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Abstract

We wish that B. A. Minteer et al. 's claim that field biologists routinely collect voucher specimens were true [“Avoiding (re)extinction,” Perspectives, 18 April, p. [260][1]]. Any museum curator will tell you that it is a constant struggle to convince them to do so, despite countless
23 MAY 2014 • VOL 344 ISSUE 6186 815SCIENCE sciencemag.org
and understood. Specimens from such
collections and their associated data are
essential for making informed decisions
about management and conservation now
and in the future. As a community, we
advocate the utmost responsibility and
care while making scientific collections
(4). Furthermore, given increasing rates
of habitat loss and global change, we
believe that responsibly collecting voucher
specimens and associated data and openly
sharing this knowledge (for example,
through GBIF, iDigBio, and VertNet) are
more necessary today than ever before.
L. A. Rocha,1* A. Aleixo,2 G. Allen,3 F.
Almeda,1 C. C. Baldwin,4 M. V. L. Barclay,5
J. M. Bates,6 A. M. Bauer,7 F. Benzoni,8
C. M. Berns,9 M. L. Berumen,10 D. C.
Blackburn,1 S. Blum,1 F. Bolaños,11 R.
C. K. Bowie,12 R. Britz,5 R. M. Brown,13
C. D. Cadena,14 K. Carpenter,15 L. M.
Ceríaco,16 P. Chakrabarty,17 G. Chaves,11
J. H. Choat,18 K. D. Clements,19 B. B.
Collette,20 A. Collins,20 J. Coyne,21 J.
Cracraft,22 T. Daniel,1 M. R. de Carvalho,23
K. de Queiroz,4 F. Di Dario,24 R. Drewes,1
J. P. Dumbacher,1 A. Engilis Jr.,25 M.
V. Erdmann,26 W. Eschmeyer,1 C. R.
Feldman,27 B. L. Fisher,1 J. Fjeldså,28 P.
W. Fritsch,1 J. F uchs, 29 A. Getahun,30 A.
Gill,31 M. Gomon,32 T. Gosliner,1 G. R.
Graves,4 C. E. Gr iswold,1 R. Guralnick,33
K. Hartel,34 K. M. Helgen,4 H. Ho, 35 D. T.
Iskandar,36 T. Iwamoto,1 Z. Jaafar,4,37 H.
F. James,4 D. Johnson,4 D. Kavanaugh,1
N. Knowlton,4 E. Lacey,12 H. K. Larson,38
P. La st ,39 J. M. Leis,40 H. Lessios,41 J.
Liebherr,42 M. Lowman,1 D. L. Mahler,25
V. Mamonekene,43 K. Matsuura,44 G. C.
Maye r,45 H. Mays Jr.,46 J. McCosker,1
R. W. McDiarmid,4 J. M cGuir e,12 M. J.
Miller,41 R. Mooi,1 R. D. Mooi,47 C. Moritz,48
P. My er s, 49 M. W. Nachman,12 R. A.
Nussbaum,49 D. Ó Foighil,49 L. R. Parenti,4
J. F. Parham,50 E. Pau l,51 G. Paulay,52 J.
Pérez-Emán,53 A. Pérez-Matus,54 S. Poe,55
J. Pogonoski,39 D. L. Rabosky,49 J. E .
Randall,56 J. D. Reimer,57 D. R. Robertson,41
M.-O. Rödel,58 M. T. Rodrigues,23 P.
Roopnarine,1 L. Rüber,59 M. J. Ryan,55 F.
Sheldon,17 G. Shinohara,44 A. Short,13 W.
B. Simison,1 W. F. Smith-Vaniz,52 V. G.
Springer, 4 M. Stiassny,22 J. G. Tello,22,60 C.
W. Thompson,49 T. Trn sk i,61 P. Tu ck e r,49
T. Valqui,62 M. Vecchione,20 E. Verheyen,63
P. C. Wainwright,25 T. A. Wheeler,64 W.
T. White,39 K. Will,12 J. T. Williams,4 G.
Williams,1 E. O. Wilson,34 K. Wi nke r,65 R.
