Blood, sweat and tears: a review of non-invasive DNA sampling

10.24072/pcjournal.98 - Peer Community Journal, Volume 2 (2022), article no. e16.

Get full text PDF Peer reviewed and recommended by PCI

The use of DNA data is ubiquitous across animal sciences. DNA may be obtained from an organism for a myriad of reasons including identification and distinction between cryptic species, sex identification, comparisons of different morphocryptic genotypes or assessments of relatedness between organisms prior to a behavioural study. DNA should be obtained while minimizing the impact on the fitness, behaviour or welfare of the subject being tested, as this can bias experimental results and cause long-lasting effects on wild animals. Furthermore, minimizing impact on experimental animals is a key Refinement principle within the ‘3Rs’ framework which aims to ensure that animal welfare during experimentation is optimised. The term ‘non-invasive DNA sampling’ has been defined to indicate collection methods that do not require capture or cause disturbance to the animal, including any effects on behaviour or fitness. In practice this is not always the case, as the term ‘non-invasive’ is commonly used in the literature to describe studies where animals are restrained or subjected to aversive procedures. We reviewed the non-invasive DNA sampling literature for the past six years (380 papers published in 2013-2018) and uncovered the existence of a significant gap between the current use of this terminology (i.e. ‘non-invasive DNA sampling’) and its original definition. We show that 58% of the reviewed papers did not comply with the original definition. We discuss the main experimental and ethical issues surrounding the potential confusion or misuse of the phrase ‘non-invasive DNA sampling’ in the current literature and provide potential solutions. In addition, we introduce the terms ‘non-disruptive’ and ‘minimally disruptive’ DNA sampling, to indicate methods that eliminate or minimise impacts not on the physical integrity/structure of the animal, but on its behaviour, fitness and welfare, which in the literature reviewed corresponds to the situation for which an accurate term is clearly missing. Furthermore, we outline when these methods are appropriate to use.

Published online:
DOI: 10.24072/pcjournal.98
Lefort, Marie-Caroline 1; Cruickshank, Robert H. 2; Descovich, Kris 3; Adams, Nigel J. 3; Barun, Arijana 2; Emami-Khoyi, Arsalan 2; Ridden, Johnathon 2; Smith, Vikki R. 2; Sprague, Rowan 2; Waterhouse, Benjamin 2; Boyer, Stéphane 4

1 Laboratoire d'Écologie et Biologie des Interactions (EBI) – UMR 7267 CNRS, Université de Poitiers, 5 rue Albert Turpain, 86073 POITIERS Cedex 9, France
2 Department of Ecology, Faculty of Agricultural and Life Sciences, PO Box 85084, Lincoln University, Lincoln 7647, Christchurch, New Zealand.
3 Environmental and Animal Sciences, Unitec Institute of Technology, 139 Carrington Road, Mt Albert, Auckland 1025, New Zealand.
4 Institut de Recherche sur la Biologie de l’Insecte (IRBI) – UMR 7261 CNRS / Université de Tours, Parc Grandmont, 37200 Tours, France
License: CC-BY 4.0
Copyrights: The authors retain unrestricted copyrights and publishing rights
     author = {Lefort, Marie-Caroline and Cruickshank, Robert H. and Descovich, Kris and Adams, Nigel J. and Barun, Arijana and Emami-Khoyi, Arsalan and Ridden, Johnathon and Smith, Vikki R. and Sprague, Rowan and Waterhouse, Benjamin and Boyer, St\'ephane},
     title = {Blood, sweat and tears: a review of non-invasive {DNA} sampling},
     journal = {Peer Community Journal},
     eid = {e16},
     publisher = {Peer Community In},
     volume = {2},
     year = {2022},
     doi = {10.24072/pcjournal.98},
     url = {}
AU  - Lefort, Marie-Caroline
AU  - Cruickshank, Robert H.
AU  - Descovich, Kris
AU  - Adams, Nigel J.
AU  - Barun, Arijana
AU  - Emami-Khoyi, Arsalan
AU  - Ridden, Johnathon
AU  - Smith, Vikki R.
AU  - Sprague, Rowan
AU  - Waterhouse, Benjamin
AU  - Boyer, Stéphane
TI  - Blood, sweat and tears: a review of non-invasive DNA sampling
JO  - Peer Community Journal
PY  - 2022
DA  - 2022///
VL  - 2
PB  - Peer Community In
UR  -
UR  -
DO  - 10.24072/pcjournal.98
ID  - 10_24072_pcjournal_98
ER  - 
%0 Journal Article
%A Lefort, Marie-Caroline
%A Cruickshank, Robert H.
%A Descovich, Kris
%A Adams, Nigel J.
%A Barun, Arijana
%A Emami-Khoyi, Arsalan
%A Ridden, Johnathon
%A Smith, Vikki R.
%A Sprague, Rowan
%A Waterhouse, Benjamin
%A Boyer, Stéphane
%T Blood, sweat and tears: a review of non-invasive DNA sampling
%J Peer Community Journal
%D 2022
%V 2
%I Peer Community In
%R 10.24072/pcjournal.98
%F 10_24072_pcjournal_98
Lefort, Marie-Caroline; Cruickshank, Robert H.; Descovich, Kris; Adams, Nigel J.; Barun, Arijana; Emami-Khoyi, Arsalan; Ridden, Johnathon; Smith, Vikki R.; Sprague, Rowan; Waterhouse, Benjamin; Boyer, Stéphane. Blood, sweat and tears: a review of non-invasive DNA sampling. Peer Community Journal, Volume 2 (2022), article  no. e16. doi : 10.24072/pcjournal.98.

