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

Comparison of methods to detect rare and cryptic species: a case study using the red fox (Vulpes vulpes)

S. J. Vine A B , M. S. Crowther A C H , S. J. Lapidge D , C. R. Dickman A , N. Mooney E , M. P. Piggott F and A. W. English G
+ Author Affiliations
- Author Affiliations

A Institute of Wildlife Research, School of Biological Sciences, University of Sydney, NSW 2006, Australia.

B Present address: World Wildlife Fund-Australia, Level 13, 235 Jones Street, Ultimo, NSW 2007, Australia.

C Department of Environment and Climate Change (NSW), PO Box 1967, Hurstville, NSW 2220, Australia.

D Invasive Animals Cooperative Research Centre, 48 Oxford Terrace, Unley, SA 5601, Australia.

E Wildlife Management Branch and Fox Eradication Branch, Department of Primary Industries and Water, GPO Box 44, Hobart, Tas. 7001, Australia.

F Australian Centre for Biodiversity, School of Biological Sciences, Monash University, Clayton, Vic. 3800, Australia. Present address: The Fenner School of Environment and Society, Australian National University, Canberra, ACT 0200, Australia.

G Faculty of Veterinary Science, University of Sydney, Werombi Road, Camden, NSW 2570, Australia.

H Corresponding author. Email: m.crowther@usyd.edu.au

Wildlife Research 36(5) 436-446 https://doi.org/10.1071/WR08069
Submitted: 12 May 2008  Accepted: 4 May 2009   Published: 21 July 2009

Abstract

Choosing the appropriate method to detect and monitor wildlife species is difficult if the species is rare or cryptic in appearance or behaviour. We evaluated the effectiveness of the following four methods for detecting red foxes (Vulpes vulpes) on the basis of equivalent person hours in a rural landscape in temperate Australia: camera traps, hair traps (using morphology and DNA from hair follicles), scats from bait stations (using DNA derived from the scats) and spotlighting. We also evaluated whether individual foxes could be identified using remote collection of their tissues. Genetic analysis of hair samples was the least efficient method of detection among the methods employed because of the paucity of samples obtained and the lack of follicles on sampled hairs. Scat detection was somewhat more efficient. Scats were deposited at 17% of bait stations and 80% of scats were amplified with a fox-specific marker, although only 31% of confirmed fox scats could be fully genotyped at all six microsatellite loci. Camera trapping and spotlighting were the most efficient methods of detecting fox presence in the landscape. Spotlighting success varied seasonally, with fox detections peaking in autumn (80% of spotlighting transects) and being lowest in winter (29% of transects). Cameras detected foxes at 51% of stations; however, there was limited seasonality in detection, and success rates varied with camera design. Log-linear models confirmed these trends. Our results showed that the appropriate technique for detecting foxes varies depending on the time of the year. It is suggested that wildlife managers should consider both seasonal effects and species biology when attempting to detect rare or elusive species.


Acknowledgements

We thank the many volunteers who helped on the project, especially Jean Vine, Tom Newsome, James Hunter, Terry Hogan, and Steve Burgun, Brian Farrell and staff at Arthursleigh for assistance in the field. Special thanks go to Paul Meek, Bill Morris, Glen Saunders, Roger Pech and Eddy Gifford for their help, and Cici Legoe for veterinary supervision. Andrea Taylor and Chris Emms also provided invaluable input into the project. The Pest Animal Control and Invasive Animal CRCs, Australian Wool Innovation (through the OutFox II program) and the Tasmanian Fox Free Taskforce provided financial and logistical support, while the University of Sydney’s Animal Ethics Committee provided ethical approval (no. L04/6-2003/1/3370).


References

Agresti A. (1996). ‘An Introduction to Categorical Data Analysis.’ (Wiley: New York.)

