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Toe-clipping vital to amphibian research

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Décio Tadeu Corrêa at University of Texas at Austin
Décio Tadeu Corrêa
Murilo Guimaraes at Federal University of Piauí
Murilo Guimaraes
Thiago AL Oliveira at Federal University of Rio Grande do Sul
Thiago AL Oliveira
Marcio Martins at University of São Paulo
Marcio Martins
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Sexism: measure
journal objectivity
Your initiative to address the
issue of sexism in publishing
is laudable (Nature 491, 495;
2012). But scientific editors may
be biased in other ways that
influence the publication process
— and they are not in the best
position to recognize and correct
their own biases.
An independent, external
assessment body that regularly
evaluates editorial practices
across scientific journals might
be the answer. This would
promote transparency and
reassure authors that their work
is being dealt with fairly. An
‘objectivity factor’ resulting
from such an assessment could
become a key metric of journal
performance, alongside its
impact factor.
Boyan K. Garvalov University of
Giessen, Germany.
boyan.garvalov@patho.med.uni-
giessen.de
Sexism: control
experimental bias
Implicit bias against women
(Nature 491, 495; 2012) has a
record of influencing the design
of experiments and collection of
data in the life and mind sciences.
Over the past four decades,
feminist scientists, historians
and philosophers of science
have presented case study
after case study showing how
sexist bias can distort scientific
results. Examples include
work by Rebecca Jordan-
Young on brain-organization
theory, Anne Fausto-Sterling
on the biological study of sex
differences and Anelis Kaiser on
neuroimaging.
In the interest of greater
accuracy, controls for sexist bias
need to be more rigorous.
Letitia Meynell Dalhousie
University, Halifax,
Sexism: conferences
should seek a balance
Conference committees and
symposia chairs should follow
Nature’s lead and be more open
and proactive about gender
balance (Nature 491, 495; 2012).
Publishing an online
declaration of gender-balance
policy would help. Data from each
of the past, say, three meetings
could also be posted online to
indicate the percentage of women
who were registrants, invited
plenary and keynote speakers,
session speakers, programme
committee me mbers, or session
chairs. If there is a significant gap
between the percentage of women
attending the conference and
the overall percentage of women
speakers or committee members,
then a policy overhaul may be
called for.
Jennifer L. Martin University of
Queensland, Brisbane, Australia.
j.martin@imb.uq.edu.au
Zhu Liu, Fengming Xi Institute
of Applied Ecology, Chinese
Academy of Sciences, Shenyang,
China.
liuzhu@iae.ac.cn
Dabo Guan University of Leeds,
Leeds, UK.
More trials needed to
assess sleeping pills
Sam Fleishman suggests that
the controlled use of sleeping
pills helps to counter the life-
disrupting consequences of
insomnia (Nature 491, 527;
2012). But, to our knowledge,
there is no convincing evidence
that sleep medication can
reactivate the health-restoring
functions of sleep.
Good-quality sleep improves
cognitive performance, vigilance,
memory and mood. Poor sleep
is associated with potentially
damaging physiological effects
such as inflammation (M. R.
Irwin et al. Brain Behav. Immun.
24, 54–57; 2010), compromised
immune-cell activity (E. Fondell
et al. Brain Behav. Immun. 25,
1367–1375; 2011) and telomere
shortening (A. A. Prather et al.
J.Aging Res. 2011, 721390; 2011).
However, the regular use of
sleeping pills has been linked
with increased mortality and
morbidity from infection,
depression or cancer (see, for
example, D. F. Kripke et al. BMJ
Open 2, e000850; 2012).
Large randomizing trials are
needed to evaluate the benefits
and risks of sleeping pills so that
they can be prescribed more
responsibly.
Maximilian Moser Medical
University of Graz, Austria
max.moser@medunigraz.at
Daniel F. Kripke University of
California San Diego, California,
USA.
CORRECTION
The Outlook article ‘Genetics:
Searching for answers’ (Nature
491 (suppl. 7422), S4–S6;
2012) incorrectly stated that
the Simons Simplex Collection
consists of 3,000 blood
samples taken from more than
700 people. In fact, it contains
13,000 blood samples taken
from 3,000 people.