Peer reviewed and recommended by PCI : 10.24072/pci.ecology.100029

Conflict of interest of the recommender and peer reviewers:
The recommender in charge of the evaluation of the article and the reviewers declared that they have no conflict of interest (as defined in the code of conduct of PCI) with the authors or with the content of the article.

[1] Anile, S.; Arrabito, C.; Mazzamuto, M.; Scornavacca, D.; Ragni, B. A non-invasive monitoring on European wildcat (Felis silvestris silvestris Schreber, 1777) in Sicily using hair trapping and camera trapping: does scented lure work?, Hystrix-Italian Journal of Mammalogy, Volume 23 | DOI

[2] Baillon, L.; Pierron, F.; Oses, J.; Pannetier, P.; Normandeau, E.; Couture, P.; Labadie, P.; Budzinski, H.; Lambert, P.; Bernatchez, L.; Baudrimont, M. Detecting the exposure to Cd and PCBs by means of a non-invasive transcriptomic approach in laboratory and wild contaminated European eels (Anguilla anguilla), Environmental Science and Pollution Research, Volume 23 (2016) no. 6, pp. 5431-5441 | DOI

[3] Banks, S. C.; Hoyle, S. D.; Horsup, A.; Sunnucks, P.; Taylor, A. C. Demographic monitoring of an entire species (the northern hairy-nosed wombat, Lasiorhinus krefftii) by genetic analysis of non-invasively collected material, Animal Conservation, Volume 6 (2003) no. 2, pp. 101-107 | DOI

[4] Barbosa, S.; Pauperio, J.; Searle, J. B.; Alves, P. C. Genetic identification of I berian rodent species using both mitochondrial and nuclear loci: application to noninvasive sampling, Molecular Ecology Resources, Volume 13 (2013) no. 1, pp. 43-56 | DOI

[5] Barbosa, S.; Paupério, J.; Herman, J. S.; Ferreira, C. M.; Pita, R.; Vale-Gonçalves, H. M.; Cabral, J. A.; Garrido-García, J. A.; Soriguer, R. C.; Beja, P.; Mira, A.; Alves, P. C.; Searle, J. B. Endemic species may have complex histories: within-refugium phylogeography of an endangered Iberian vole, Molecular Ecology, Volume 26 (2017) no. 3, pp. 951-967 | DOI

[6] Barrett-Lennard, L.; Smith, T. G.; Ellis, G. M. A cetacean biopsy system using lightweight pneumatic darts, and its effect on the behavior of killer whales, Marine Mammal Science, Volume 12 (1996) no. 1, pp. 14-27 | DOI

[7] Bateson, M. Cumulative stress in research animals: Telomere attrition as a biomarker in a welfare context?, BioEssays, Volume 38 (2016) no. 2, pp. 201-212 | DOI

[8] Baumgardt, J. A.; Goldberg, C. S.; Reese, K. P.; Connelly, J. W.; Musil, D. D.; Garton, E. O.; Waits, L. P. A method for estimating population sex ratio for sage‐grouse using noninvasive genetic samples, Molecular Ecology Resources, Volume 13 (2013) no. 3, pp. 393-402 | DOI

[9] Bearzi, G. First report of a common dolphin (Delphinus delphis) death following penetration of a biopsy dart, Journal of Cetacean Research and Management, Volume 2 (2000)

[10] Bienert, F.; De Danieli, S.; Miquel, C.; Coissac, E.; Poillot, C.; Brun, J.-J.; Taberlet, P. Tracking earthworm communities from soil DNA, Molecular Ecology, Volume 21 (2012) no. 8, pp. 2017-2030 | DOI

[11] Boulanger, J.; Stenhouse, G.; Munro, R. Sources of heterogeneity bias when DNA mark-recapture sampling methods are applied to grizzly bear (Ursus arctos) populations, Journal of Mammalogy, Volume 85 (2004) no. 4, pp. 618-624 | DOI

[12] Boyer, S. R code “Blood Sweat and Tears.” Dataset and code. Figshare, 2019 | DOI