Akaike, H. (1974). A new look at the statistical model identification. IEEE Transactions on Automatic Control 19, 716–723.
CrossRef |

Allen, L. , Engeman, R. , and Krupa, H. (1996). Evaluation of three relative abundance indices for assessing dingo populations. Wildlife Research 23, 197–206.
CrossRef |

Banks, S. C. , Hoyle, S. D. , Horsup, A. , Sunnucks, P. , and Taylor, A. C. (2003). Demographic monitoring of an entire species (the northern hairy-nosed wombat, Lasiorhinus krefftii) by genetic analysis of non-invasively collected material. Animal Conservation 6, 101–107.
CrossRef |

Berry, O. , Sarre, S. D. , Farrington, L. , and Aitken, N. (2007). Faecal DNA detection of invasive species: the case of feral foxes in Tasmania. Wildlife Research 34, 1–7.
CrossRef |

Boonstra, R. , Kanter, M. , and Krebs, C. J. (1992). A tracking technique to locate small mammals at low densities. Journal of Mammalogy 73, 683–685.
CrossRef |

Brunner H. , and Triggs B. (2002). Hair ID: An Interactive Tool for Identifying Australian Mammalian Hair.’ (CSIRO Publishing: Melbourne.)

Buckland, S. T. , Goudie, I. B. J. , and Borchers, D. L. (2000). Wildlife population assessment: past developments and future directions. Biometrics 56, 1–12.
CrossRef | CAS | PubMed |

Buckland, S. T. , Magurran, A. E. , Green, R. E. , and Fewster, R. M. (2005). Monitoring change in biodiversity through composite indices. Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences 360, 243–254.
CrossRef | CAS | PubMed |

Bullard, R. W. , Leiker, T. J. , Peterson, J. E. , and Kilburn, S. R. (1978a). Volatile components of fermented egg, an animal attractant and repellent. Journal of Agricultural and Food Chemistry 26, 155–159.
CrossRef | CAS |

Bullard, R. W. , Shumake, S. A. , Campbell, D. A. , and Turkowski, F. J. (1978b). Preparation and evaluation of a synthetic fermented egg coyote attractant and deer repellent. Journal of Agricultural and Food Chemistry 26, 160–163.
CrossRef | CAS |

Bureau of Meteorology (2005). Monthly climate statistics for Goulburn TAFE site. Available at http://www.bom.gov.au/climate/averages/tables/cw_070263.shtml [Accessed May 2005]

Burnham, K. P. , and Anderson, D. R. (2001). Kullback–Leibler information as a basis for strong inference in ecological studies. Wildlife Research 28, 111–119.
CrossRef |

Burnham K. P. , and Anderson D. R. (2002). ‘Model Selection and Multimodel Inference: A Practical Information–Theoretic Approach.’ 2nd edn. (Springer: New York.)

Catling, P. C. , Burt, R. J. , and Kooyman, R. (1997). A comparison of techniques used in a survey of the ground-dwelling and arboreal mammals in forests in north-eastern New South Wales. Wildlife Research 24, 417–432.
CrossRef |

Caughley G. (1977). ‘Analysis of Vertebrate Populations.’ (John Wiley: London.)

Cavallini, P. (1994). Faeces counts as an index of fox abundance. Acta Theriologica 39, 417–424.


Coman, B. J. (1988). The age structure of a sample of foxes (Vulpes vulpes) taken by hunters in Victoria. Australian Wildlife Research 15, 223–229.
CrossRef |

Cutler, T. L. , and Swann, D. E. (1999). Using remote photography in wildlife ecology: a review. Wildlife Society Bulletin 27, 571–581.