Winterbottom,66 C. C. Witt55
1California Academy of Sciences, San Francisco, CA
94118, USA. 2Museu Paraense Emílio Goeldi, Belém,
PA, 66040 -170, Brazil. 3Western Australian Museum,
Perth, WA, 6986, Aust ralia. 4Smithsonian Institution,
Washin gton, DC 20 560, USA. 5Natural History
Museu m, London, SW 7 5BD, UK. 6Field Museum of
Natural History, Chicago, IL 60605, USA. 7Villanova
University, Villanova, PA 19085, USA. 8University of
Milano-Bicocca, Milan, 20126, Italy. 9Utica College,
Utica , NY 13502, USA. 10 King Abdullah University
of Science and Technology, Thuwal, 23955, Saudi
Arabia. 11Universidad de Costa Rica, San José,
11501-2060, Costa Rica. 12University of California,
Berkeley, CA 94720–3161, USA. 13University of
Kansas, Lawrence, KS 66045, USA. 14Universidad de
los Andes, Bogotá, 4976, Colombia. 15Old Dominion
University, Norfolk, VA 23529, USA. 16Museu Nacional
de História Natural e da Ciência, Lisbon, 7005-
638, Portugal. 17Louisiana State University, Baton
Rouge, LA 7 0803, USA. 18James Cook University,
Townsville, 4811, Australia. 19University of Auckland,
Auckland, 1142, New Zealand. 20NOAA Systematics
Labo ratory, Washing ton, DC 200 13, USA. 21University
of Chicago, Chicago, IL 60637, USA. 22American
Museum of Natural History, New York, NY 10024,
USA. 23Universidade de São Paulo, São Paulo, SP,
05508-090, Brazil. 24Universidade Federal do Rio de
Janeiro, Macaé, RJ, 27965-045, Brazil. 25University
of California, Davis, CA 95616, USA. 26Conservation
International, Denpasar, Bali, 80235, Indonesia.
27University of Nevada, Reno, NV 89557–0314, USA.
28Natural History Museum of Denmark, Copenhagen,
DK-2100, Denmark. 29Muséum National d’Histoire
Naturelle, Paris, 75005, France. 30Addis Ababa
University, Addis Ababa, 1176, Ethiopia. 31University
of Sydn ey, Sydney, NSW, 2006, Austra lia. 32Museum
Victoria, Melbourne, 3001, VIC, Australia. 33University
of Colorado, Boulder, CO 80309–0334, USA.
34Harvard University, Cambridge, MA 02138, USA.
35National Museum of Marine Biology & Aquarium,
Pingtung, 944, Taiwan. 36Institut Teknologi Bandung,
Bandung, 40132, Indonesia. 37National University
of Singapore, 117543, Singapore. 38Museum and Art
Gallery of the Northern Territory, Darwin, 0820, NT,
Australia. 39CSIRO Marine & Atmospheric Research,
Hobart, TAS, 7000, Australia. 40Australian Museum,
Sydney, NSW, 2010, Aus tralia. 41Smithsonian
Tropical Research Institute, Balboa, 0843-03092,
Panamá. 42Cornell University, Ithaca, NY 14853, USA.
43Université Marien Ngouabi, Brazzaville, B.P. 69,
Republic of Congo. 44National Museum of Nature
and Science, Tsukuba, 305-0005, Japan. 45University
of Wisconsin-Parkside, Kenosha, WI 53141–2000,
USA. 46Cincinnati Museum Center, Cincinnati, OH
45203, US A. 47The Manitoba Museum, Winnipeg,
MB, R3B 0N2, Canada. 48Australian National
University, Canberra, ACT, 0200, Australia.
49University of Michigan, Ann Arbor, MI 48109–1079,
USA. 50California State University, Fullerton, CA
92831, USA. 51The Ornithological Council, Chevy
Chase, MD 20815, USA. 52University of Florida,
Gainesville, FL 32611, USA. 53Universidad Central
de Venezuela, Caracas, 1041, Venezuela. 54Ponti cia
Universidad Católica de Chile, Santiago 6513677,
Chile. 55University of New Mexico, Albuquerque,
NM 871 31–0001, USA . 56Bernice P. Bishop
Museum, Honolulu, HI 96817, USA. 57University
of the Ryukyus, Nishihara, 903-0213, Japan.
58Museum für Naturkunde, Berlin, 10115, Germany.