Missing data mean
holes in tree of life
As part of the Open Tree of Life
project (http://opentreeoflife.
org), we surveyed publications
covering all domains of life and
found that most phylogenetic
trees and nucleotide alignments
from the past two decades have
been irrevocably lost.
Of 6,193 papers we surveyed
in more than 100 peer-reviewed
journals, only 17% present
accessible trees and alignments
(used to infer relatedness).
Contacting lead authors to
procure data sets was only 19%
successful. DNA sequences
were deposited in GenBank for
almost all these studies, but it is
the actual character alignments
that are pivotal for reproducing
phylogenetic analyses. We
estimate that more than 64% of
existing alignments or trees are
permanently lost.
This problem will increasingly
hinder phylogenetic inference
as the use of whole-genome data
sets becomes common. Journals
need to reinforce a policy of
online data deposition, either
as supplementary material or in
repositories such as TreeBASE
(http://treebase.org) or
Dryad (http://datadryad.org) —
including for data sets based on
previously published sequences.
Ecologists, evolutionary biologists
and others will then have access to
rigorous phylogenetics for testing
their hypotheses.
Bryan T. Drew* University of
Florida, Gainesville, USA.
bdrew@ufl.edu
*On behalf of 8 co-signatories (see
go.nature.com/gzqcr9 for full list).
Toe-clipping vital to
amphibian research
Keeping a record of the global
decline of amphibian populations
depends on the identification
and marking of individuals in the
field, commonly by toe-clipping.
This work is under threat: the
Brazilian federal government and
non-governmental organizations
want to prohibit toe-clipping
without scientific justification.
Toe-clipping is a simple,
cost-effective, minimally
invasive marking technique that
has been in use for decades in
herpetological research. The
Brazilian federal agency that
enforces environmental policies,
IBAMA, is claiming that the
practice is a form of mutilation
and should be a criminal offence
under federal law (see go.nature.
com/qkij7l; in Portuguese).
The Brazilian Herpetological
Society has protested against
this anthropocentric position
(see go.nature.com/thpwdg;
in Portuguese) on the grounds
that it would set back efforts to
understand amphibian decline.
Brazil is home to the greatest
amphibian diversity on Earth,
but knowledge of population
dynamics is scant and will
remain so without access to
reliable marking methods. We
acknowledge that toe-clipping is
not an ideal solution but, when
properly implemented, it has
minimal effects on amphibian
survival and behaviour. Without
this technique, it will be harder to
obtain crucial information that
could prevent amphibian species
from becoming extinct (W. C.
Funk et al. Nature 433, 193; 2005).
Décio T. Corrêa* State
University of Campinas, São
Paulo, Brazil.
decio.tadeu@gmail.com
Nova Scotia, Canada.
letitia.meynell@dal.ca
*On behalf of 5 co-signatories (see
go.nature.com/5sgsqo for full list).
17 JANUARY 2013 | VOL 493 | NATURE | 305
CORRESPONDENCE COMMENT
© 2013 Macmillan Publishers Limited. All rights reserved
... comm.; L. Brannelly pers. obs.; see Perry et al. 2011;Correa 2013). Although the primary purpose of ethics boards is to restrict the pain and discomfort of research animals, the perception of pain and suffering of amphibians during toe clipping is predominantly an anthropomorphized intuition (Langkilde and Shine 2006;Fisher et al. 2013), particularly after May (2004) called the practice barbaric. ...
... Although the primary purpose of ethics boards is to restrict the pain and discomfort of research animals, the perception of pain and suffering of amphibians during toe clipping is predominantly an anthropomorphized intuition (Langkilde and Shine 2006;Fisher et al. 2013), particularly after May (2004) called the practice barbaric. Even so, toe clipping remains the most widely used marking method for anurans, and has been defended by many as simple, cost-effective, having relatively minor health impacts, and the operationally best method for particular species (e.g., Phillott et al. 2007Phillott et al. , 2008Phillott et al. , 2010Phillott et al. , 2011Perry et al. 2011;Correa 2013). Moreover, it does not increase measurable distress above that experienced from handling alone (Kinkhead et al. 2006;Fisher et al. 2013). ...
