Evaluation of short-, mid- and long-term effects of toe clipping on a wild rodentBenny Borremans A D , Vincent Sluydts B , Rhodes H. Makundi C and Herwig Leirs A
A University of Antwerp, Evolutionary Ecology Group, Groenenborgerlaan 171, 2020 Antwerpen, Belgium.
B Institute of Tropical Medicine, Unit of Medical Entomology, 2000 Antwerpen, Belgium.
C Sokoine University of Agriculture, Pest Management Center, Morogoro, Tanzania
D Corresponding author. Email: firstname.lastname@example.org
Wildlife Research 42(2) 143-148 https://doi.org/10.1071/WR14109
Submitted: 3 June 2014 Accepted: 9 September 2014 Published: 3 December 2014
Context: Toe clipping is a widely used method for permanent marking of small mammals, but its effects are not well known, despite the ethical and scientific implications. Most studies do not find any clear effects, but there is some indication that toe clipping can affect survival in specific cases. Although effects on survival are arguably the most important, more subtle effects are also plausible, yet very few studies have included body condition and none has investigated effects on mobility.
Aims: We analysed the effects of toe clipping on free-living Mastomys natalensis, a common, morphologically and behaviourally intermediate small rodent.
Methods: Using a 17-year capture–mark–recapture dataset, we compared movement, body weight and survival between newly and previously clipped animals, and tested whether any of these parameters correlated with the number of clipped toes.
Key results: No evidence for a correlation between total number of clips and any of the variables was found. Newly clipped animals had a slightly smaller weight change and larger travel distance than did those that were already clipped, and we show that this is most likely due to stress caused by being captured, clipped and handled for the first time rather than to the actual clipping.
Conclusions: The combination of trapping, handling and marking has a detectable effect on multimammate mice; however, there is no evidence for a clear effect of toe clipping.
Implications: Our study suggests a re-evaluation of ethical guidelines on small-mammal experiments, so as to reach a rational, fact-based decision on which marking method to use.
Additional keywords: animal ethics, animal welfare, capture–mark–recapture, individual identification, Mastomys natalensis, permanent marking, survival.
ReferencesAmbrose, H. W. (1972). Effect of habitat familiarity and toe-clipping on rate of owl predation in Microtus pennsylvanicus. Journal of Mammalogy 53, 909–912.
| Effect of habitat familiarity and toe-clipping on rate of owl predation in Microtus pennsylvanicus.CrossRef |
Bates, D., and Maechler, M. (2012). ‘Matrix: Sparse and Dens Matrix Classes and Methods. R package Version 1.0-9.’ Available at http://Matrix.R-forge.R-project.org/ [Verified October 2014]
Bates, D., Maechler, M., and Bolker, B. (2012). ‘lme4: Linear Mixed-effects Models using S4 Classes. R package Version 0.999999-0.’ Available at http://CRAN.R-project.org/package=lme4.
Borremans, B., Hughes, N. K., Reijniers, J., Sluydts, V., Katakweba, A. A. S., Mulungu, L. S., Sabuni, C. A., Makundi, R. H., and Leirs, H. (2014). Happily together forever: temporal variation in spatial patterns and complete lack of territoriality in a promiscuous rodent. Population Ecology 56, 109–118.
| Happily together forever: temporal variation in spatial patterns and complete lack of territoriality in a promiscuous rodent.CrossRef |
Braude, S., and Ciszek, D. (1998). Survival of naked mole-rats marked by implantable transponders and toe-clipping. Journal of Mammalogy 79, 360–363.
| Survival of naked mole-rats marked by implantable transponders and toe-clipping.CrossRef |
Burnham, K. P., and Anderson, D. R. (2002). ‘Model Selection and Multimodel Inference: a Practical Information-theoretic Approach.’ (Springer: New York.)