[13] Boyer, S.; Wratten, S. D.; Holyoake, A.; Abdelkrim, J.; Cruickshank, R. H. Using Next-Generation Sequencing to Analyse the Diet of a Highly Endangered Land Snail (Powelliphanta augusta) Feeding on Endemic Earthworms, PLoS ONE, Volume 8 (2013) no. 9 | DOI

[14] Brekke, P.; Bennett, P. M.; Santure, A. W.; Ewen, J. G. High genetic diversity in the remnant island population of hihi and the genetic consequences of re-introduction, Molecular Ecology, Volume 20 (2011) no. 1, pp. 29-45 | DOI

[15] Brown MW; Kraus SD; Gaskin DE, Special Issue Report. International Whaling Commission, 1991

[16] Brown, V. A.; Willcox, E. V.; Fagan, K. E.; Bernard, R. F. Identification of Southeastern Bat Species Using Noninvasive Genetic Sampling of Individual Guano Pellets, Journal of Fish and Wildlife Management, Volume 8 (2017) no. 2, pp. 632-639 | DOI

[17] Brzeziński, M.; Romanowski, J. Experiments on sprainting activity of otters ( Lutra lutra ) in the Bieszczady Mountains, southeastern Poland / Observations des épreintes de la loutre ( Lutra lutra ) sur les montagnes du Bieszczady au sud-est de la Pologne, Mammalia, Volume 70 (2006) | DOI

[18] Cohen, O.; Barocas, A.; Geffen, E. Conflicting management policies for the Arabian wolfCanis lupus arabsin the Negev Desert: is this justified?, Oryx, Volume 47 (2013) no. 2, pp. 228-236 | DOI

[19] Collins, R. A.; Armstrong, K. F.; Holyoake, A. J.; Keeling, S. Something in the water: biosecurity monitoring of ornamental fish imports using environmental DNA, Biological Invasions, Volume 15 (2012) no. 6, pp. 1209-1215 | DOI

[20] Creel, S. Social dominance and stress hormones, Trends in Ecology & Evolution, Volume 16 (2001) no. 9, pp. 491-497 | DOI

[21] Cullingham, C. I.; Thiessen, C. D.; Derocher, A. E.; Paquet, P. C.; Miller, J. M.; Hamilton, J. A.; Coltman, D. W. Population structure and dispersal of wolves in the Canadian Rocky Mountains, Journal of Mammalogy, Volume 97 (2016) no. 3, pp. 839-851 | DOI

[22] Dai, Y.; Lin, Q.; Fang, W.; Zhou, X.; Chen, X. Noninvasive and nondestructive sampling for avian microsatellite genotyping: a case study on the vulnerable Chinese Egret (Egretta eulophotes), Avian Research, Volume 6 (2015) no. 1 | DOI

[23] Dalén, L.; Götherström, A.; Meijer, T.; Shapiro, B. Recovery of DNA from Footprints in the Snow, The Canadian Field-Naturalist, Volume 121 (2007) no. 3 | DOI

[24] Ditmer, M. A.; Vincent, J. B.; Werden, L. K.; Tanner, J. C.; Laske, T. G.; Iaizzo, P. A.; Garshelis, D. L.; Fieberg, J. R. Bears Show a Physiological but Limited Behavioral Response to Unmanned Aerial Vehicles, Current Biology, Volume 25 (2015) no. 17, pp. 2278-2283 | DOI

[25] Doerr, L.; Richardson, K.; Ewen, J.; Armstrong, D. Effect of supplementary feeding on reproductive success of hihi (stitchbird, Notiomystis cincta) at a mature forest reintroduction site, New Zealand Journal of Ecology, Volume 41 (2016) no. 1 | DOI

[26] Duenas, J.; Cruickshank, R.; Ross, J. Optimisation of a microsatellite panel for the individual identification of brushtail possums using low template DNA, New Zeland Journal of Ecology, Volume 39 (2015)

[27] Fiorito, G.; Affuso, A.; Basil, J.; Cole, A.; de Girolamo, P.; D’Angelo, L.; Dickel, L.; Gestal, C.; Grasso, F.; Kuba, M.; Mark, F.; Melillo, D.; Osorio, D.; Perkins, K.; Ponte, G.; Shashar, N.; Smith, D.; Smith, J.; Andrews, P. L. Guidelines for the Care and Welfare of Cephalopods in Research –A consensus based on an initiative by CephRes, FELASA and the Boyd Group, Laboratory Animals, Volume 49 (2015) no. 2_suppl, pp. 1-90 | DOI

[28] Ford, B.; Govindarajulu, P.; Larsen, K.; Russello, M. Evaluating the efficacy of non-invasive genetic sampling of the Northern Pacific rattlesnake with implications for other venomous squamates, Conservation Genetics Resources, Volume 9 (2017) no. 1, pp. 13-15 | DOI

