859.
| Seasonal patterns of prey availability and the foraging behavior of arctic foxes (Alopex lagopus) in a waterfowl nesting area.Crossref | GoogleScholarGoogle Scholar |
Thompson, M. (1983). Populations of the Murray River tortoise, Emydura (Chelodina): the effect of egg predation by the red fox, Vulpes vulpes. Wildlife Research 10, 363–371.
| Populations of the Murray River tortoise, Emydura (Chelodina): the effect of egg predation by the red fox, Vulpes vulpes.Crossref | GoogleScholarGoogle Scholar |
Triggs, B. (2004). ‘Tracks, Scats, and Other Traces.’ (Oxford University Press, Melbourne, Australia.)
Trocini, S. (2013). Health assessment and hatching success of two Western Australian loggerhead turtle (Caretta caretta) populations. PhD thesis, Murdoch University, Perth.
Veríssimo, D., Jones, D., Chaverri, R., and Meyer, S. (2012). Jaguar Panthera onca predation of marine turtles: conflict between flagship species in Tortuguero, Costa Rica. Oryx 46, 340–347.
| Jaguar Panthera onca predation of marine turtles: conflict between flagship species in Tortuguero, Costa Rica.Crossref | GoogleScholarGoogle Scholar |
White, J. G., Gubiani, R., Smallman, N., Snell, K., and Morton, A. (2006). Home range, habitat selection and diet of foxes (Vulpes vulpes) in a semi-urban riparian environment. Wildlife Research 33, 175–180.
| Home range, habitat selection and diet of foxes (Vulpes vulpes) in a semi-urban riparian environment.Crossref | GoogleScholarGoogle Scholar |
Whytlaw, P. A., Edwards, W., and Congdon, B. C. (2013). Marine turtle nest depredation by feral pigs (Sus scrofa) on the western Cape York Peninsula, Australia: implications for management. Wildlife Research 40, 377–384.
Wilhoft, D. C., Del Baglivo, M. G., and Del Baglivo, M. D. (1979). Observations on mammalian predation of snapping turtle nests (Reptilia, Testudines, Chelydridae). Journal of Herpetology 13, 435–438.
| Observations on mammalian predation of snapping turtle nests (Reptilia, Testudines, Chelydridae).Crossref | GoogleScholarGoogle Scholar |
Williams, C. L., Blejwas, K., Johnston, J. J., and Jaeger, M. M. (2003). A coyote in sheep’s clothing: predator identification from saliva. Wildlife Society Bulletin 31, 926–932.
Wilson, G. R., Brittingham, M. C., and Goodrich, L. J. (1998). How well do artificial nests estimate success of real nests. The Condor 100, 357–364.
| How well do artificial nests estimate success of real nests.Crossref | GoogleScholarGoogle Scholar |
Yerli, S., Canbolat, A., Brown, L., and Macdonald, D. (1997). Mesh grids protect loggerhead turtle Caretta caretta nests from red fox Vulpes vulpes predation. Biological Conservation 82, 109–111.
| Mesh grids protect loggerhead turtle Caretta caretta nests from red fox Vulpes vulpes predation.Crossref | GoogleScholarGoogle Scholar |