Burt, W. H. (1943). Territoriality and home range concepts as applied to mammals. Journal of Mammalogy 24, 346–352.
| Territoriality and home range concepts as applied to mammals.CrossRef |
Calenge, C. (2006). The package adehabitat for the R software: a tool for the analysis of space and habitat use by animals. Ecological Modelling 197, 516–519.
| The package adehabitat for the R software: a tool for the analysis of space and habitat use by animals.CrossRef |
Castelhano-Carlos, M. J., Sousa, N., Ohl, F., and Baumans, V. (2010). Identification methods in newborn C57BL/6 mice: a developmental and behavioural evaluation. Laboratory Animals 44, 88–103.
| Identification methods in newborn C57BL/6 mice: a developmental and behavioural evaluation.CrossRef | 1:CAS:528:DC%2BC3cXnsFKgsbk%3D&md5=ff423e8d7c0c0afa44f1cf77262063acCAS | 19854756PubMed |
Choquet, R., Lebreton, J.-D., Gimenez, O., Reboulet, A.-M., and Pradel, R. (2009). U-CARE: utilities for performing goodness of fit tests and manipulating CApture–REcapture data. Ecography 32, 1071–1074.
| U-CARE: utilities for performing goodness of fit tests and manipulating CApture–REcapture data.CrossRef |
Dice, L. R. (1938). Some census methods for mammals. The Journal of Wildlife Management 2, 119–130.
| Some census methods for mammals.CrossRef |
Fagerstone, K. A., and Johns, B. A. (1987). Transponders as permanent identification markers for domestic ferrets, black-footed ferrets, and other wildlife. The Journal of Wildlife Management 51, 294–297.
| Transponders as permanent identification markers for domestic ferrets, black-footed ferrets, and other wildlife.CrossRef |
Fullagar, P. J., and Jewell, P. A. (1965). Marking small rodents and the difficulties of using leg rings. Journal of Zoology 147, 224–228.
| Marking small rodents and the difficulties of using leg rings.CrossRef |
Hamley, J. M., and Falls, J. B. (1975). Reduced activity in transmitter-carrying voles. Canadian Journal of Zoology 53, 1476–1478.
| Reduced activity in transmitter-carrying voles.CrossRef |
Iwaki, S., Matsuo, A., and Kast, A. (1989). Identification of newborn rats by tattooing. Laboratory Animals 23, 361–364.
| Identification of newborn rats by tattooing.CrossRef | 1:STN:280:DyaK3c%2Fkt1Wlsg%3D%3D&md5=5969e023cbb12def32dfd076d0eaa71fCAS | 2811276PubMed |
Korn, H. (1987). Effects of live-trapping and toe-clipping on body weight of European and African rodent species. Oecologia 71, 597–600.
| Effects of live-trapping and toe-clipping on body weight of European and African rodent species.CrossRef |
Laake, J. (2013). RMark: an R interface for analysis of capture-recapture data with MARK. In ‘AFSC Processed Report 2013-01’. pp. 25. Alaska Fisheries Science Center, National Marine Fisheries Service, Seattle, WA.
Lebreton, J., Burnham, K., Clobert, J., and Anderson, D. (1992). Modelling survival and testing biological hypotheses using marked animals: a unified approach with case studies. Ecological Monographs 62, 67–118.
| Modelling survival and testing biological hypotheses using marked animals: a unified approach with case studies.CrossRef |
Leclercq, G. C., and Rozenfeld, F. M. (2001). A permanent marking method to identify individual small rodents from birth to sexual maturity. Journal of Zoology 254, 203–206.
| A permanent marking method to identify individual small rodents from birth to sexual maturity.CrossRef |
Leirs, H. (1994). ‘Population Ecology of Mastomys natalensis (Smith, 1834). Implications for Rodent Control in Africa.’ Agricultural Ed. Nr35. (Belgian Administration for Development Cooperation: Brussels.)
Leirs, H., Verheyen, W., Michiels, M., Verhagen, R., and Stuyck, J. (1989). The relation between rainfall and the breeding season of Mastomys natalensis (Smith, 1834) in Morogoro, Tanzania. Annales de la Societe Royale Zoologique de Belgique 119, 59–64.
Lemon, J. (2006). Plotrix: a package in the red light district of R. R News 6, 8–12.
Lewin-Koh, N. J., and Bivand, R. (2012). ‘Maptools: Tools for Reading and Handling Spatial Objects. R Package Version 0.8-18.’ Available at http://CRAN.R-project.org/package=maptools.
