Nº 66, Janeiro-Dezembro de 2013
Diogo Loretto1,2,*, Marcelo Weksler1,3, Ana Lazar1,4, Alexandre R. Percequillo1,5, Cibele R. Bonvicino1,6,
José L. Cordeiro1,7, Alexandra M.R. Bezerra8, Ana P. Carmignotto9, Ana C. Delciellos2, André F. Testoni10,
Carlos E.V. Grelle2, Diego Astúa11, Eleonore Z.F. Setz12, Emerson M. Vieira13, Fabiano Melo14, Jayme A. Prevedello2,
Jorge R. Marinho15, Julio C. Voltolini16, Maja Kajin17, Mariana Ferreira2, Martín R. Alvarez18, Matheus F. Dalloz2,
Maurício E. Graipel19, Mônica Aragona20, Monica Perissé21, Natalie Olifiers4, Paula Ferreira2, Paulo S. D’Andrea4,
Priscilla L. Zangrandi2, Renato Crouzeilles2, Ricardo Moratelli7, Ricardo T. Santori22, Rosana Gentile4,
Rui Cerqueira2, Susi M. Pacheco23, Suzy E. Ribeiro2, Vitor Rademaker24
Ensaio
On the practice of toe clipping for small mammal
studies in Brazil
Diretoria da Sociedade Brasileira de Mastozoologia, Departamento de Ecologia, Instituto de Biologia, Universidade Federal do Rio de Janeiro – UFRJ.
Avenida Carlos Chagas Filho, 373, sala A2‑084, Bloco A, Cidade Universitária, CEP 21941‑902, Rio de Janeiro, RJ, Brasil.
2 Laboratório de Vertebrados, Departamento de Ecologia, Instituto de Biologia, Universidade Federal do Rio de Janeiro – UFRJ.
Avenida Carlos Chagas Filho, 373, sala A2‑084, Bloco A, Cidade Universitária, CEP 21941‑902, Rio de Janeiro, RJ, Brasil.
3 Departamento de Zoologia, Instituto de Biociências, Universidade Federal do Estado do Rio de Janeiro – UNIRIO.
Avenida Pasteur, 458, Urca, CEP 22290‑255, Rio de Janeiro, RJ, Brasil.
4
Laboratório de Biologia e Parasitologia de Mamíferos Silvestres Reservatórios, Pavilhão Lauro Travassos, Fundação Instituto Oswaldo Cruz – FIOCRUZ.
Avenida Brasil, 4.365, Manguinhos, CEP 21040‑900, Rio de Janeiro, RJ, Brasil.
5 Escola Superior de Agricultura “Luiz de Queiroz” da Universidade de São Paulo – ESALQ.
Avenida Pádua Dias, 11, São Dimas, CEP 13418‑900, Piracicaba, SP, Brasil.
6
Divisão de Genética, Instituto Nacional de Câncer – INCA. Rua André Cavalcanti, 37, Centro, 4º andar, CEP 20231‑050, Rio de Janeiro, RJ, Brasil.
7 Campus Fiocruz Mata Atlântica, Pavilhão Agrícola – FIOCRUZ. Estrada Rodrigues Caldas, 3.400, Taquara, Jacarepaguá, CEP 22713‑375,
Rio de Janeiro, RJ, Brasil.
8 Departamento de Zoologia, Instituto de Ciências Biológicas, Universidade de Brasília – UnB, Campus Universitário Darcy Ribeiro.
Asa Norte, CEP 70910‑900, Brasília, DF, Brasil.
9
Laboratório de Diversidade Animal, Departamento de Biologia, Centro de Ciências e Tecnologias aplicadas à Sustentabilidade,
Universidade Federal de São Carlos – UFSCar, Campus Sorocaba. Rodovia João Leme dos Santos (SP‑264), s/n, km 110, sala ATLAB‑115,
Bairro Itinga, CEP 18052‑780, Sorocaba, SP, Brasil.
10ECOAMA Consultoria e Assessoria Ambiental. Rua Silvano Cândido da Silva Sênior, 245, Sala 03, Ponta Aguda, CEP 89050‑280, Blumenau, SC, Brasil.
11Laboratório de Mastozoologia, Departamento de Zoologia, Universidade Federal de Pernambuco – UFPE. Avenida Professor Moraes Rego, s/n,
Cidade Universitária, CEP 50740‑465, Recife, PE, Brasil.
12Laboratório de Ecologia e Comportamento de Mamíferos – LAMA, Departamento de Biologia Animal, Instituto de Biologia,
Universidade Estadual de Campinas – UNICAMP. Rua Monteiro Lobato, 255, Cidade Universitária, CEP 13083‑862, Campinas, SP, Brasil.
13Laboratório de Ecologia de Vertebrados, Departamento de Ecologia, Instituto de Ciências Biológicas, Universidade de Brasília – UnB,
Campus Universitário Darcy Ribeiro. Asa Norte, CEP 70910‑900, Brasília, DF, Brasil.
14
Departamento de Ciências Biológicas, Campus Jataí, Universidade Federal de Goiás – UFG. BR‑364, km 192, Parque Industrial, CEP 75801‑615,
Jataí, GO, Brasil.