Dallaire, A. , and Ruckebusch, Y. (1974). Rest-activity cycle and sleep patterns in captive foxes (Vulpes vulpes). Cellular and Molecular Life Sciences 30, 59–60.
CrossRef |

Davison, A. , Birks, J. D. S. , Brookes, R. C. , Braithwaite, T. C. , and Messenger, J. E. (2002). On the origin of faeces: morphological versus molecular methods for surveying rare carnivores from their scats. Journal of Zoology 257, 141–143.
CrossRef |

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


Dickman, C. R. , Predavec, M. , and Lynam, A. J. (1991). Differential predation of size and sex classes of mice by the barn owl, Tyto alba. Oikos 62, 67–76.
CrossRef |

Edwards, G. P. , de Preu, N. D. , Shakeshaft, B. J. , and Crealy, I. V. (2000). An evaluation of two methods of assessing feral cat and dingo abundance in central Australia. Wildlife Research 27, 143–149.
CrossRef |

Field, S. A. , Tyre, A. J. , Thorn, K. H. , O’Connor, P. J. , and Possingham, H. P. (2005). Improving the efficiency of wildlife monitoring by estimating detectability: a case study of foxes (Vulpes vulpes) on the Eyre Peninsula, South Australia. Wildlife Research 32, 253–258.
CrossRef |

Foran, D. R. , Minta, S. C. , and Heinemeyer, K. S. (1997). DNA-based analysis of hair to identify species and individuals for population research and monitoring. Wildlife Society Bulletin 25, 705–726.


Francisco, L. V. , Langston, A. A. , Mellersh, C. S. , Neal, C. L. , and Ostrander, E. A. (1996). A class of highly polymorphic tetranucleotide repeats for canine genetic mapping. Mammalian Genome 7, 359–362.
CrossRef | CAS | PubMed |

Glen, A. S. , and Dickman, C. R. (2003). Monitoring bait removal in vertebrate pest control: a comparison using track identification and remote photography. Wildlife Research 30, 29–33.
CrossRef |

Gu, W. , and Swihart, R. K. (2004). Absent or undetected? Effects of non-detection of species occurrence on wildlife–habitat models. Biological Conservation 116, 195–203.
CrossRef |

Harrison, R. L. , Barr, D. J. , and Drago, J. W. (2002). A comparison of population survey techniques for swift foxes (Vulpes velox) in New Mexico. American Midland Naturalist 148, 320–337.
CrossRef |

Hines J. E. (2006). ‘PRESENCE Version 2.2 – Software to Estimate Occupancy and Related Parameters.’ (USGS-PWRC: Laurel, MD.)

Holmes, N. G. , Dickens, H. F. , Parker, H. L. , Binns, M. M. , Mellersh, C. S. , and Sampson, J. (1995). Eighteen canine microsatellites. Animal Genetics 24, 132–133.


Hunt, R. , Dall, D. , and Lapidge, S. J. (2007). Effect of a synthetic lure on site visitation and bait uptake by foxes (Vulpes vulpes) and wild dogs (Canis lupis dingo/Canis lupis familiaris). Wildlife Research 34, 461–466.
CrossRef |

Jackson, R. M. , Roe, J. R. , Wangchuk, R. , and Hunter, D. O. (2006). Estimating snow leopard population abundance using photography and capture–recapture techniques. Wildlife Society Bulletin 34, 772–781.
CrossRef |

Karanth, U. K. (1995). Estimating tiger (Panthera tigris) populations from camera-trap data using capture–recapture models. Biological Conservation 71, 333–338.
CrossRef |

Kay, B. , Gifford, E. , Perry, R. , and van de Ven, R. (2000). Trapping efficiency for foxes (Vulpes vulpes) in central New South Wales: age and sex biases and the effects of reduced fox abundance. Wildlife Research 27, 547–552.
CrossRef |

Kohn, M. H. , and Wayne, R. K. (1997). Facts from faeces revisited. Trends in Ecology & Evolution 12, 223–227.
CrossRef |

Kohn, M. H. , York, E. C. , Kamradt, D. A. , Haught, G. , Sauvajof, R. M. , and Wayne, R. K. (1999). Estimating population size by genotyping faeces. Proceedings of the Royal Society of London. Series B. Biological Sciences 266, 657–663.
CrossRef | CAS |