Lindner, E., and Fuelling, O. (2002). Marking methods in small mammals: ear-tattoo as an alternative to toe-clipping. Journal of Zoology 256, 159–163.
| Marking methods in small mammals: ear-tattoo as an alternative to toe-clipping.CrossRef |
Metzgar, L. H. (1967). An experimental comparison of screech owl predation on resident and transient white-footed mice (Peromyscus leucopus). Journal of Mammalogy 48, 387–391.
| An experimental comparison of screech owl predation on resident and transient white-footed mice (Peromyscus leucopus).CrossRef |
Murray, D., and Fuller, M. (2000). A critical review of the effects of marking on the biology of vertebrates. In ‘Research Techniques in Animal Ecology’. (Eds L. Boitani and T. K. Fuller.) pp. 15–64. (Columbia University Press: New York.)
National Research Council of the National Academies (2011). ‘Guide for the Care and Use of Laboratory Animals.’ 8th edn. (National Research Council of the National Academies: Washington, DC.)
Ostfeld, R. S., and Heske, E. J. (1993). Sexual dimorphism and mating systems in voles. Journal of Mammalogy 74, 230–233.
| Sexual dimorphism and mating systems in voles.CrossRef |
Pavone, L., and Boonstra, R. (1985). The effects of toe clipping on the survival of the meadow vole (Microtus pennsylvanicus). Canadian Journal of Zoology 63, 499–501.
| The effects of toe clipping on the survival of the meadow vole (Microtus pennsylvanicus).CrossRef |
Peng, R. D., and Murta, A. (2012). ‘gpclib: General Polygon Clipping Library for R. R Package Version 1.5-3.’ Available at http://CRAN.R-project.org/package=gpclib.
Pradel, R. (1993). Flexibility in survival analysis from re-capture data: handling trap-dependence. In ‘Marked Individuals in the Study of Bird Population’. (Eds J. Lebreton and P. North.) pp. 29–37. (Birkhäuser: Basel, Switzerland.)
Pradel, R., Hines, J., Lebreton, J., and Nichols, J. (1997). Capture–recapture survival models taking account of transients. Biometrics 53, 60–72.
| Capture–recapture survival models taking account of transients.CrossRef |
Pradel, R., Wintrebert, C., and Gimenez, O. (2003). A proposal for a goodness-of-fit test to the Arnason–Schwarz multisite capture–recapture model. Biometrics 59, 43–53.
| A proposal for a goodness-of-fit test to the Arnason–Schwarz multisite capture–recapture model.CrossRef | 12762440PubMed |
R Core Team (2013). ‘R: a Language and Environment for Statistical Computing.’ Available at http://www.r-project.org.
Schaefer, D. C., Asner, I. N., Seifert, B., Bürki, K., and Cinelli, P. (2010). Analysis of physiological and behavioural parameters in mice after toe clipping as newborns. Laboratory Animals 44, 7–13.
| Analysis of physiological and behavioural parameters in mice after toe clipping as newborns.CrossRef | 1:CAS:528:DC%2BC3cXjvVCku7w%3D&md5=82716150c9c811658835ad9dcee3f5a2CAS | 19535388PubMed |
Sikes, R. S., and Gannon, W. L. (2011). Guidelines of the American Society of Mammalogists for the use of wild mammals in research. Journal of Mammalogy 92, 235–253.
| Guidelines of the American Society of Mammalogists for the use of wild mammals in research.CrossRef |
Sluydts, V., Davis, S., Mercelis, S., and Leirs, H. (2009). Comparison of multimammate mouse (Mastomys natalensis) demography in monoculture and mosaic agricultural habitat: implications for pest management. Crop Protection 28, 647–654.
| Comparison of multimammate mouse (Mastomys natalensis) demography in monoculture and mosaic agricultural habitat: implications for pest management.CrossRef |
Stickel, L. F. (1954). A comparison of certain methods of measuring ranges of small mammals. Journal of Mammalogy 35, 1–15.
| A comparison of certain methods of measuring ranges of small mammals.CrossRef |
Stockdale, L. G. (1932). Technique for marking rats numerically with dye. Journal of Comparative Psychology 14, 237–240.
| Technique for marking rats numerically with dye.CrossRef |
Tamarin, R., and Krebs, C. (1969). Microtus population biology. II. Genetic changes at the transferrin locus in fluctuating populations of two vole species. Evolution 23, 183–211.
| Microtus population biology. II. Genetic changes at the transferrin locus in fluctuating populations of two vole species.CrossRef |