15
Departamento de Ciências Biológicas, Universidade Regional Integrada – URI, Campus de Erechim. Avenida Sete de Setembro, 1.621,
Bairro Fátima, CEP 99700‑000, Erechim, RS, Brasil.
16Grupo de Pesquisa e Ensino em Biologia da Conservação – ECOTROP, Departamento de Biologia, Universidade de Taubaté – UNITAU.
Avenida Tiradentes, 500, Jardim das Nações, CEP 12030‑010, Taubaté, SP, Brasil.
17Instituto de Biologia Roberto Alcântara Gomes – IBRAG, Departamento de Ecologia, Universidade do Estado do Rio de Janeiro – UERJ.
Rua São Francisco Xavier, 524, Maracanã, CEP 20550‑900, Rio de Janeiro, RJ, Brasil.
18Departamento de Ciências Biológicas, Universidade Estadual Santa Cruz – UESC. Rodovia Jorge Amado, km 16, Salobrinho, CEP 45662‑900,
Ilhéus, BA, Brasil.
19Departamento de Ecologia e Zoologia, Centro de Ciências Biológicas, Universidade Federal de Santa Catarina – UFSC, Campus Universitário.
Rua Roberto Sampaio Gonzaga, s/n, Trindade, CEP 88040‑900, Florianópolis, SC, Brasil.
20Centro de Referência da Biodiversidade Regional, Departamento de Botânica e Ecologia, Instituto de Biociências,
Universidade Federal de Mato Grosso – UFMT. Avenida Fernando Corrêa da Costa, 2.367, Boa Esperança, CEP 78060‑900, Cuiabá, MT, Brasil.
21Rua Raul Veiga, 389/202 B, Centro, CEP 28907‑090, Cabo Frio, RJ, Brasil.
22Faculdade de Formação de Professores, Universidade do Estado do Rio de Janeiro – UERJ. Rua Doutor Francisco Portela, 1.470, Patronato,
CEP 24435‑005, São Gonçalo, RJ, Brasil.
23Instituto Sauver. Avenida Pernambuco, 2.623/404, Floresta, CEP 90240‑005, Porto Alegre, RS, Brasil.
24SARUÊ Consultoria, Pesquisa & Desenvolvimento. Rua Lúcio de Mendonça, 27/101, Maracanã, CEP 20270‑040, Rio de Janeiro, RJ, Brasil.
*[email protected]
1
On November 8th, 2012, the Brazilian Ministry of
Environment (MMA), through The Chico Mendes Institute of Biodiversity Conservation (ICMBio/MMA), issued
the Circular Letter no. 01/2012/COINF/CGPEQ/DIBIO,
regarding toe clipping as a method of individual identification for studying small mammals, and requested
expert opinion on the subject. We provide below the
response we submitted to the Ministry, which is the
official position of the Brazilian Society of Mammalogists
(SBMz) on the subject.
The study of population ecology, especially of small
non-volant mammals (rodents and marsupials, orders
Rodentia and Didelphimorphia), depends mainly on
monitoring individuals to understand ecological patterns and processes, originated both from natural or
anthropogenic factors. There are two basic methods
1
Ensaio
Nº 66, Janeiro-Dezembro de 2013
2
to efficiently monitor animal populations in the wild,
namely static life history tables or dynamic cohort tables (Begon et al. 2006). The first requires information
of representative population samples in a given locality
and time interval, so that age classes can be estimated.
This method is commonly used to study species with
long lifespan, mostly diurnal, and relatively easy to find
in their natural habitats.
The second option, dynamic cohort tables, requires
regular monitoring of individuals in the population from
birth to death (e.g., Fernandez 1995, Gentile et al. 2000,
Flowerdew et al. 2004, Macedo et al. 2006). This approach is commonly used to study short lifespan species
(one or a few years), such as small non-volant mammals
(e.g., rodents and marsupials), and represent an important tool in the study of life histories, population dynamics, and classic and evolutionary demography. Pivotal to
this approach, it requires precise individual recognition
of specimens through durable body marking.
Among the several methods available for marking
small non-volant mammals (e.g., Korn 1987, Wood &
Slade 1990, Braude & Ciszek 1998, Meserve et al. 2003,
Fisher & Blomberg 2009) the most widely used recently
in Brazil are ear tagging and toe clipping (e.g., Macedo
et al. 2007, Schmitz 2008, Bonecker et al. 2009). Regarding the latter, it is imperative to clarify that mammalogists do not cut entire toes while applying toe clipping.
We avoid the use of “toe ablation” because it can lead
to misinterpretations. Brazilian mammalogists cut distal
phalanges to individually identify animals.
Scientific papers, testimonies, and reports from
experts indicate that toe clipping method is effective as
an ultimately body marking (Carmignotto A.P., Graipel
M.E., Vieira E.M., Voltolini J.C., Testoni A., pers. obs.),
but it does not cause irreversible harm to the health of
the animals (Schmitz 2008, Fisher & Blomberg 2009).
