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

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 http://dx.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.


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 doi:10.1109/TAC.1974.1100705

Allen L. Engeman R. Krupa H. 1996 Evaluation of three relative abundance indices for assessing dingo populations. Wildlife Research 23 197 206 doi:10.1071/WR9960197

Banks S. C. Hoyle S. D. Horsup A. Sunnucks P. 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 doi:10.1017/S1367943003003135

Berry O. Sarre S. D. Farrington L. Aitken N. 2007 Faecal DNA detection of invasive species: the case of feral foxes in Tasmania. Wildlife Research 34 1 7 doi:10.1071/WR06082

Boonstra R. Kanter M. Krebs C. J. 1992 A tracking technique to locate small mammals at low densities. Journal of Mammalogy 73 683 685 doi:10.2307/1382044

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. Borchers D. L. 2000 Wildlife population assessment: past developments and future directions. Biometrics 56 1 12 doi:10.1111/j.0006-341X.2000.00001.x

Buckland S. T. Magurran A. E. Green R. E. 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 doi:10.1098/rstb.2004.1589

Bullard R. W. Leiker T. J. Peterson J. E. Kilburn S. R. 1978 a Volatile components of fermented egg, an animal attractant and repellent. Journal of Agricultural and Food Chemistry 26 155 159 doi:10.1021/jf60215a078

Bullard R. W. Shumake S. A. Campbell D. A. Turkowski F. J. 1978 b Preparation and evaluation of a synthetic fermented egg coyote attractant and deer repellent. Journal of Agricultural and Food Chemistry 26 160 163 doi:10.1021/jf60215a037

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. Anderson D. R. 2001 Kullback–Leibler information as a basis for strong inference in ecological studies. Wildlife Research 28 111 119 doi:10.1071/WR99107

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. 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 doi:10.1071/WR96073

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
doi:10.1071/WR9880223

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

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


Davison A. Birks J. D. S. Brookes R. C. Braithwaite T. C. 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
doi:10.1017/S0952836902000730

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. Lynam A. J. 1991 Differential predation of size and sex classes of mice by the barn owl, Tyto alba. Oikos 62 67 76
doi:10.2307/3545447

Edwards G. P. de Preu N. D. Shakeshaft B. J. Crealy I. V. 2000 An evaluation of two methods of assessing feral cat and dingo abundance in central Australia. Wildlife Research 27 143 149 doi:10.1071/WR98067

Field S. A. Tyre A. J. Thorn K. H. O’Connor P. J. 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 doi:10.1071/WR05010

Foran D. R. Minta S. C. 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. Ostrander E. A. 1996 A class of highly polymorphic tetranucleotide repeats for canine genetic mapping. Mammalian Genome 7 359 362
doi:10.1007/s003359900104

Glen A. S. Dickman C. R. 2003 Monitoring bait removal in vertebrate pest control: a comparison using track identification and remote photography. Wildlife Research 30 29 33 doi:10.1071/WR01059

Gu W. Swihart R. K. 2004 Absent or undetected? Effects of non-detection of species occurrence on wildlife–habitat models. Biological Conservation 116 195 203 doi:10.1016/S0006-3207(03)00190-3

Harrison R. L. Barr D. J. Drago J. W. 2002 A comparison of population survey techniques for swift foxes (Vulpes velox) in New Mexico. American Midland Naturalist 148 320 337 doi:10.1674/0003-0031(2002)148[0320:ACOPST]2.0.CO;2

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. Sampson J. 1995 Eighteen canine microsatellites. Animal Genetics 24 132 133

Hunt R. Dall D. 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
doi:10.1071/WR05110

Jackson R. M. Roe J. R. Wangchuk R. Hunter D. O. 2006 Estimating snow leopard population abundance using photography and capture–recapture techniques. Wildlife Society Bulletin 34 772 781 doi:10.2193/0091-7648(2006)34[772:ESLPAU]2.0.CO;2

Karanth U. K. 1995 Estimating tiger (Panthera tigris) populations from camera-trap data using capture–recapture models. Biological Conservation 71 333 338 doi:10.1016/0006-3207(94)00057-W

Kay B. Gifford E. Perry R. 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 doi:10.1071/WR98089

Kohn M. H. Wayne R. K. 1997 Facts from faeces revisited. Trends in Ecology & Evolution 12 223 227 doi:10.1016/S0169-5347(97)01050-1

Kohn M. H. York E. C. Kamradt D. A. Haught G. Sauvajof R. M. Wayne R. K. 1999 Estimating population size by genotyping faeces. Proceedings of the Royal Society of London. Series B. Biological Sciences 266 657 663 doi:10.1098/rspb.1999.0686

Lade J. A. Murray N. D. Marks C. A. Robinson N. A. 1996 Microsatellite differentiation between Phillip Island and mainland Australian populations of the red fox Vulpes vulpes. Molecular Ecology 5 81 87 doi:10.1111/j.1365-294X.1996.tb00293.x

Lobert B. Lumsden L. Brunner H. Triggs B. 2001 An assessment of the accuracy and reliability of hair identification of south-eastern Australian mammals. Wildlife Research 28 637 641 doi:10.1071/WR00124

Long R. A. Donovan T. M. MacKay P. Zielinski W. J. Buzas J. S. 2007 a Effectiveness of scat detection dogs for detecting forest carnivores. Journal of Wildlife Management 71 2007 2017 doi:10.2193/2006-230