Lade, J. A. , Murray, N. D. , Marks, C. A. , and Robinson, N. A. (1996). Microsatellite differentiation between Phillip Island and mainland Australian populations of the red fox Vulpes vulpes. Molecular Ecology 5, 81–87.
CrossRef | CAS | PubMed |

Lobert, B. , Lumsden, L. , Brunner, H. , and Triggs, B. (2001). An assessment of the accuracy and reliability of hair identification of south-eastern Australian mammals. Wildlife Research 28, 637–641.
CrossRef |

Long, R. A. , Donovan, T. M. , MacKay, P. , Zielinski, W. J. , and Buzas, J. S. (2007a). Effectiveness of scat detection dogs for detecting forest carnivores. Journal of Wildlife Management 71, 2007–2017.
CrossRef |

Long, R. A. , Donovan, T. M. , Mackay, P. , Zielinski, W. J. , and Buzas, J. S. (2007b). Comparing scat detection dogs, cameras, and hair snares for surveying carnivores. Journal of Wildlife Management 71, 2018–2025.
CrossRef |

Lucchini, V. , Fabri, E. , Marucco, F. , Ricci, S. , Boitani, L. , and Randi, E. (2002). Noninvasive molecular tracking of colonizing wolf (Canis lupus) packs in the western Italian Alps. Molecular Ecology 11, 857–868.
CrossRef | CAS | PubMed |

Lynam, A. J. , Rabinowitz, A. , Myint, T. , Maung, M. , Latt, K. T. , and Po, S. H. T. (2009). Estimating abundance with sparse data: tigers in northern Myanmar. Population Ecology 51, 115–121.
CrossRef |

Macdonald D. W. (1987). ‘Running with the Fox.’ (Unwin Hyman Ltd: London.)

MacKenzie, D. I. , Nichols, J. D. , Sutton, N. , Kawanishi, K. , and Bailey, L. L. (2005). Improving inferences in population studies of rare species that are detected imperfectly. Ecology 86, 1101–1113.
CrossRef |

MacKenzie D. I. , Nichols J. D. , Royle J. A. , Pollock K. H. , Bailey L. L. , and Hines J. E. (2006). ‘Occupancy Estimation and Modeling: Inferring Patterns and Dynamics of Species Occurrence.’ (Academic Press: London.)

Mahon, P. S. , Banks, P. B. , and Dickman, C. R. (1998). Population indices for wild carnivores: a critical study in sand-dune habitat, south-western Queensland. Wildlife Research 25, 11–22.
CrossRef |

Meek, P. D. , and Saunders, G. (2000). Home range and movement of foxes (Vulpes vulpes) in coastal New South Wales. Australian Wildlife Research 27, 663–668.
CrossRef |

Mills, L. S. , Pilgrim, K. L. , Schwortz, M. K. , and McKelvey, K. (2000). Identifying lynx and other North American felids based on mtDNA analysis. Conservation Genetics 1, 285–288.
CrossRef | CAS |

Mills, D. J. , Harris, B. , Claridge, A. W. , and Barry, S. C. (2002). Efficacy of hair-sampling techniques for the detection of medium-sized terrestrial mammals. I. A comparison between hair-funnels, hair-tubes and indirect signs. Wildlife Research 29, 379–387.
CrossRef |

Mooney N. , Emms C. , and Bloomfield T. E. (2005). Developing a strategic fox eradication program in a sceptical social environment. In ‘Proceedings of the 13th Australasian Vertebrate Pest Conference, Te Papa, Wellington, New Zealand’. (Eds J. Parkes, M. Statham and G. Edwards.) pp. 150–151. (Manaaki Whenua –Landcare Research: Lincoln, New Zealand.) Available at http://www.landcareresearch.co.nz/news/conferences.asp [Verified May 2009]

Moruzzi, T. L. , Fuller, T. K. , DeGraaf, R. M. , Brooks, R. T. , and Li, W. (2002). Assessing remotely triggered cameras for surveying carnivore distribution. Wildlife Society Bulletin 30, 380–386.