[29] Fumanal, B.; Martin, J.-F.; Bon, M. High through-put characterization of insect morphocryptic entities by a non-invasive method using direct-PCR of fecal DNA, Journal of Biotechnology, Volume 119 (2005) no. 1, pp. 15-19 | DOI

[30] Garshelis, D. L. On the allure of noninvasive genetic sampling — putting a face to the name, Ursus, Volume 17 (2006) no. 2, pp. 109-123 | DOI

[31] Gauthier, J.; Sears, R. Behavioral response of four species of balaenopterid whales to biopsy sampling, Marine Mammal Science, Volume 15 (1999) no. 1, pp. 85-101 | DOI

[32] Gemmell, N. J.; Majluf, P. Projectile biopsy sampling of fur seals, Marine Mammal Science, Volume 13 (1997) no. 3, pp. 512-516 | DOI

[33] Godwin, B.; Albeke, S.; Bergman, H.; Walters, A.; Ben-David, M. Density of river otters (Lontra canadensis) in relation to energy development in the Green River Basin, Wyoming, Science of The Total Environment, Volume 532 (2015), pp. 780-790 | DOI

[34] Hamilton, M. J.; Sadowsky, M. J. DNA Profiling in Ecology In: Encyclopedia of Life Sciences (2010) | DOI

[35] Hamm, C. A.; Aggarwal, D.; Landis, D. A. Evaluating the impact of non-lethal DNA sampling on two butterflies, Vanessa cardui and Satyrodes eurydice, Journal of Insect Conservation, Volume 14 (2010) no. 1, pp. 11-18 | DOI

[36] Harcourt, R. G.; Turner, E.; Hall, A.; Waas, J. R.; Hindell, M. Effects of capture stress on free-ranging, reproductively active male Weddell seals, Journal of Comparative Physiology A, Volume 196 (2010) no. 2, pp. 147-154 | DOI

[37] Hebert, P. D. N.; Penton, E. H.; Burns, J. M.; Janzen, D. H.; Hallwachs, W. Ten species in one: DNA barcoding reveals cryptic species in the neotropical skipper butterfly Astraptes fulgerator, Proceedings of the National Academy of Sciences, Volume 101 (2004) no. 41, pp. 14812-14817 | DOI

[38] Henry, P.; Henry, A.; Russello, M. A. A Noninvasive Hair Sampling Technique to Obtain High Quality DNA from Elusive Small Mammals, Journal of Visualized Experiments (2011) no. 49 | DOI

[39] Herrando-Pérez, S.; Brook, B. W.; Bradshaw, C. J. A. Ecology Needs a Convention of Nomenclature, BioScience, Volume 64 (2014) no. 4, pp. 311-321 | DOI

[40] Hodges, K. E. Defining the problem: terminology and progress in ecology, Frontiers in Ecology and the Environment, Volume 6 (2008) no. 1, pp. 35-42 | DOI

[41] Hollands, C. The animals (scientific procedures) act 1986, The Lancet, Volume 328 (1986) no. 8497, pp. 32-33 | DOI

[42] Hollenbeck, N.; Scheel, D.; Gravley, M. C.; Sage, G. K.; Toussaint, R.; Talbot, S. L. Use of Swabs for Sampling Epithelial Cells for Molecular Genetics Analyses inEnteroctopus, American Malacological Bulletin, Volume 35 (2017) no. 2, pp. 145-157 | DOI

[43] Huang, H.; Wang, H.; Li, L.; Wu, Z.; Chen, J. Genetic Diversity and Population Demography of the Chinese Crocodile Lizard (Shinisaurus crocodilurus) in China, PLoS ONE, Volume 9 (2014) no. 3 | DOI

[44] Janse, M.; Kappe, A. L.; Van Kuijk, B. L. M. Paternity testing using the poisonous sting in captive white-spotted eagle rays Aetobatus narinari : a non-invasive tool for captive sustainability programmes, Journal of Fish Biology, Volume 82 (2013) no. 3, pp. 1082-1085 | DOI

[45] Jedlicka, J. A.; Vo, A.-T. E.; Almeida, R. P. P. Molecular scatology and high-throughput sequencing reveal predominately herbivorous insects in the diets of adult and nestling Western Bluebirds (Sialia mexicana) in California vineyards, The Auk, Volume 134 (2017) no. 1, pp. 116-127 | DOI

[46] Jones, S. P.; Kennedy, S. W. Feathers as a source of RNA for genomic studies in avian species, Ecotoxicology, Volume 24 (2015) no. 1, pp. 55-60 | DOI

[47] Karamanlidis, A. A.; Stojanov, A.; de Gabriel Hernando, M.; Ivanov, G.; Kocijan, I.; Melovski, D.; Skrbinšek, T.; Zedrosser, A. Distribution and genetic status of brown bears in FYR Macedonia: implications for conservation, Acta Theriologica, Volume 59 (2014) no. 1, pp. 119-128 | DOI