59Naturhistorisches Museum der Burgergemeinde
Bern, Bern, CH-3005, Switzerland. 60Long Island
University, Brooklyn, NY 11201–8423, USA.
61Auckland Museum, Auckland, 1142, New Zealand.
62Centro de Ornitologia y Biodiversidad, Lima, 33,
Peru. 63Royal Belgian Institute of Natural Sciences,
Brussels, 1000, Belgium. 64McGill University,
Montreal, QC, H9X 3V9, Canada. 65University of
Alas ka Museum , Fairb anks, AK 99775, US A. 66Royal
Ontario Museum, Toronto, ON, M5S 2C6, Canada.
*Corresponding author. E-mail: LRocha@
calacademy.org
REFERENCES
1. E. Fulle r, The Great Auk (H. N. Abrams, New York, 1999).
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Specimen collection:
Plan for the future
WE WISH THAT B. A. Minteer et al.’s claim
that field biologists routinely collect
voucher specimens were true [“Avoiding
(re)extinction,” Perspectives, 18 April,
p. 260]. Any museum curator will tell you
that it is a constant struggle to convince
them to do so, despite countless publications
rendered unreliable because it is impossible
to verify species’ identities. The necessity
of voucher specimens varies by taxon and
region, but in general, it is good practice to
deposit them and as much data as possible,
including DNA and photos in life.
We certainly do not wish to see any
species driven to extinction by overcollect-
ing, but submit that this is rare and more
associated with commercial or ardent,
recreational overcollecting than sensible
scientific vouchering (1, 2). If the kill of
a single individual increases the extinc-
tion risk of a species, then it is well below
viable population size and already among
the “walking dead.
Dawkins’ description of evolution
as improbability on a colossal scale is
nowhere more evident than in morphol-
ogy. Whether or not a species survives,
museum specimens represent a window
on many of its most remarkable novel-
ties. Molecular data, although helpful in
identifications, is neither a panacea nor
surrogate for museum specimens, espe-
cially when it comes to newly discovered
species. Describing a new species without
depositing a holotype when a specimen
can be preserved borders on taxonomic
malpractice. Even given good photographs
and a tissue sample, there are reasons to
collect one or more complete specimens.
We do not know what morphological
characters will prove important in future
studies of species status, phylogenetic
Published by AAAS
INSIGHTS |
LETTERS
816 23 MAY 2014 • VOL 344 ISSUE 6186 sciencemag.org SCIENCE
relationships, or genetic or epigenetic
variation. As taxonomists and ecologists,
we do not want to know only that a spe-
cies exists but to understand what makes
it unique compared to related species.
Given the importance of the phenotype-
environment interface in natural selection,
we potentially sacrifice the most impor-
tant things to know about a species when
we forego more than superficial evidence
of anatomical details.
With millions of species threatened by
extinction, it would be tragic were we left
with no more than a few photographs and
sequences as evidence they were once here.
Given well-preserved specimens, we can
continue to marvel at adaptations, discover
models for biomimicry, refine theories of
character transformations, and verify the
state of internal or external structures
discovered in related species. As the last
generation with the opportunity to explore,
discover, and document millions of species
evolved over billions of years, we should
not be so arrogant as to assume what sci-
ence of the future may want or need.
Frank-T. Krell1 and Quentin D. Wheeler2
1Department of Zoology, Denver Museum of Nature
& Science, Denver, CO 80205, USA. 2College
of Environmental Science and Forestry, State
University of New York, Syracuse, NY 13210, USA.
*Corresponding author. E-mail: frank.krell@dmns.org
REFERENCES
1. D. A. Norton et al., Tax on 43, 181 (1994).
2. K. Winker et al., Auk 127, 690 (2010).
Response
THE PURPOSE OF OUR Perspective was
to raise awareness about an issue that
will increase in prevalence as the global
biodiversity crisis unfolds: Absent a
reliable estimate of population size, is
it prudent and ethical to collect a newly
observed individual of a species so rare it
was thought extinct [e.g., (1)]? We sup-
port the work of natural history museums,
and nowhere in our discussion did we
argue that responsible collecting should
be halted. Specimen collections provide
invaluable contributions to many dis-
ciplines beyond taxonomy [e.g., (2, 3)];
moreover, we continue to collect ourselves
(J.P.C. and R.P.). We repeatedly emphasized
that we were targeting the specific context
of small and vulnerable populations only.