Long R. A. Donovan T. M. Mackay P. Zielinski W. J. Buzas J. S. 2007 b Comparing scat detection dogs, cameras, and hair snares for surveying carnivores. Journal of Wildlife Management 71 2018 2025 doi:10.2193/2006-292

Lucchini V. Fabri E. Marucco F. Ricci S. Boitani L. Randi E. 2002 Noninvasive molecular tracking of colonizing wolf (Canis lupus) packs in the western Italian Alps. Molecular Ecology 11 857 868 doi:10.1046/j.1365-294X.2002.01489.x

Lynam A. J. Rabinowitz A. Myint T. Maung M. Latt K. T. Po S. H. T. 2009 Estimating abundance with sparse data: tigers in northern Myanmar. Population Ecology 51 115 121 doi:10.1007/s10144-008-0093-5

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

MacKenzie D. I. Nichols J. D. Sutton N. Kawanishi K. Bailey L. L. 2005 Improving inferences in population studies of rare species that are detected imperfectly. Ecology 86 1101 1113 doi:10.1890/04-1060

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. Dickman C. R. 1998 Population indices for wild carnivores: a critical study in sand-dune habitat, south-western Queensland. Wildlife Research 25 11 22 doi:10.1071/WR97007

Meek P. D. Saunders G. 2000 Home range and movement of foxes (Vulpes vulpes) in coastal New South Wales. Australian Wildlife Research 27 663 668 doi:10.1071/WR98030

Mills L. S. Pilgrim K. L. Schwortz M. K. McKelvey K. 2000 Identifying lynx and other North American felids based on mtDNA analysis. Conservation Genetics 1 285 288 doi:10.1023/A:1011574209558

Mills D. J. Harris B. Claridge A. W. 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 doi:10.1071/WR01031

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. Li W. 2002 Assessing remotely triggered cameras for surveying carnivore distribution. Wildlife Society Bulletin 30 380 386

Mowat G. 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
doi:10.2307/3802989

Murphy M. A. Waits L. P. 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

O’Connell A. F. Talancy N. W. Bailey L. L. Sauer J. R. Cook R. Gilbert A. T. 2006 Estimating site occupancy and detection probability parameters for mammals in a coastal ecosystem. Journal of Wildlife Management 70 1625 1633
doi:10.2193/0022-541X(2006)70[1625:ESOADP]2.0.CO;2

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. 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 doi:10.1046/j.1365-294X.1997.00206.x

Peakall R. Smouse P. E. 2006 GenAlEx 6: genetic analysis in Excel. Population genetic software for teaching and research. Molecular Ecology Notes 6 288 295 doi:10.1111/j.1471-8286.2005.01155.x

Peterson L. M. 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. Bishop R. L. 1972 Dispersal and mortality of red foxes. Journal of Wildlife Management 36 237 248
doi:10.2307/3799056

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 doi:10.1071/WR03096

Piggott M. P. Taylor A. C. 2003 a 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 doi:10.1071/WR02077

Piggott M. P. Taylor A. C. 2003 b Extensive evaluation of faecal preservation and DNA extraction methods in Australian native and introduced species. Australian Journal of Zoology 51 341 355 doi:10.1071/ZO03012

Piggott M. P. Bellemain E. Taberlet P. 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 doi:10.1023/B:COGE.0000031138.67958.44

Piggott M. P. Wilson R. Banks S. C. Marks C. A. Gigliotti F. Taylor A. C. 2008 Evaluating exotic predator control programs using non-invasive genetic tagging. Wildlife Research 35 617 624 doi:10.1071/WR08040

Pollock K. H. Nichols J. D. Simon T. R. Farnsworth G. L. Bailey L. L. Sauer J. R. 2002 Large scale wildlife monitoring studies – statistical methods for design and analysis. Environmetrics 13 105 119 doi:10.1002/env.514

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. Harris S. 2004 Methods of monitoring red foxes Vulpes vulpes and badgers Meles meles: are field signs the answer? Mammal Review 34 75 98
doi:10.1046/j.0305-1838.2003.00029.x

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. Holmes K. 2001 An evaluation of two indices of red fox (Vulpes vulpes) abundance in an arid environment. Wildlife Research 28 419 424 doi:10.1071/WR00075

Simcharoen S. Pattanavibool A. Karanth K. U. Nichols J. D. 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 doi:10.1017/S0030605307414107

Sloane M. A. Sunnucks P. Alpers D. Beheregaray B. 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 doi:10.1046/j.1365-294x.2000.00993.x

Sunnucks P. 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

Taberlet P. Cammarra J. J. Griffen S. Uhres E. Hanotte O. Waits L. P. Dubois-Paganon C. Burke T. Bouvet J. 1997 Noninvasive genetic tracking of the endangered Pyrrenean brown bear population. Molecular Ecology 6 869 876
doi:10.1111/j.1365-294X.1997.tb00141.x

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. 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 doi:10.1111/j.1442-8903.2008.00389.x

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

Trolle M. Kery M. 2003 Estimation of ocelot density in the Pantanal using capture–recapture analysis of camera trapping data. Journal of Mammalogy 84 607 614 doi:10.1644/1545-1542(2003)084<0607:EOODIT>2.0.CO;2

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. Taberlet P. 2001 Estimating the probability of identity among genotypes in natural populations: cautions and guidelines. Molecular Ecology 10 249 256 doi:10.1046/j.1365-294X.2001.01185.x

Wilson G. J. 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 doi:10.1071/WR00033

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



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