[48] Kauffman, L. K.; Bjork, J. K.; Gallup, J. M.; Boggiatto, P. M.; Bellaire, B. H.; Petersen, C. A. Early Detection ofBrucella Canisvia Quantitative Polymerase Chain Reaction Analysis, Zoonoses and Public Health, Volume 61 (2014) no. 1, pp. 48-54 | DOI

[49] Koczur, L. M.; Williford, D.; DeYoung, R. W.; Ballard, B. M. Bringing back the dead: Genetic data from avian carcasses, Wildlife Society Bulletin, Volume 41 (2017) no. 4, pp. 796-803 | DOI

[50] Kowarski, K. Effects of Remote Biopsy Sampling on Long-Finned Pilot Whales (Globicephala melas) in Nova Scotia, Aquatic Mammals, Volume 40 (2014) no. 2, pp. 117-125 | DOI

[51] Krützen, M.; Barre, L. M.; Moller, L. M.; Heithaus, M. R.; Simms, C.; Sherwin, W. B. A biopsy system for small cetaceans: darting success and wound healing in Tursiops spp., Marine Mammal Science, Volume 18 (2002) no. 4, pp. 863-878 | DOI

[52] Lampa, S.; Henle, K.; Klenke, R.; Hoehn, M.; Gruber, B. How to overcome genotyping errors in non-invasive genetic mark-recapture population size estimation-A review of available methods illustrated by a case study, The Journal of Wildlife Management, Volume 77 (2013) no. 8, pp. 1490-1511 | DOI

[53] Lefort, M.-C.; Boyer, S.; De Romans, S.; Glare, T.; Armstrong, K.; Worner, S. Invasion success of a scarab beetle within its native range: host range expansion versus host-shift, PeerJ, Volume 2 (2014) | DOI

[54] Lefort, M.-C.; Wratten, S.; Cusumano, A.; Varennes, Y.-D.; Boyer, S. Disentangling higher trophic level interactions in the cabbage aphid food web using high-throughput DNA sequencing, Metabarcoding and Metagenomics, Volume 1 (2017) | DOI

[55] Li, J.; Cui, Y.; Jiang, J.; Yu, J.; Niu, L.; Deng, J.; Shen, F.; Zhang, L.; Yue, B.; Li, J. Applying DNA barcoding to conservation practice: a case study of endangered birds and large mammals in China, Biodiversity and Conservation, Volume 26 (2017) no. 3, pp. 653-668 | DOI

[56] Llaneza, L.; García, E. J.; López-Bao, J. V. Intensity of Territorial Marking Predicts Wolf Reproduction: Implications for Wolf Monitoring, PLoS ONE, Volume 9 (2014) no. 3 | DOI

[57] López, H.; Contreras-Díaz, H. G.; Oromí, P.; Juan, C. Delimiting species boundaries for endangered Canary Island grasshoppers based on DNA sequence data, Conservation Genetics, Volume 8 (2007) no. 3, pp. 587-598 | DOI

[58] Madden, A. A.; Barberán, A.; Bertone, M. A.; Menninger, H. L.; Dunn, R. R.; Fierer, N. The diversity of arthropods in homes across the United States as determined by environmental DNA analyses, Molecular Ecology, Volume 25 (2016) no. 24, pp. 6214-6224 | DOI

[59] Magoun, A. J.; Long, C. D.; Schwartz, M. K.; Pilgrim, K. L.; Lowell, R. E.; Valkenburg, P. Integrating motion‐detection cameras and hair snags for wolverine identification, The Journal of Wildlife Management, Volume 75 (2011) no. 3, pp. 731-739 | DOI

[60] Malekian, M.; Sadeghi, P.; Goudarzi, F. Assessment of environmental DNA for detection of an imperiled Amphibian, the luristan newt (Neurergus kaiseri, Schmidt 1952), Herpetological Conservation and Biology, Volume 13 (2018)

[61] Mannise, N.; Trovat, R. G.; Duarte, J. M. B.; Maldonado, J. E.; González, S. Using non–invasive genetic techniques to assist in maned wolf conservation in a remnant fragment of the Brazilian Cerrado, Animal Biodiversity and Conservation, Volume 41 (2018) no. 2, pp. 315-319 | DOI

[62] Marschalek, D. A.; Jesu, J. A.; Berres, M. E. Impact of non-lethal genetic sampling on the survival, longevity and behaviour of the Hermes copper (Lycaena hermes) butterfly, Insect Conservation and Diversity, Volume 6 (2013) no. 6, pp. 658-662 | DOI

[63] McCarthy, M. A.; Parris, K. M. Clarifying the effect of toe clipping on frogs with Bayesian statistics, Journal of Applied Ecology, Volume 41 (2004) no. 4, pp. 780-786 | DOI