We would like to believe that we live in
Rocha et al.’s world in which the respon-
sible collector follows every regulation and
ethical code (where these exist). Our own
experience and research, however, paint
a more complicated picture. A culture of
responsible scientific practice is harder to
establish than just following regulatory
prescriptions and ethical injunctions (4).
Rocha et al. also introduce a red herring by
raising the distinction between individual-
and population- or species-level concern
in conservation, which we understand
and have discussed elsewhere (5). It is
obvious that our Perspective concerns
survival of populations and species; the
individual specimen becomes important in
our argument because of the small size of
populations, especially when (as in the case
of rediscovered amphibian populations)
such individuals are found coexisting with
the lethal pathogen that likely greatly
reduced their numbers (6).
Nowhere do we claim that scientific
collection is a leading driver of extinction.
We are aware of the major threats posed by
habitat loss and fragmentation, commer-
cial use, exotic species, toxins, infectious
diseases, and climate change (7). Collectors
may have taken the last Auks, but the spe-
cies was pushed to the brink of extinction
by centuries of human overexploitation.
Still, the point remains that without a reli-
able estimate of population size, collecting
individuals from a small, isolated popula-
tion can pose an extinction risk. We believe
that it is important to highlight this risk,
and to suggest how to mitigate the threat.
We are troubled by Krell and Wheeler’s
argument, which seems to suggest that col-
lecting in vulnerable populations is justified
as a way to preserve the present for a future
in which many species will be extinct. Even
small populations seem eligible for collect-
ing based on their claim that such species
are already among the “walking dead.” If
collecting a specimen increases extinction
risk, however, then it is a threat to biodi-
versity and should be avoided. Krell and
Wheeler object to the “arrogance” of assum-
ing “what science of the future may want
or need,” but we find more hubris in their
suggestion that taxonomists and ecologists
should be unconcerned about driving the
final nail in a species’ coffin.
Cultural change in science can be dif-
ficult. Long-established techniques are
questioned as alternatives arise. Specimen
collection is no exception, especially in
light of growing concerns about our enter-
ing a sixth mass extinction event (8), and
we encourage more research into new
ways to document Earth’s biodiversity.
A precautionary approach to scientific
collection will help ensure that we do not
put additional pressure on already vulner-
able populations as we seek to identify
organisms new to science, or to confirm a
species’ welcome return from the dead.
Ben A. Minteer,1* James P. Collins,1
Robert Puschendorf 2
1School of Life Sciences, Arizona State University,
Tempe, AZ 85287, USA. 2School of Biological
Sciences, Plymouth University, Drake Circus,
Plymouth, Devon PL4 8AA, UK.
*Corresponding author. E-mail: ben.minteer@asu.edu
REFERENCES
1. IUCN Red List of Threatened Species, Craugastor
fleischmanni (www.iucnredlist.org/details /56603/0).
2. C. Moritz et al., Science 322, 261 (2008).
3. R. Puschendorf, F. Bolaños, G. Chaves, Biol. Conserv. 132,
136 (2006).
4. B. A. Mint eer, J. P. Col lins, Sci. Eng. Ethics 14, 483 (2008).
5. B. A. Min teer, J. P. Collins, I LAR J. 54, 41 (2013).
6. M. J. Ryan, F. Bol años, G. C haves, Sci ence (2010);
published online: www.sciencemag.org/content/329/
59 9 7/1 2 72 /r e pl y.
7. J. P. Collin s, M. Cr ump, Extinction in Our Times: Global
Amphibian Decline (Oxford Univ. Press, Oxford, 2009).
8. E. Kolb ert, The Sixth Extinction: An Unnatural History
(Henry Holt, New York, 2014).
ERRATA
Editor’s note: We are simplifying our proce-
dure for making corrections to articles pub-
lished in Science, while maintaining transpar-
ency for our readers. The full text and PDF
les will be corrected online as soon as pos-
sible, with an explanation at the end of the
full text and, for corrections involving data or
metadata, in an accompanying online Erra-
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published online will appear in a subsequent
print issue in this space.