... To date, no study has assessed the efficacy of these three marking methods on a single species to determine the most reliable marking method to be used in capture-mark-recapture studies. However, animal ethics boards are enforcing the use of these methods over toe clipping (Funk et al. 2005;Phillott et al. 2008;Perry et al. 2011;Correa 2013). ...
Comparison of three widely used marking techiques for adult anuran species Litoria verreauxii alpina
Article
Full-text available
  • Oct 2014
Effective marking techniques are required for both laboratory and field studies of adult amphibians, especially when individuals cannot be identified based on color or pattern. We compared the efficacy of four marking techniques: toe clipping, visual implant elastomer (VIE) tags, and passive integrative transponder (PIT) tags injected into two locations (the body cavity and subcutaneously) in the endangered Alpine Tree Frog, Litoria verreauxii alpina. The most effective marking method was toe clipping, with 96.1% correct identifications. The second best marking method was PIT tags injected subcutaneously, where tags were retained in 73.3% of animals after six weeks, but tag retention might decrease over time due to tag expulsion. PIT tags injected into the body cavity were poorly retained (33.3%). The least successful marking method was VIE tags, as individuals were correctly identified only 18.4% of the time. We conclude that toe clipping may remain the most effective marking method for some amphibian species, where modern tagging techniques are unreliable due to low tag retention and high tag movement. Researchers should conduct marking trials before implementing large scale marking schemes in unstudied species, and they should publish negative results as well as desired outcomes.
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... Esta técnica es una de las más utilizadas para marcar anuros y salamandras (6,11,12) . Sin embargo, su utilización ha generado numerosas controversias relacionadas con la ética y el bienestar animal (13,14,15) y por haberse detectado en ciertos estudios una disminución en la probabilidad de recaptura en algunas especies de anfibios (16) . Otro inconveniente reportado con el corte de falanges en los estudios a largo plazo (varios años) es la posibilidad de regeneración tisular observado en algunas especies (17,18) . ...
... Por el contrario, la técnica ha sido bien valorada por muchos estudios por considerarla como la más simple de aplicar, de bajo costo, con impactos controlables para el bienestar de los ejemplares manipulados y operativamente como la mejor o única técnica posible de aplicar para muchas especies (13,15) . Con todas las consideraciones y medidas de higiene y salud puestas en consideración, los cortes de falanges son utilizados además como fuente de ADN para estudios genéticos y para identificar enfermedades implicadas en la disminución de muchas poblaciones de anfibios (13,14) . ...
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... Frequent toe loss has been documented in some species of scincids, lacertids, and dactyloidids (Middelburg and Strijbosch 1988;Hudson 1996;Vervust et al. 2009). Finally, some consider toe-clipping to be unethical (Funk et al. 2005;May 2004;Perry et al. 2011;Corrêa 2013). ...
... On the other hand, although researchers and institutions often conclude that toe-clipping is humane (Langkilde and Shine 2006;Perry et al. 2011), others argue that it is not (May 2004). Further, public and political perception of toe-clipping is negative, and this might interfere with researchers' choice of marking technique (Mellor et al. 2004;Corrêa 2013). To minimize possible conflicts arising from concerns about toe-clipping, we suggest that photographic identification should be evaluated and adopted whenever it can be used to meet research objectives. ...