[64] Miller, B.; Kean, C. Encyclopedia and Dictionary of Medicine, Nursing, and Allied Health, WB Saunders Company, 1983

[65] Modave, E.; MacDonald, A. J.; Sarre, S. D. A single mini-barcode test to screen for Australian mammalian predators from environmental samples, GigaScience, Volume 6 (2017) no. 8 | DOI

[66] Monteiro, N. M.; Silva, R. M.; Cunha, M.; Antunes, A.; Jones, A. G.; Vieira, M. N. Validating the use of colouration patterns for individual recognition in the worm pipefish using a novel set of microsatellite markers, Molecular Ecology Resources, Volume 14 (2014) no. 1, pp. 150-156 | DOI

[67] Morinha, F.; Travassos, P.; Carvalho, D.; Magalhaes, P.; Cabral, J. A.; Bastos, E. DNA sampling from body swabs of terrestrial slugs (Gastropoda: Pulmonata): a simple and non-invasive method for molecular genetics approaches, Journal of Molluscan Studies, Volume 80 (2014) no. 1, pp. 99-101 | DOI

[68] Murphy, D. D.; Noon, B. D. Coping with Uncertainty in Wildlife Biology, The Journal of Wildlife Management, Volume 55 (1991) no. 4 | DOI

[69] Mächler, E.; Deiner, K.; Steinmann, P.; Altermatt, F. Utility of environmental DNA for monitoring rare and indicator macroinvertebrate species, Freshwater Science, Volume 33 (2014) no. 4, pp. 1174-1183 | DOI

[70] Nelson, G. L.; Graves, B. M. Anuran Population Monitoring: Comparison of the North American Amphibian Monitoring Program's Calling Index with Mark-Recapture Estimates for Rana clamitans, Journal of Herpetology, Volume 38 (2004) no. 3, pp. 355-359 | DOI

[71] Nguyen, H. Q.; Kim, Y. I.; Borzée, A.; Jang, Y. Efficient isolation method for high-quality genomic DNA from cicada exuviae, Ecology and Evolution, Volume 7 (2017) no. 20, pp. 8161-8169 | DOI

[72] Nichols, R. V.; Königsson, H.; Danell, K.; Spong, G. Browsed twig environmental DNA: diagnostic PCR to identify ungulate species, Molecular Ecology Resources, Volume 12 (2012) no. 6, pp. 983-989 | DOI

[73] Oi, C. A.; López-Uribe, M. M.; Cervini, M.; Del Lama, M. A. Non-lethal method of DNA sampling in euglossine bees supported by mark–recapture experiments and microsatellite genotyping, Journal of Insect Conservation, Volume 17 (2013) no. 5, pp. 1071-1079 | DOI

[74] Pagano, A. M.; Peacock, E.; McKinney, M. A. Remote biopsy darting and marking of polar bears, Marine Mammal Science, Volume 30 (2014) no. 1, pp. 169-183 | DOI

[75] Parris, K. M.; McCall, S. C.; McCarthy, M. A.; Minteer, B. A.; Steele, K.; Bekessy, S.; Medvecky, F. Assessing ethical trade-offs in ecological field studies, Journal of Applied Ecology, Volume 47 (2010) no. 1, pp. 227-234 | DOI

[76] Player, D.; Lausen, C.; Zaitlin, B.; Harrison, J.; Paetkau, D.; Harmston, E. An alternative minimally invasive technique for genetic sampling of bats: Wing swabs yield species identification, Wildlife Society Bulletin, Volume 41 (2017) no. 3, pp. 590-596 | DOI

[77] Ponjoan, A.; Bota, G.; De La Morena, E. L. G.; Morales, M. B.; Wolff, A.; Marco, I.; Mañosa, S. Adverse Effects of Capture and Handling Little Bustard, Journal of Wildlife Management, Volume 72 (2008) no. 1, pp. 315-319 | DOI

[78] Porco, D.; Rougerie, R.; Deharveng, L.; Hebert, P. Coupling non‐destructive DNA extraction and voucher retrieval for small soft‐bodied Arthropods in a high‐throughput context: the example of Collembola, Molecular Ecology Resources, Volume 10 (2010) no. 6, pp. 942-945 | DOI

[79] Proffitt, K. M.; Goldberg, J. F.; Hebblewhite, M.; Russell, R.; Jimenez, B. S.; Robinson, H. S.; Pilgrim, K.; Schwartz, M. K. Integrating resource selection into spatial capture-recapture models for large carnivores, Ecosphere, Volume 6 (2015) no. 11 | DOI

[80] Prunier, J.; Kaufmann, B.; Grolet, O.; Picard, D.; Pompanon, F.; Joly, P. Skin swabbing as a new efficient DNA sampling technique in amphibians, and 14 new microsatellite markers in the alpine newt ( Ichthyosaura alpestris ), Molecular Ecology Resources, Volume 12 (2012) no. 3, pp. 524-531 | DOI