Erratum for the Research Article: “Total
Synthesis of a Functional Designer Eukaryotic
Chromosome” by N. Annaluru et al., Science
344, 1254596 (2014). Published online 18 April;
10.1126/science.1254596
Erratum for the Report: “Wild Pollinators
Enhance Fruit Set of Crops Regardless of
Honey Bee Abundance” by L. A. Garibaldi et al.,
Science 344, 1255213 (2014). Published online 2
May; 10.1126/science.1255213
Erratum for the News & Analysis: “Designer
Microbes Expand Life’s Genetic Alphabet”
by R. F. Service, Science 344, 1255780
(2014). Published online 16 May; 10.1126/
science.1255780
Erratum for the Report: “I-Love-Q: Unexpected
Universal Relations for Neutron Stars and
Quark Stars” by K. Yagi and N. Yunes, Science
344, 1250349 (2014). Published online 23 May;
10.1126/science.1250349
Erratum for the Report: “Mapping the
Cellular Response to Small Molecules Using
Chemogenomic Fitness Signatures” by A. Y. Lee
et al., Science 344, 1255771 (2014). Published
online 23 May; 10.1126/science.1255771
Published by AAAS
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... It is important to mention that approaches that promote taking the publication of images from databases and photo-based descriptions as a replacement to species descriptions based on type specimen(s) are misguided (Marshall & Evenhuis 2015). Such approaches functionally dismiss the most important biological empirical evidence, the specimen(s) itself (Amorim et al. 2016;Krell & Wheeler 2014). Biodiversity inventory websites must assist in the publication of taxonomic descriptive work abiding the International Code of Zoological Nomenclature rules (ICZN 1999). ...
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Spider community inventories have relatively well-established standardized collecting protocols. Such protocols set rules for the orderly acquisition of samples to estimate community parameters and to establish comparisons between areas. These methods have been tested worldwide, providing useful data for inventory planning and optimal sampling allocation efforts. The taxonomic counterpart of biodiversity inventories has received considerably less attention. Species lists and their relative abundances are the only link between the community parameters resulting from a biotic inventory and the biology of the species that live there. However, this connection is lost or speculative at best for species only partially identified (e. g., to genus but not to species). This link is particularly important for diverse tropical regions were many taxa are undescribed or little known such as spiders. One approach to this problem has been the development of biodiversity inventory websites that document the morphology of the species with digital images organized as standard views. Their main contributions are the dissemination of phenotypic data for species difficult to identify or new with the assignment of species codes, allowing species comparisons between areas regardless of their taxonomic status. The present paper describes a protocol to produce these websites almost automatically. This protocol was successfully applied to 237 species from a tropical primary forest in Mexico. The time and infrastructure required for the documentation of these species are discussed. Taxonomic information in terms of identification challenges, possible new species, and potential nomenclatural issues is described. In addition, the conventional community parameters (e. g., inventory completeness, species richness estimations, sampling intensity) are also calculated and compared through time and between methods. An optimized version for sampling allocation effort per season is presented and compared with protocols optimized for other tropical forests.
... Sin embargo, los taxónomos, caso de Kress (2014), opinan que describir una nueva especie sin depositar un holotipo es una mala práctica, si bien con excepciones (Lindenmayer & Sche- ele, 2017) como ciertos vertebrados, invertebrados pelágicos o especies ubicadas en enclaves de difícil acceso. De hecho, este tema, en los últimos años, se ha convertido en foco de discusión para muchos autores (Dubois & Nemésio, 2007;Minteer et al., 2014;Krell & Wheeler, 2014;Marshall & Evenhuis, 2015;Santos et al. 2016) (ver Cianferoni & Berto- lozzi, 2016, así como Chaladze (2017); Ceríaco, Gutiérrez, Dubois et al., 2016;Donegan (2008); Faúndez (2017); Gutiérrez & Pine (2017) y Zhang (2017). ...
... On the loss of the type series. Several issues have been brought up regarding the description of species based solely on photographic records (Minteer et al. 2014;Rocha et al. 2014;Krell & Wheeler 2014;Amorim et al. 2016). The species described in this paper does not fit in the debates presented in literature about that controversy (Marshall & Evenhuis 2015;Amorim et al. 2016), since the type series was destroyed while the paper was under preparation and the authors did not have the chance to send vouchers to other institutions, as it was intended for right after this publication. ...
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