Computer-aided Individual Identification of Sceloporus consobrinus Based on Patterns of Head Scalation
Article
Full-text available
  • Dec 2017
Investigations into the ecology of lizards often require that individuals be marked for identification so that demography and life history traits can be evaluated. While toe-clipping is the most common method of individually marking lizards, it may reduce survival and be unreliable for some species. Our objective was to determine whether scalation patterns on the heads of prairie lizards (Sceloporus consobrinus) could be used to accurately identify individuals. We used a sample of alcohol-preserved specimens and the photographic identification software Interactive Individual Identification Systems (I3S) to identify individuals based on their unique patterns of scale intersections. The I3S software produces a fingerprint of each individual based on a series of points positioned by the user. For our project, these points were placed at scale intersections on the dorsal surface of the head. In our first trial, two researchers independently marked scale intersections on a random sample of 30 lizards. All of the 30 lizards were correctly matched by I3S. The second trial simulated a capture-mark-recapture study. In this trial, we had an average error rate of 7.4%. We conclude that the pattern of scale intersections on the dorsal surface of the head of prairie lizards is unique to each individual, and that I3S is a suitable alternative to toe-clipping when identifying individual prairie lizards.
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... Toe-clipping is a useful and very safe marking method in mark-recapture studies with anurans (e.g. Phillott et al. 2011;Corrêa et al. 2013). We continuously recaptured healthy marked frogs throughout the study period. ...
Jumping between narrow banks: social spacing of the stream-dwelling montane frog, Crossodactylus trachystomus (Hylodidae)
Article
Full-text available
  • Aug 2023
Spacing patterns among individuals can reveal many ecological and behavioral features, such as responses to resource availability and social organization. The study of the amphibian movements still constitutes a gap in the knowledge of the animal ecology, and the general issues of the patterns of home range are poorly known to date. Herein, we evaluated the social spacing of a small stream-dwelling frog (Crossodactylus trachystomus), an endemic species from the Espinhaço mountain range in southeastern Brazil. We found that C. trachystomus shows one of the smallest home ranges among anurans, indicating a high philopatry level. We also showed that the home range size did not differ between females and males, neither was influenced by individual body size, which reveals a possible limitation for the use of larger home ranges in riparian systems. The distribution of home ranges showed high overlap among adult males, suggesting a weak territorial behavior or a possible “dear enemy effect” for this species. Beyond expanding the knowledge about the spatial ecology and behavior of the genus Crossodactylus, our outcomes contributed to the understanding of space use and the social organization of frogs, revealing spatial patterns that can be expected for other stream-dwelling frog species.
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... The importance of reliably identifying individuals in populations to investigate species' ecology and behaviour is well documented (Wiirsig & Jefferson, 1990). However, the negative effects that accompany some methods of identification have received attention (Phillott et al., 2008;Perry et al., 2011;Corrêa, 2013). For instance, when mark-recapture surveys are carried out, artificial marking methods have often involved physical additions to the animal such as paint or tracking devices, which may affect behaviour and survival (Ferner, 1979;Lemckert, 1996;Schmidt & Schwarzkopf, 2010). ...
Effectiveness of the field identification of individual natterjack toads (Epidalea calamita) using comparisons of dorsal features through citizen science
Article
Full-text available
  • Jan 2018
  • HERPETOL J
Citizen science is now making an important contribution, both in the collection of large amounts of data over wide geographical areas and in promoting environmental awareness and engagement communities. However, as there are many participating observers, the reliability of the data collected needs to be assessed. This study used a citizen science approach to investigate whether dorsal features, when photographed, can be used in the identification of individual natterjack toads (Epidalea calamita). Epidalea calamita individuals from a population located at Prestatyn, North Wales, were captured, photographed and released in a legally compliant manner. Forty human participants each completed a timed exercise to match photographs of individual toads that had been taken from different angles. Sixty-five percent of the participants accurately matched photographs on their first attempt. The effect of training on the accuracy and speed at which participants could identify individuals from photographs was then assessed. Twenty of the participants received basic training on recognising the key features of dorsal patterns before carrying out the exercise again. Following training, average accuracy increased to 90% and participants were 41.5% quicker in completing the exercise than those that were untrained. The study revealed that basic training of participants who are involved in citizen science projects was beneficial by having a significant impact on accuracy and speed. In addition, we demonstrate that the dorsal features of tubercles and scarring are useful in identifying individuals of E. calamita in the field.