[81] Quinn, T. P.; Wirsing, A. J.; Smith, B.; Cunningham, C. J.; Ching, J. Complementary use of motion-activated cameras and unbaited wire snares for DNA sampling reveals diel and seasonal activity patterns of brown bears (Ursus arctos) foraging on adult sockeye salmon (Oncorhynchus nerka), Canadian Journal of Zoology, Volume 92 (2014) no. 10, pp. 893-903 | DOI

[82] R Core Team R: A language and environment for statistical computing. R Foundation for Statistical Computing. Vienna, Austria., 2018

[83] RStudio RStudio: Integrated development for R. , 2017 ([Online] RStudio, Inc., Boston, MA URL http://www.rstudio. com.)

[84] Reinardy, H. C.; Skippins, E.; Henry, T. B.; Jha, A. N. Assessment of DNA damage in sperm after repeated non-invasive sampling in zebrafish Danio rerio, Journal of Fish Biology, Volume 82 (2013) no. 3, pp. 1074-1081 | DOI

[85] Richter, A.; Weinhold, D.; Robertson, G.; Young, M.; Edwards, T.; Hnatiuk, S.; Osborne, W. More than an empty case: a non invasive technique for monitoring the Australian critically endangered golden sun moth, Synemon plana (Lepidoptera: Castniidae), Journal of Insect Conservation, Volume 17 (2013) no. 3, pp. 529-536 | DOI

[86] Ringler, E. Testing skin swabbing for DNA sampling in dendrobatid frogs, Amphibia-Reptilia, Volume 39 (2018) no. 2, pp. 245-251 | DOI

[87] Robinson, S. J.; Waits, L. P.; Martin, I. D. Estimating abundance of American black bears using DNA-based capture–mark–recapture models, Ursus, Volume 20 (2009) no. 1, pp. 1-11 | DOI

[88] Roffler, G. H.; Talbot, S. L.; Luikart, G.; Sage, G. K.; Pilgrim, K. L.; Adams, L. G.; Schwartz, M. K. Lack of sex-biased dispersal promotes fine-scale genetic structure in alpine ungulates, Conservation Genetics, Volume 15 (2014) no. 4, pp. 837-851 | DOI

[89] Roques, J. A.; Abbink, W.; Geurds, F.; van de Vis, H.; Flik, G. Tailfin clipping, a painful procedure: Studies on Nile tilapia and common carp, Physiology & Behavior, Volume 101 (2010) no. 4, pp. 533-540 | DOI

[90] Rorat, A.; Kachamakova-Trojanowska, N.; Jozkowicz, A.; Kruk, J.; Cocquerelle, C.; Vandenbulcke, F.; Santocki, M.; Plytycz, B. Coelomocyte-derived fluorescence and DNA markers of composting earthworm species, Journal of Experimental Zoology Part A: Ecological Genetics and Physiology, Volume 321 (2014) no. 1, pp. 28-40 | DOI

[91] Rovang, S.; Nielsen, S. E.; Stenhouse, G. In the trap: detectability of fixed hair trap DNA methods in grizzly bear population monitoring, Wildlife Biology, Volume 21 (2015) no. 2, pp. 68-79 | DOI

[92] Roy, J.; Vigilant, L.; Gray, M.; Wright, E.; Kato, R.; Kabano, P.; Basabose, A.; Tibenda, E.; Kühl, H. S.; Robbins, M. M. Challenges in the use of genetic mark-recapture to estimate the population size of Bwindi mountain gorillas (Gorilla beringei beringei), Biological Conservation, Volume 180 (2014), pp. 249-261 | DOI

[93] Sboner, A.; Mu, X.; Greenbaum, D.; Auerbach, R. K.; Gerstein, M. B. The real cost of sequencing: higher than you think!, Genome Biology, Volume 12 (2011) no. 8 | DOI

[94] Seguel, M.; Paredes, E.; Pavés, H.; Gottdenker, N. L. Capture-induced stress cardiomyopathy in South American fur seal pups (Arctophoca australis gracilis), Marine Mammal Science, Volume 30 (2014) no. 3, pp. 1149-1157 | DOI

[95] Steyer, K.; Simon, O.; Kraus, R. H. S.; Haase, P.; Nowak, C. Hair trapping with valerian-treated lure sticks as a tool for genetic wildcat monitoring in low-density habitats, European Journal of Wildlife Research, Volume 59 (2013) no. 1, pp. 39-46 | DOI

[96] Suarez, R. K.; Moyes, C. D. Metabolism in the age of ‘omes’, Journal of Experimental Biology, Volume 215 (2012) no. 14, pp. 2351-2357 | DOI