Mowat, G. , and Strobeck, C. (2000). Estimating population size of grizzly bears using hair capture, DNA profiling, and mark-recapture analysis. The Journal of Wildlife Management 64, 183–193.
CrossRef |

Murphy, M. A. , Waits, L. P. , and Kendall, K. C. (2003). The influence of diet on faecal DNA amplification and sex identification in brown bears (Ursus arctos). Molecular Ecology Notes 12, 2261–2265.
CAS |

O’Connell, A. F. , Talancy, N. W. , Bailey, L. L. , Sauer, J. R. , Cook, R. , and Gilbert, A. T. (2006). Estimating site occupancy and detection probability parameters for mammals in a coastal ecosystem. Journal of Wildlife Management 70, 1625–1633.
CrossRef |

Parker B. (2002). Biology of the European red fox (Vulpes vulpes) at Arthursleigh, in the southern highlands of New South Wales. M.Appl.Sci. Thesis, University of Sydney.

Paxinos, E. , McIntosh, C. , Ralls, K. , and Fleischer, R. (1997). A non-invasive method for distinguishing among canid species: amplification and enzyme restriction of DNA from dung. Molecular Ecology 6, 483–486.
CrossRef | CAS | PubMed |

Peakall, R. , and Smouse, P. E. (2006). GenAlEx 6: genetic analysis in Excel. Population genetic software for teaching and research. Molecular Ecology Notes 6, 288–295.
CrossRef |

Peterson, L. M. , and Thomas, J. A. (1998). Performance of Trailmaster® infrared sensors in monitoring captive coyotes. Wildlife Society Bulletin 26, 592–596.


Phillips, R. L. , Andrews, A. D. , Storm, G. L. , and Bishop, R. L. (1972). Dispersal and mortality of red foxes. Journal of Wildlife Management 36, 237–248.
CrossRef |

Piggott, M. P. (2004). Effect of sample age and season of collection on the reliability of microsatellite genotyping of faecal DNA. Wildlife Research 31, 485–493.
CrossRef | CAS |

Piggott, M. P. , and Taylor, A. C. (2003a). Remote collection of animal DNA and its application in conservation management and understanding the population biology of rare and cryptic species. Wildlife Research 30, 1–13.
CrossRef |

Piggott, M. P. , and Taylor, A. C. (2003b). Extensive evaluation of faecal preservation and DNA extraction methods in Australian native and introduced species. Australian Journal of Zoology 51, 341–355.
CrossRef | CAS |

Piggott, M. P. , Bellemain, E. , Taberlet, P. , and Taylor, A. C. (2004). A multiplex pre-amplification method that significantly improves microsatellite amplification and error rates for faecal DNA in limiting conditions. Conservation Genetics 5, 417–420.
CrossRef | CAS |

Piggott, M. P. , Wilson, R. , Banks, S. C. , Marks, C. A. , Gigliotti, F. , and Taylor, A. C. (2008). Evaluating exotic predator control programs using non-invasive genetic tagging. Wildlife Research 35, 617–624.
CrossRef |

Pollock, K. H. , Nichols, J. D. , Simon, T. R. , Farnsworth, G. L. , Bailey, L. L. , and Sauer, J. R. (2002). Large scale wildlife monitoring studies – statistical methods for design and analysis. Environmetrics 13, 105–119.
CrossRef |

Quinn G. P. , and Keough M. J. (2002). ‘Experimental Design and Data Analysis for Biologists.’ (Cambridge University Press: Cambridge, UK.)

Rice, G. (1995). Trailmaster® camera system: the dark side. Wildlife Society Bulletin 23, 110–113.