The method is effective for studying species with different life histories (semifossorial, aquatic, and terrestrial)
in the field (Schmitz 2008). Indeed, there are several
studies showing that toe clipping (i) does not influence
recapture rates (Voltolini et al. 1996), nor (ii) decreases
survival rates of individuals (e.g., Wood & Slade 1990,
Kajin et al. 2008, Schmitz 2008, Fisher & Blomberg 2009),
and that there is complete healing of toes tips (Gentile
R., Graipel M.E., Vieira E.M., Testoni A., pers. obs.).
Like any other available method of individual marking, toe clipping may cause some loss of information, due
to the occurrence of natural toe loss. Losing information represents a serious problem: it affects estimates,
results, and predictive power of studies. Nonetheless,
our experience, as field Mammalogists, points the use of
toe clipping can be advantageous over other methods,
such as ear tagging, as this method can reach 20‑70%
higher rates of loss of information (Carmignotto A.P.,
Graipel M.E., pers. obs.). However, ear tagging can also
achieve low rates of loss marking (e.g., 3.8%; Cerqueira
R., unpublished data). Indeed, to reduce loss rates to
extremely low levels, individuals should have both ears
tagged. Double marking has been applied successfully in
the long-term population study (1997‑2013) conducted
by the Laboratório de Vertebrados at Federal University
of Rio de Janeiro (UFRJ), in Serra dos Órgãos National
Park, Rio de Janeiro state. In this study, only 0.7% of
double ear tagged individuals lost both tags between
trapping sessions (Cerqueira, R., pers. obs., data from
Macedo 2007, Macedo et al. 2007, Kajin et al. 2008, Ferreira 2011, Santana 2012).
An important issue regarding toe clipping refers to
marsupial neonates. Rodent neonates are seldom captured, but marsupial females are commonly captured
with pouch young. In this case, toe clipping is the only
available method for individual identification of the litter members, with minimum harm to neonates (from
20 mm body length; Fisher & Blomberg 2009). For example, over a nine-year population study of the common Atlantic Forest opossum (Didelphis aurita WiedNeuwied, 1826; Didelphimorphia, Didelphidae), toe
clipping revealed unknown aspects of its ecology and
natural history (Kajin 2008, Kajin et al. 2008). Among
them, authors identified the weaning stage as the most
critical moment in the species’ life cycle, when selective
pressures are more intense (Kajin 2008, see also Ferreira
et al., in press). Toe clipping allowed accurate estimation
of survival rates, thus providing reliable estimates of the
opossum population growth or decline. The results are
highlighted as a potential generalized hypothesis for
most other Neotropical marsupial species. To our knowledge, there are no alternative efficient methods available for individually marking neonate marsupials, since
the use of microchips or ear tags would not be suitable
for such small animals (20‑80 mm body length). Therefore, toe clipping is the only marking option for several
ongoing studies in Brazil, which address issues concerning ecology, philopatry, use of space, life history and demography of small mammals.
The scientific community must always seek alternatives to minimize or eliminate any discomfort or stress
caused to animals manipulated in field studies, in accordance with the 3Rs (reduction, refinement and replacement) of animal welfare (www.nc3rs.org.uk/page.
asp?id=7). SBMz and coauthors of this letter argue that
the toe clipping method must not be eliminated from
the Brazilian mammalogy, but the use of alternative,
less invasive methods, such as tattoos, ear tags, and microchips should be considered whenever possible. The
most important reason for keeping the use of toe clipping is its uniqueness for individual marking of marsupial
pouch young and its effectiveness as a marking tool for
other small mammals (up to 100 g body weight). We also
stress the need to comply with several fundamental requisites when performing toe clipping:
— Surgical instruments must be sterilized before toe
clipping, and cicatrizing agent must be applied
afterwards. When the method is applied to adult
animals (less than 100 g), we also recommended
previous disinfection and, if possible, application of
an anesthetic spray.
— Toe clipping should be used only in animals below
100 g of body weight (Cerqueira, R., pers. comm.).
In larger animals, other individual marking techniques must be used, unconditionally.
— Only one (01) distal phalanx per member may be
cut, and a maximum of two (02) phalanges per individual should be cut to achieve the number combination needed;
— Under no circumstances marsupials’ opposable
thumbs should be cut, because it would affect animals’ ability to climb;
— The use of toe clipping and ear tagging in fossorial or semifossorial species, such as rodents of the
genus Blarinomys Thomas, 1896 (Rodentia, Cricetidae) still need to be evaluated, because such techniques may hinder the ability of animals to dig.
For demographic studies, entire offspring can be
marked with a single combination of clipped toes, without loss of information, since weaned juveniles receive
other individual marks, such as ear tags or microchips,
when recaptured in future opportunities. It ensures the
recognition of parental relationship, and increases the
number of litters that can be concomitantly marked.
Finally, the Brazilian Society of Mammalogists, and
coauthors who signed this letter, are extremely favorable to the implementation of a public forum, chaired
by ICMBio/MMA, for further debates on issues involving
the knowledge, welfare, ethics, and the study of mammals in Brazil. As the principal interested parties in these
subjects, the community of Brazilian mammalogists is
committed with, and should be involved as active participants on these debates.
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