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... However, its use is currently debated as an invasive method, potentially causing infections and altering behaviors, especially for small species like hylids (Clarke 1972, Golay and Durrer 1994, Lemckert 1996, Waddle et al. 2008, Guimaraes et al. 2014. As a result, the environmental administration of the Federative Republic of Brazil has considered a ban on toe-clipping (Corrêa 2013). In contrast, the use of natural markers in photographic identification method (PIM) has gained popularity because of technological advances, being relatively inexpensive, and its noninvasive quality. ...
Treefrog lateral line as a mean of individual identification through visual and software assisted methodologies
Article
Full-text available
  • Dec 2017
Background Ecological research often requires monitoring of a specific individual over an extended period of time. To enable non-invasive re-identification, consistent external marking is required. Treefrogs possess lateral lines for crypticity. While these patterns decrease predator detection, they also are individual specific patterns. In this study, we tested the use of lateral lines in captive and wild populations of Dryophytes japonicus as natural markers for individual identification. For the purpose of the study, the results of visual and software assisted identifications were compared. Results In normalized laboratory conditions, a visual individual identification method resulted in a 0.00 rate of false-negative identification (RFNI) and a 0.0068 rate of false-positive identification (RFPI), whereas Wild-ID resulted in RFNI = 0.25 and RFNI = 0.00. In the wild, female and male data sets were tested. For both data sets, visual identification resulted in RFNI and RFPI of 0.00, whereas the RFNI was 1.0 and RFPI was 0.00 with Wild-ID. Wild-ID did not perform as well as visual identification methods and had low scores for matching photographs. The matching scores were significantly correlated with the continuity of the type of camera used in the field. Conclusions We provide clear methodological guidelines for photographic identification of D. japonicus using their lateral lines. We also recommend the use of Wild-ID as a supplemental tool rather the principal identification method when analyzing large datasets.
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... Esse tipo de marcação (batch mark) foi utilizado para que os indivíduos recapturados nas armadilhas não fossem recontados nas amostragens subsequentes. A relevância desse método de marcação de anuros em estudos populacionais foi apresentada por Corrêa et al. (2013). A procura auditiva e visual consistiu em censos efetuados no período noturno, sendo examinados os microhábitats acessíveis (e.g., bromélias, folhiço e tronco de árvores) e os sítios aquáticos utilizados pelas espécies de anfíbios durante o período reprodutivo. ...
Herpetofauna da Estação Ecológica de Bauru, um fragmento de Mata Atlântica no estado de São Paulo, Brasil
Article
Full-text available
  • Jun 2017
A herpetofauna do estado de São Paulo pode ser considerada a mais conhecida no país. No entanto, ainda existem consideráveis lacunas amostrais, sobretudo em remanescentes de vegetação natural presentes na região central do estado. Nesse contexto, o objetivo deste estudo foi gerar informações sobre a composição, riqueza e abundância de anfíbios e répteis na Estação Ecológica de Bauru, um fragmento de Mata Atlântica presente no centro-oeste do estado de São Paulo. O levantamento das espécies foi conduzido mensalmente de outubro/2007 a março/2008, totalizando 30 dias de inventário. A amostragem foi realizada por meio de armadilhas de interceptação e queda, encontro ocasional, procura auditiva e procura visual. Foram registradas 20 espécies de anfíbios pertencentes a nove gêneros e quatro famílias (Bufonidae, Hylidae, Leptodactylidae e Microhylidae) e oito espécies de répteis pertencentes a oito gêneros e sete famílias (Amphisbaenidae, Dactyloidae, Gymnophthalmidae, Mabuyidae, Teiidae, Dipsadidae e Viperidae). Este estudo contribui para ampliar o conhecimento sobre a diversidade de anfíbios e répteis na Mata Atlântica, um dos hotspots mundiais prioritários para a conservação biológica.
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... The method has been called "barbaric" (May, 2004) and is often questioned by animal ethics boards as causing unnecessary harm to study animals. Despite this criticism, it is currently the most widely used marking method for anurans, and has been defended by many because it is simple and cost effective (e.g., Phillott et al., 2007;Correa, 2013). This method has the added benefit of providing tissue for genetic analysis (Donnelly et al., 1994;Perry et al., 2011). ...
Visual implant elastomer (VIE) tags are an unreliable method of identification in adult anurans
Article
Full-text available
  • Jul 2013
  • HERPETOL J
There has long been debate over alternatives to toe-clipping as an individual marking method in anurans. Alternative methods include visible implant elastomer (VIE) tags and passive integrated transponder (PIT) tags. VIE tags are low cost, easy to insert and have been used successfully in reptiles, fish and salamanders without tag loss or movement. In this study, we tested whether two species of VIE-tagged anurans (captive Kihansi spray toads, Nectophrynoides asperginis, and leopard frogs Lithobates pipiens) experienced tag movement or loss that could lead to errors in individual identification. VIE tag movement occurred in 50% of the tags implanted which caused 70.6% of individuals to be potentially misidentified. These results demonstrate that the use of VIE tags to individually mark anurans can be highly unreliable. We therefore recommend either verifying the reliability of VIE tags through species- and life stage-specific pilot studies, or choosing another method of marking.
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... While toe clipping can have biologically negative effects on study subjects, most studies examining this method have empirically determined that toe-clipping poses little risk to most herpetofauna, if implemented correctly (Perry et al., 2011). Moreover, toe-clipping can be the best method for studies on small amphibians when few marking alternatives are available, and the information gained is relevant to conservation of that species (Correa et al., 2013;Funk et al., 2005;Grafe et al., 2011;Perry et al., 2011;Swanson et al., 2013). All field workers received the same training in field protocols and field workers changed over time. ...
Spatial and temporal variation in population dynamics of Andean frogs: Effects of forest disturbance and evidence for declines
Article
Full-text available
  • Jul 2014
Biodiversity loss is a global phenomenon that can result in the collapse of food webs and critical ecosystem services. Amphibian population decline over the last century is a notable case of species loss because amphibians survived the last four major extinction events in global history, their current rate of extinction is unprecedented, and their rate of extinction is greater than that for most other taxonomic groups. Despite the severity of this conservation problem and its relevance to the study of global biodiversity loss, major knowledge gaps remain for many of the most threatened species and regions in the world. Rigorous estimates of population parameters are lacking for many amphibian species in the Neotropics. The goal of our study was to determine how the demography of seven species of the genus Pristimantis varied over time and space in two cloud forests in the Ecuadorian Andes. We completed a long term capture–mark–recapture study to estimate abundance, survival, and population growth rates in two cloud forests in the Ecuadorian Andes; from 2002 to 2009 at Yanayacu in the Eastern Cordillera and from 2002 to 2003 at Cashca Totoras in the Western Cordillera. Our results showed seasonal and annual variation in population parameters by species and sex. P. bicantus experienced significant reductions in abundance over the course of our study. Abundance, apparent survival, and population growth rates were lower in disturbed than in primary or mature secondary forest. The results of our study raise concerns for the population status of understudied amphibian groups and provide insights into the population dynamics of Neotropical amphibians.
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Manual de técnicas y protocolos para el relevamiento y estudio de anfibios de Argentina - Parte I
Book
Full-text available
  • Nov 2021
El objetivo principal de este Manual es el desarrollo de un compendio de técnicas y protocolos estándares para el inventario y monitoreo de poblaciones de anfibios, actualizado con los procedimientos, herramientas y técnicas de análisis más recientes y adaptado a las condiciones y realidades nacionales. Su contenido está destinado a ayudar a superar algunas de las dificultades que se pueden enfrentar al configurar un programa de inventario y monitoreo para anfibios. Pretendemos brindar una orientación práctica sobre cómo diseñar y llevar a cabo estudios que puedan servir para múltiples aplicaciones más allá de las necesidades de un proyecto particular. En este manual compilamos las experiencias y consejos de numerosos especialistas sobre diferentes temáticas que pudieran permitir a los lectores y usuarios de este manual obtener la mayor cantidad y calidad de datos durante la realización de futuros proyectos de investigación relacionados con estas temáticas.
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