Sadlier, L. M. J. , Webbon, C. C. , Baker, P. J. , and Harris, S. (2004). Methods of monitoring red foxes Vulpes vulpes and badgers Meles meles: are field signs the answer? Mammal Review 34, 75–98.
CrossRef |

Saunders G. R. , and McLeod L. (2007). ‘Improving Fox Management Strategies in Australia.’ (Bureau of Rural Sciences: Canberra.)

Saunders G. , Coman B. J. , Kinnear J. , and Braysher M. (1995). ‘Managing Vertebrate Pests: Foxes.’ (Australian Government Publishing Service: Canberra.)

Saunders G. , Lane C. , Harris S. , and Dickman C. (2006). ‘Foxes in Tasmania: a Report of an Incursion by an Invasive Species.’ (Invasive Animals Cooperative Research Centre: Canberra.)

Sharp, A. , Norton, M. , Marks, A. , and Holmes, K. (2001). An evaluation of two indices of red fox (Vulpes vulpes) abundance in an arid environment. Wildlife Research 28, 419–424.
CrossRef |

Simcharoen, S. , Pattanavibool, A. , Karanth, K. U. , Nichols, J. D. , and Kumar, N. S. (2007). How many tigers Panthera tigris are there in Huai Kha Khaeng Wildlife Sanctuary, Thailand? An estimate using photographic capture-recapture sampling. Oryx 41, 447–453.
CrossRef |

Sloane, M. A. , Sunnucks, P. , Alpers, D. , Beheregaray, B. , and Taylor, A. C. (2000). Highly reliable genetic identification of individual northern hairy-nosed wombats from single remotely collected hairs: a feasible censusing method. Molecular Ecology 9, 1233–1240.
CrossRef | CAS | PubMed |

Sunnucks, P. , and Hales, D. F. (1996). Numerous transposed sequences of mitochondrial cytochrome oxidase I–II in aphids of the genus Sitobion (Hemiptera: Aphididae). Molecular Biology and Evolution 13, 510–524.
CAS | PubMed |

Taberlet, P. , Cammarra, J. J. , Griffen, S. , Uhres, E. , Hanotte, O. , Waits, L. P. , Dubois-Paganon, C. , Burke, T. , and Bouvet, J. (1997). Noninvasive genetic tracking of the endangered Pyrrenean brown bear population. Molecular Ecology 6, 869–876.
CrossRef | CAS | PubMed |

Thompson W. L. , White G. C. , and Gowan C. (1998). ‘Monitoring Vertebrate Populations.’ (Academic Press: San Diego, CA.)

Towerton, A. L. , Penman, T. D. , Blake, M. E. , Deane, A. T. , Kavanagh, R. P. , and Dickman, C. R. (2008). The potential for remote cameras to monitor visitation by birds and predators at malleefowl mounds. Ecological Management & Restoration 9, 64–67.
CrossRef |

Triggs B. (1996). ‘Scats, Tracks and other Traces: a Field Guide to Australian Mammals.’ (Oxford University Press: Melbourne.)

Trolle, M. , and Kery, M. (2003). Estimation of ocelot density in the Pantanal using capture–recapture analysis of camera trapping data. Journal of Mammalogy 84, 607–614.
CrossRef |

Vine S. J. (2004). Detection of the red fox Vulpes vulpes in the southern highlands of New South Wales: a comparison of methods. M.Appl.Sci. Thesis, University of Sydney, Sydney.

Waits, L. P. , Luikart, G. , and Taberlet, P. (2001). Estimating the probability of identity among genotypes in natural populations: cautions and guidelines. Molecular Ecology 10, 249–256.
CrossRef | CAS | PubMed |

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.
CrossRef |

Woods, J. G. , Paetkau, D. , Lewis, D. , McLellan, B. N. , Proctor, M. , and Strobeck, C. (1999). Genetic tagging of free-ranging black and brown bears. Wildlife Society Bulletin 27, 616–627.



Rent Article (via Deepdyve) Export Citation Cited By (41)