[97] Sugimoto, T.; Aramilev, V. V.; Kerley, L. L.; Nagata, J.; Miquelle, D. G.; McCullough, D. R. Noninvasive genetic analyses for estimating population size and genetic diversity of the remaining Far Eastern leopard (Panthera pardus orientalis) population, Conservation Genetics, Volume 15 (2014) no. 3, pp. 521-532 | DOI

[98] Suleman, M. A.; Wango, E.; Sapolsky, R. M.; Odongo, H.; Hau, J. Physiologic manifestations of stress from capture and restraint of free-ranging male African green monkeys (Cercopithecus aethiops), Journal of Zoo and Wildlife Medicine, Volume 35 (2004) no. 1, pp. 20-24 | DOI

[99] Taberlet, P.; Luikart, G. Non-invasive genetic sampling and individual identification, Biological Journal of the Linnean Society, Volume 68 (1999) no. 1-2, pp. 41-55 | DOI

[100] Taberlet, P.; Waits, L. P.; Luikart, G. Noninvasive genetic sampling: look before you leap, Trends in Ecology & Evolution, Volume 14 (1999) no. 8, pp. 323-327 | DOI

[101] Thomson, J. A.; Heithaus, M. R. Animal-borne video reveals seasonal activity patterns of green sea turtles and the importance of accounting for capture stress in short-term biologging, Journal of Experimental Marine Biology and Ecology, Volume 450 (2014), pp. 15-20 | DOI

[102] du Toit, Z.; Grobler, J. P.; Kotze, A.; Jansen, R.; Dalton, D. L. Scale samples from Temminck’s ground pangolin (Smutsia temminckii): a non-invasive source of DNA, Conservation Genetics Resources, Volume 9 (2017) no. 1, pp. 1-4 | DOI

[103] Uno, R.; Kondo, M.; Yuasa, T.; Yamauchi, K.; Tsuruga, H.; Tamate, H. B.; Yoneda, M. Assessment of genotyping accuracy in a non-invasive DNA-based population survey of Asiatic black bears (Ursus thibetanus): lessons from a large-scale pilot study in Iwate prefecture, northern Japan, Population Ecology, Volume 54 (2012) no. 4, pp. 509-519 | DOI

[104] Vila, M.; Auger-Rozenberg, M. A.; Goussard, F.; Lopez-Vaamonde, C. Effect of non-lethal sampling on life-history traits of the protected mothGraellsia isabelae(Lepidoptera: Saturniidae), Ecological Entomology, Volume 34 (2009) no. 3, pp. 356-362 | DOI

[105] Vucicevic, M.; Stevanov-Pavlovic, M.; Stevanovic, J.; Bosnjak, J.; Gajic, B.; Aleksic, N.; Stanimirovic, Z. Sex Determination in 58 Bird Species and Evaluation of CHD Gene as a Universal Molecular Marker in Bird Sexing, Zoo Biology, Volume 32 (2013) no. 3, pp. 269-276 | DOI

[106] Waldner, T.; Traugott, M. DNA‐based analysis of regurgitates: a noninvasive approach to examine the diet of invertebrate consumers, Molecular Ecology Resources, Volume 12 (2012) no. 4, pp. 669-675 | DOI

[107] Waterhouse, B. R.; Boyer, S.; Wratten, S. D. Pyrosequencing of prey DNA in faeces of carnivorous land snails to facilitate ecological restoration and relocation programmes, Oecologia, Volume 175 (2014) no. 2, pp. 737-746 | DOI

[108] Williams, D. A.; Leach, C.; Hale, A. M.; Karsten, K. B.; Mujica, E.; Barber, D.; Linam, L. A.; Rains, N. Development of tetranucleotide microsatellite loci and a non-invasive DNA sampling method for Texas horned lizards (Phrynosoma cornutum), Conservation Genetics Resources, Volume 4 (2011) no. 1, pp. 43-45 | DOI

[109] Wisely, S.; Maldonado, J.; Fleische, R. A technique for sampling ancient DNA that minimizes damage to museum specimens, Conservation Genetics, Volume 5 (2004) no. 1, pp. 105-107 | DOI

[110] Woodruff, S. P.; Johnson, T. R.; Waits, L. P. Examining the use of fecal pellet morphometry to differentiate age classes in Sonoran pronghorn, Wildlife Biology, Volume 22 (2016) no. 5, pp. 217-227 | DOI

[111] Yannic, G.; Broquet, T.; Strøm, H.; Aebischer, A.; Dufresnes, C.; Gavrilo, M. V.; Grant Gilchrist, H.; Mallory, M. L.; Guy Morrison, R. I.; Sabard, B.; Sermier, R.; Gilg, O. Genetic and morphological sex identification methods reveal a male-biased sex ratio in the Ivory Gull Pagophila eburnea, Journal of Ornithology, Volume 157 (2016) no. 3, pp. 861-873 | DOI

Cited by Sources: