ArticlePDF Available

Avoiding (Re)extinction


Abstract and Figures

Alternative methods of identification should be used to avoid collection of voucher specimens of threatened or rediscovered species.
No caption available
Content may be subject to copyright.
DOI: 10.1126/science.1250953
, 260 (2014);344 Science
et al.Ben A. Minteer
Avoiding (Re)extinction
This copy is for your personal, non-commercial use only.
clicking here.colleagues, clients, or customers by
, you can order high-quality copies for yourIf you wish to distribute this article to others
here.following the guidelines
can be obtained byPermission to republish or repurpose articles or portions of articles
): April 23, 2014 (this information is current as of
The following resources related to this article are available online at
version of this article at:
including high-resolution figures, can be found in the onlineUpdated information and services,
, 1 of which can be accessed free:cites 12 articlesThis article
subject collections:This article appears in the following
registered trademark of AAAS.
is aScience2014 by the American Association for the Advancement of Science; all rights reserved. The title
CopyrightAmerican Association for the Advancement of Science, 1200 New York Avenue NW, Washington, DC 20005.
(print ISSN 0036-8075; online ISSN 1095-9203) is published weekly, except the last week in December, by theScience
on April 23, 2014www.sciencemag.orgDownloaded from on April 23, 2014www.sciencemag.orgDownloaded from on April 23, 2014www.sciencemag.orgDownloaded from
ield biologists have traditionally col-
lected voucher specimens to con-
rm a species’ existence. This prac-
tice continues to this day but can magnify
the extinction risk for small and often iso-
lated populations. The availability of ade-
quate alternative methods of documenta-
tion, including high-resolution photography,
audio recording, and nonlethal sampling,
provide an opportunity to revisit and recon-
sider fi eld collection practices and policies.
Cases such as the extinction of the great
auk remind us what is at stake in taking ani-
mals from small and declining populations.
The last wild great auk (Pinguinus impen-
nis) was sighted in 1844 on Eldey Island,
Iceland. Centuries of exploitation for food
and feathers, and, to some degree, a chang-
ing climate, had stressed the species, but
overzealous museum collectors also played
a role in its extinction ( 1). As the bird’s num-
bers dwindled in the 19th century, ornitholo-
gists and curators increasingly prized great
auk skins and eggs, with museums and uni-
versities sending out collection parties to
procure specimens. On Eldey, fishermen
killed the fi nal breeding pair of the fl ightless
birds and sold them to a local chemist, who
stuffed the specimens and preserved them in
spirits. Their internal organs now reside at
the Zoological Museum in Copenhagen ( 2).
The great auk’s disappearance predates
the rise of a robust societal ethic of conser-
vation and the emergence of a scientifi c con-
cern for global biodiversity decline in the
late 20th century. Yet, there is still a strong
and widespread impulse to procure speci-
mens of rare or rediscovered species for sci-
entifi c purposes.
In their global review of species reap-
pearances, Scheffers et al. ( 3) document at
least 351 species that have been rediscovered
since 1889, mostly in the tropics. In recent
years, scientific and media attention has
been drawn to the rediscovery of amphib-
ian species thought to be extinct, including
11 species in Costa Rica alone (see the fi g-
ure). Many amphibian rediscoveries have
been documented by collecting specimens
upon fi rst encounter, a practice one of us has
carried out in the past [R.P. with Craugas-
tor ranoides, ( 4)]. Such rediscovered spe-
cies typically exist in small populations with
small range sizes and are therefore highly
vulnerable. The desire to collect voucher
specimens to verify the reappearance of spe-
cies presumed extinct can be heightened by
the recognition of the organism’s rarity, as in
the case of private individuals seeking to own
and display rare animal specimens for their
perceived scarcity and thus value. Rediscov-
eries can also be accidental, as many missing
species are hard to identify in the fi eld and
collected specimens may turn out to be from
very small populations, with the risk of col-
lection only realized well after the fact ( 5).
Many taxa are difficult to identify
from morphology alone. The collection of
voucher specimens by field biologists is
therefore increasingly augmented by other
kinds of samples. Cultural traditions within
a research community can, however, rein-
force the collection of voucher specimens
even where it is not necessary by insisting
that a preserved specimen in a natural his-
tory collection is the gold standard—or only
standard—for publishing a species descrip-
tion or documenting a species’ presence.
Collecting specimens is no longer required
to describe a species or to document its
The concern about overcollection goes
well beyond the case of rediscovered spe-
Avoiding (Re)extinction
Ben A. Minteer ,
James P. Collins ,
Karen E. Love ,
Robert Puschendorf
Alternative methods of identifi cation should be
used to avoid collection of voucher specimens
of threatened or rediscovered species.
Species loss and rediscovery in Costa Rica. The fungal pathogen Batrachochytrium dendrobatidis (Bd)
has been linked to the decline and extinction of amphibians worldwide ( 12). For example, amphibian popu-
lations in Costa Rica experienced substantial declines, with 20 of the 199 species feared extinct, after Bd
moved through the country from the mid-1980s to the early 1990s ( 13, 14). However, 11 of the 23 species
have been rediscovered ( 4). Holdridge’s toad (Incilus holdridgei) (see photo), a species endemic to a single
volcano, vanished during the declines and was declared extinct by the International Union for Conservation
of Nature and Natural Resources in 2007 but was rediscovered in 2008. Today, relict populations persist in
areas where Bd once contributed to their demise.
School of Life Sciences, Arizona State University, Tempe,
AZ 85287, USA.
School of Biological Sciences, Plymouth
University, Drake Circus, Plymouth, Devon PL4 8AA, UK.
Published by AAAS SCIENCE VOL 344 18 APRIL 2014
raphene is highly conductive, fl ex-
ible, and has controllable permit-
tivity and hydrophilicity, among
its other distinctive properties ( 1, 2). These
properties could enable the development
of multifunctional biomedical devices ( 3).
A key issue for such applications is the
determination of the possible interactions
with components of the biological milieu
to reveal the opportunities offered and the
limitations posed. As with any other nano-
material, biological studies of graphene
should be performed with very specific,
well-designed, and well-characterized types
of materials with defi ned exposure. We out-
line three layers of complexity that are inter-
connected and need to be considered care-
fully in the development of graphene for use
in biomedical applications: material charac-
teristics; interactions with biological com-
ponents (tissues, cells, and proteins); and
biological activity outcomes.
Graphene has now been developed in
many different forms in terms of shapes, sizes,
chemical modifi cations, and other character-
istics that can produce dramatically different
results when studied biologically. Methods
for producing graphene include direct exfolia-
tion in organic liquids ( 4, 5), reduction of gra-
phene oxide (GO) ( 6), and epitaxial growth
by CVD (chemical vapor deposition) on cop-
per ( 7) or epitaxial growth on silicon carbide
( 8). The three aspects of this layer of structural
complexity—the thickness, the lateral extent,
and the surface functionalization of gra-
phene—are illustrated in panel A of the fi gure
and show how the materials produced by dif-
ferent methods fall in very different parts of
this parameter space. These different physical
and chemical characteristics dictate the suit-
ability of a material for specifi c biomedical
These wide discrepancies between the
available graphene types will crucially
determine the second layer of complexity,
that of interactions of graphene with living
cells and their compartments. In panel B
Exploring the Interface of
Graphene and Biology
Kostas Kostarelos
1, 3
and Kostya S. Novoselov
2 ,3
To take advantage of the properties of
graphene in biomedical applications,
well-defi ned materials need to be matched
with intended applications.
Nanomedicine Laboratory, Faculty of Medical and Human
Sciences, University of Manchester, Manchester, UK.
of Physics and Astronomy, University of Manchester, Oxford
Road, Manchester, M13 9PL, UK.
National Graphene Insti-
tute, University of Manchester, Oxford Road, Manchester
M13 9PL, UK. E-mail:;
cies. It also applies to the more common sce-
nario of documenting newly discovered spe-
cies, which (like most rediscovered species)
often exist in small, isolated populations and
therefore suffer from the same problems if
voucher specimens are collected from the
eld. Field collection of individuals from
small and declining populations vulnera-
ble to extinction is also a common practice.
Collection both by professional and amateur
scientists has been linked to the decline or
loss of a range of animal species, includ-
ing Mexico’s elf owl (Micrathene whitneyi
soccorroensis) ( 6). Plants have also been
affected by scientifi c overcollection; Nor-
ton et al. ( 7) cite the case of the scientifi c
collection–driven decline and extinction of
uncommon plant taxa in New Zealand over
the past two centuries.
Perhaps the most powerful alternative
method to collection is a series of good
photographs, which can even be used to
describe a species, complemented by other
lines of evidence, such as molecular data
and a description of a species’ mating call
for birds, amphibians, or insects. Advances
in handheld technology have made it much
easier and cheaper to identify species; most
smartphones have a camera and a voice
recorder suffi cient to gather high-resolution
images as well as an organism’s call. Such
nonlethal techniques were used successfully
for the identifi cation of the bird Bugun lio-
cichla, a species that was newly discovered
in India in 2006 ( 8). The bird’s discoverer
deliberately chose not to collect a voucher
specimen for fear of imperiling the popula-
tion; instead, a combination of photos, audio
recordings, and feathers were used to distin-
guish the species.
In the case of rediscovered species, many
were already well described, and a good-
quality image should suffi ce. For rediscov-
ered, rare, and newly discovered species,
molecular techniques (such as skin swab-
bing for DNA) are an increasingly effec-
tive way to sample a specimen to confi rm
an identity with no or minimal harm to the
organism ( 9, 10). For this system to work,
the DNA of relict populations and newly dis-
covered species must be sequenced and the
data made publicly available. This would, for
example, make future population rediscov-
eries easier to document.
The multivariate description of a species
that results from combining high-resolution
photographs, sonograms (as appropriate),
molecular samples, and other characteristics
that do not require taking a specimen from
the wild can be just as accurate as the collec-
tion of a voucher specimen without increas-
ing the extinction risk. Clearly there remains
a long-running debate over the appropriate
standards for scientifi c description absent
a voucher specimen ( 11). The benefi ts and
costs of verifi cation-driven specimen col-
lection, however, should be more openly
and systematically addressed by scientifi c
societies, volunteer naturalist groups, and
museums. Sharing of specimen information,
including obligations to store genetic infor-
mation from voucher specimens in widely
accessible digital repositories, can also help
to reduce the future need to collect animals
from the wild.
1. S. A. Brengtson, Auk 101, 1 (1984).
2. E. Fuller, The Great Auk: The Extinction of the Original
Penguin (Bunker Hill, Piermont, New Hampshire, 2003).
3. B. R. Scheffers, D. L. Yong, J. B. Harris, X. Giam, N. S.
Sodhi, PLOS ONE 6, e22531 (2011).
4. A. García-Rodríguez, G. Chaves, C. Benavides-Varela,
R. Puschendorf, Divers. Distrib. 18, 204 (2012).
5. K. Nishida, Brenesia 66, 78 (2006).
6. R. Rodriguez-Estrella, M. C. Blázquez Moreno, Biodivers.
Conserv. 15, 1621 (2006).
7. D. A. Norton, J. M. Lord, D. R. Given, P. J. De Lange, Taxon
43, 181 (1994).
8. R. Athreya, Indian Birds 2, 82 (2006).
9. J. Prunier et al., Mol. Ecol. Resour. 12, 524 (2012).
10. A. M. Mendoza, J. C. García-Ramírez, H. Cárdenas-Henao,
Mol. Ecol. Resour. 12, 470 (2012).
11. N. J. Collar, Ibis 141, 358 (1999).
12. J. P. Collins, M. L. Crump, Extinction in Our Times: Global
Amphibian Declines (Oxford Univ. Press, 2009).
13. F. Bolaños, Ambientico 107, 12 (2002).
14. B. L. Phillips, R. Puschendorf, Proc. Biol. Sci. 280,
20131290 (2013).
Published by AAAS
... For rare species and subspecies that are, or are expected to be, listed as 'threatened' (i.e., 'Critically Endangered', 'Endangered', 'Vulnerable') on The IUCN Red List of Threatened Species, it is now widely considered to be unethical and unjustifiable for individuals to be killed in order to serve as holotypes or as other members of the type series. As such, the use of a live specimen in photographs is taken to be an adequate alternative to a physical voucher specimen (Wakeham-Dawson et al. 2002;Jones et al. 2005;Polaszek et al. 2005;Donegan 2008;Minteer et al. 2014aMinteer et al. , 2014bPape et al. 2016). The use of individuals in photographs to form type series is expected to increase as the vast majority of rare species and subspecies have yet to be described and named (Ceballos and Ehrlich 2009). ...
... 4. Conduct biogeographical and comparative morphological and molecular research across the geographic distribution of C. angolensis to further our understanding of the evolution, phylogeography, and taxonomic arrangement of this species (Grubb et al. 2003;McDonald et al. 2022). In this regard, the low number of individuals, small geographic distribution, isolation, and vulnerability of C. a. mahale, and probably also of C. a. prigoginei, dictate that no wild individuals should be 'collected' (Wakeham-Dawson et al. 2002;Jones et al. 2005;Polaszek et al. 2005;Donegan 2008;Minteer et al. 2014aMinteer et al. , 2014bPape et al. 2016). Many more photographs should be acquired of wild individuals and made widely available. ...
Full-text available
The polytypic Angola colobus Colobus angolensis is a widespread species that, in eastern Africa, is often restricted to small, highly isolated, areas. In 1966, evidence for an undescribed subspecies of C. angolensis was obtained in Mahale Mountains National Park, central west Tanzania. Mahale C. angolensis has only been observed twice by scientists (1976 and 1979) and remained unnamed. In April 2022, 43 years after the last published observation, we observed, heard, and photographed a group of Mahale C. angolensis. Given the considerable current geographic isolation (~100 km across L. Tanganyika; ~330 km across land) of this monkey from its conspecifics, together with the distinctive coloration and pattern of its pelage, we here designate this as a new subspecies. We also describe the environment in which Mahale C. angolensis lives, discuss its paleobiogeography, taxonomic arrangement, and threats, and provide recommendations for conservation and research. Mahale C. angolensis is endemic to the montane forests of Mahale Mountains National Park where it has been observed at only two sites, the south slope of Mt. Ihumo (~1,970 m asl) and on the ridge between Mt. Nkungwe and Mt. Kahoko (~2,350 m asl). In addition, bouts of 'roar' loud calls were heard on nearby Mt. Mhensabantu (~2,050 m asl) on two occasions. The geographic distribution of Mahale C. angolensis is likely between 10 km² and 50 km². The size of this population is probably <400 individuals, with <200 adults. This monkey appears to occur wholly within a remote and rugged part of Mahale Mountains National Park where agricultural encroachment and poaching are not major concerns at this time. The primary threats are habitat loss due to fire, and to a warming climate. With its small population and severely restricted geographic distribution, Mahale C. angolensis qualifies as a 'Critically Endangered' subspecies under current IUCN Red List degree of threat criteria.
... For almost two decades, we have been witnessing different attempts to accelerate the taxonomic process and numerous debates for and against some of the proposals. The two most "revolutionary" proposals are, in fact, technological approaches in which species descriptions should be replaced with DNA barcodes [130,131], while type specimens should be replaced with photographs of species taken in the field [131,132]. From its beginnings, taxonomy has been integrative, but species descriptions are based on a set of characters (with emphasize character state), and, in most cases, illustrated with line drawings and/or (later) photographs. In a broader context, those "revolutionary" approaches are just simplifications of taxonomy in the way of using just one character (DNA barcodes) instead of many [6], and keeping the illustration, but not the voucher specimens. ...
... Researchers who advocate those ideas give many different reasons why it is "better" than traditional taxon-omy. For example, Minteer et al. stated that voucher specimens should be replaced with a "series of good photographs, which can even be used to describe a species, complemented by molecular data and a description of a species' mating call for birds, amphibians, or insects" in order to avoid the extinction that can be caused by collecting [132]. There are at least two questionable aspects of this statement. ...
Full-text available
Taxonomic impediment is one of the main roadblocks to managing the current biodiversity crisis. Insect taxonomy is the biggest contributor to the taxonomic impediment, both in terms of the knowledge gap and the lack of experts. With this study, we tried to size the knowledge gap by analyzing taxonomical studies on the subfamily Aphidiinae (Hymenoptera: Braconidae) conducted from 2010 to 2021. All available taxonomic knowledge gathered in this period is critically summarized: newly described species, detection of alien species, published identification keys, etc. All findings are discussed relative to the current state of general taxonomy. Future prospects for taxonomy are also discussed.
... The growth of museum collections through live specimen collection [1] is a relic of the extractive, colonial science practices of the 20th century [2]. While others have already discussed whether collecting might jeopardize threatened wildlife populations [3,4], there is another harm perpetuated through this practice. Removing an animal from its natural habitat and killing it for the purpose of storing it in a museum collection reinforces the stance that humans have dominion over other living creatures. ...
Full-text available
Compassionate collection involves minimizing harm while collecting museum data in the field. By adopting this practice, natural history museums could better maintain existing collections, accommodate more nonlethal specimens and data, and foster an inclusive community.
... rare and endangered species or species with low population densities) is limited. They can also produce biased results because of the direct interference of humans and their technologies in the research process (Vucetich, Nelson 2007;Minteer et al. 2014;Field et al. 2019). In addition, these methods, despite their long tradition, are time-consuming and labor-intensive (Zemanova, 2020). ...
Full-text available
The data on the intraspecific genetic variation for monitoring and conservation of wild populations is an important link for the assessment of the organisms resistance to changing environmental conditions and anthropogenic pressures. The metabarcoding of DNA from the aquatic environment provides a gradual transition to non-invasive methods of biodiversity research, including within-species level. However, the degradation of DNA under UV light in the aquatic environment limits the choice of markers in favor of short standardized regions. Hence, the consequences of information loss when shifting from barcode to metabarcode are not entirely clear. The efforts on approbation and calibration at the intraspecies level under experimental conditions are limited to molecular genetic markers designed for target species. In this study, we aimed to address these challenges: to assess the intraspecific variation in different taxa based on the COI barcode reduced to Leray region (~313bp), accessible from the GenBank, as well as experimentally evaluate the possibility to identify Operational Taxonomic Units (OTUs) and Amplicon Sequence Variant (ASVs) in marine eDNA among abundant species of the Zostera sp. community in the northern Sea of Japan: Hexagrammos octogrammus , Pholidapus dybowskii (Teleostei: Perciformes), and Pandalus latirostris (Arthropoda: Decapoda). The three abovementioned species were collected at two distant locations in the Great Bay of the Japan Sea and placed into a separate 150-liter aquaria to produce both – individual and mock communities eDNA samples. Then all individuals were euthanized and genotyped individually for 650 bp and 313 bp COI gene regions. The COI Leray region was amplified based on the eDNA of mock communities and individual specimens. The resulting amplicons were sequenced on the Illumina 250 bp pair-end platform and processed based on the Begum pipeline. Along with the OTUs based on both global and local references we tried to retrieve individual haplotypes from the obtained reads. We found that eDNA samples from the experiment when blasting on local reference produce additional OTUS which we consider to be NUMTS. Surprisingly, the presence of NUMTS in the eDNA samples reduces the detection of ASVs, which may be related both to the low sequencing coverage in the experiment and probably to the natural competition of pseudogenes for primer binding sites during amplification. Perhaps a PCR-free, metagenomic approach, despite poor accessibility, might solve these difficulties. In addition, we have gathered and analyzed natural water samples from one of the sample locations of Zostera sp. community with a little sequence coverage and failed to retrieve any reliable information about OTUs and ASVs of taxa in mock communities, which may indicate much higher biomass of non-target organisms in the studied community. A total of 90 sequence data sets were collected for some common groups of multicellular organisms (Mollusca, Echinodermata, Crustacea, Polychaeta and Actinopterygii) through the search on the mitochondrial COI gene in the popset database of the NCBI. The separate sets of sequences of Leray region were generated. Then, the values of haplotypic variability, as well as the number of population clusters of the same dataset were calculated for the region of original length and Leray region. The produced results reflect the decrease of population diversity by 1 cluster in average while switching from barcode to metabarcode. In addition we found that the length of the Leray fragment can vary in the Echinoderms.
... None of this changes the need to respect that for many the taking of individuals as specimens for scientific research is abhorrent and unacceptable (see, for example, discussions in Remsen 1995Remsen , 1997Bekoff & Elzanowski 1997;Minteer et al. 2014;Russo et al. 2017). Equally, there are those who feel that scientific collection of specimens, while of course needing to be done sensibly, sensitively and with checks and balances (Costello et al. 2016), ultimately is what underpins the scientific order we try to bring to understanding, conserving and managing the populations that comprise biodiversity (Remsen 1997;Winker & Withrow 2017;Schmitt et al. 2018). ...
A case is made for why researchers should consider the possibilities that the north Queensland population of Spotted Quail-thrush Cinclosoma punctatum discovered in 2008 may be neither geographically or genetically isolated nor taxonomically distinct. Field and museum work are clearly needed to address these questions as well as the biology of the north Queensland population itself.
... Continued support of museums by funding agencies and dedication to collect specimens by museums are urgently needed to build and maintain this critical scientific resource moving forward and this topic should be a global priority. Yet collecting new specimens is still criticized and overlooked as an invaluable investment in the future (Minteer et al., 2014). However, this criticism is often due to misconceptions about the perceived negative impact of museum collecting on wildlife populations (Remsen, 1995;Hope et al., 2018). ...
Full-text available
Historical DNA obtained from voucher specimens housed in natural history museums worldwide have allowed the study of elusive, rare or even extinct species that in many cases are solely represented by museum holdings. This has resulted in the increase of taxonomic representation of many taxa, has led to the discovery of new species, and has yielded stunning novel insights into the evolutionary history of cryptic or even undescribed species. Peromyscus mekisturus, is a critically endangered cricetid rodent endemic to Mexico and is only known from two museum specimens collected in 1898 and 1947. Intensive field work efforts to attempt to determine if viable populations still exist have failed, suggesting that this species is extinct or is nearing extinction. In addition, a recent study using mitogenomes demonstrated that P. mekisturus forms a well-supported clade outside the genus Peromyscus and hypothesized that this taxon is the sister group of the genus Reithrodontomys. Here, we used target enrichment and high-throughput sequencing of several thousand nuclear ultraconserved elements and mitogenomes to reconstruct dated phylogenies to test the previous phylogenetic hypothesis. We analyzed the holotype and the only other known specimen of P. mekisturus and museum samples from other peromyscine rodents to test the phylogenetic position of the species. Our results confirm that the only two specimens known to science of P. mekisturus belong to the same species and support the hypothesis that this species belongs to an undescribed genus of cricetid rodents that is sister to the genus Reithrodontomys. We dated the origin of P. mekisturus together with other speciation events in peromyscines during the late Pliocene – early Pleistocene and related these events with the Pleistocene climatic cycles. In light of our results, we recommend a taxonomic re-evaluation of this enigmatic species to properly recognize its taxonomic status as a new genus. We also acknowledge the relevance of generating genomic data from type specimens and highlight the need and importance of continuing to build the scientific heritage of the collections to study and better understand past, present, and future biodiversity.
... Voucher collections alone are unlikely to represent a primary cause of population losses in insects. Only in rare instances have collections been shown to contribute to population loss or species extinction (see Minteer et al. 2014 for review). Furthermore, we do not claim that annual collections of ≈6,000 bumble bees per se (in line with our results from the SCAN database) from across North America have had marked negative impacts on most wild populations. ...
Full-text available
Global declines of arthropods have garnered widespread attention because the loss of insect species threatens critical ecosystem services such as decomposition, pest control, and pollination (Sánchez-Bayo et al. 2019 and citations therein). Although the extent of the “insect apocalypse” is currently under debate (Didham et al. 2020), insect declines are well documented worldwide, with habitat loss, agricultural intensification, and climate change cited as primary drivers of losses in biomass and diversity (Raven and Wagner 2021). These losses have stimulated conservation action and research effort. However, lethal sampling continues as a common entomological practice, despite conservation concern and increasing research. Facing myriad extant pressures, vulnerable insect populations may be less resilient to traditional sampling norms than broadly assumed. We raise as an emerging concern the potentially damaging yet unknown impacts of contemporary specimen collection on wild insect populations. Reviewing the literature on temporal sampling trends in bumble bees as a case study, we highlight the value of non-lethal sampling alternatives and underscore the need for proactive, empirically informed sampling guidelines that reflect taxon-specific conservation needs.
... Though the impact of lethal sampling on wild bee populations for scientific or conservation purposes dwarfs the impact of other anthropogenic stressors (Keilsohn et al., 2018), and it is certainly not among the main drivers of bee and insect declines (Miliči c et al., 2021;Potts et al., 2010;S anchez-Bayo & Wyckhuys, 2019), reducing the numbers of captures is an ethical, logistical, and scientifically defensible long-term objective (Drinkwater et al., 2019;Tepedino & Portman, 2021), especially for rare species or species of conservation concern (Minteer et al., 2014) and in intense spatially and temporally replicated sampling (Montgomery et al., 2021). The goal of minimizing harm to animal populations while simultaneously achieving scientific research objectives has been addressed with the "3Rs" approach since the 1950s (Russell & Burch, 1959). ...
Full-text available
Bees are important pollinators of wild and domesticated flowering plant species. Over the last 30 years, an increasing number of scientific articles have been published on the ecology and conservation of wild bees. To achieve research goals, many studies have pursued the lethal take of wild bees. Although the impact of lethal take for scientific pursuits is likely negligible compared to the negative impacts of human‐mediated phenomena such as climate change, urbanization, and agricultural intensification, it is important to evaluate the history of lethal take on scientific endeavors. In our study, we evaluated a random sample of 30 years of scientific publications on wild bees. Across 1426 surveyed publications, 536 reported the lethal take of wild bees. We found that 61% of these studies lethally captured wild bees primarily for species identification. Furthermore, we determined passive sampling of wild bees resulted in substantially more lethal collections than active methods per study. However, combined approaches of passive and active collection resulted in the greatest lethal take of wild bees per study. Finally, we determined that 64% of the studies did not provide deposition information for their samples, hindering additional research that could be done with them. The increasing availability of video and photographic devices and artificial intelligence approaches to identification, the development of low and noninvasive molecular methods, and the ease of sharing information, allow for a timely discussion on alternative routes and potentially new best practices in bee research. We focus our discussion on alternative methods for minimizing lethal captures for identification purposes and through passive methods, and for maximizing the utility of the data collected. Finally, we provide a framework for continued engagement among researchers and managers to develop strategies that can contribute to reducing our impact on wild bee communities and making the most of collected specimens. To achieve research goals, many studies have pursued the lethal capture of wild bees. We conducted a literature search of last 30 years of scientific research on wild bees and we found that 61% of studies (from a random sample of the total) lethally captured wild bees, primarily for species identification and with passive sampling methods. We then discuss the current available alternative methods for minimizing lethal captures and maximizing the utility of the data collected, and thus, for reducing our impact on wild bee communities.
Full-text available
Ecological studies with Scarabaeinae dung beetles have increased exponentially over the past 30 years, using lethal pitfall traps baited with mammal feces or carrion as the preferred sampling method. Different studies have determined the distance between pitfall traps for effective sampling, but the number of traps is often subjective, leading to excessive or poor sampling. This study provides quantitative guidelines for establishing the sample size for optimal completeness of dung beetle diversity by systematically reviewing the relationship between sampling intensity and sampling coverage, habitat type, and the journal impact factor in peer-reviewed research. We gathered 94 studies covering a range from México to Argentina. Sampling was conducted mainly in forested habitats, followed by treeless agriculture and agroforestry systems, with a median value of 50 pitfall traps per sampled habitat. Sampling completeness was above 0.9 in 95% of the studies. Oversampling ranged from 1 to more than 96,000 individuals, and sampling deficit varied between 2 and 3,300 specimens. Sampling intensity and the journal impact factor were significantly and positively correlated with oversampling, but these variables did not explain the sampling deficit. The positive correlation between journal impact factor and oversampling may reflect a publication bias where high-impact journals and researchers seek more generalizable information obtained with a higher sampling intensity. Dung beetle oversampling was not homogeneous between habitats, being highest in old-growth forests and lowest in disturbed habitats such as pastures and forest edges. Our results show that the collection intensity used in dung beetle studies should be reconsidered carefully. By incorporating ethical principles used in animal science, we suggest sampling guidelines for a robust sampling scheme of dung beetle diversity, which would also prevent oversampling. Consciously reducing sampling intensity will make resource use more cost-effective. We suggest increasing the number of independent sampling units rather than intensifying subsampling, thereby increasing the predictive power of statistical models to obtain more robust evidence of the phenomena under study.
Full-text available
The Caribbean monk seal (Monachus tropicalis), the only seal species native to Central America, was declared extinct in 2008, with the last confirmed sighting in 1952. This species historically had a broad range throughout the gulf of Mexico. This article discusses the history of Western science on the monk seal, from its first recorded sighting by a Western colonizer in 1492 to scientific collection in the 1800s and 1900s, as a history of the erasure of this species. Museum practices of collecting and displaying Caribbean monk seals have directly contributed to this erasure, and ways of writing a new history by giving the Caribbean monk seal the capacity to refuse erasure are suggested.
Full-text available
The virulence of a pathogen can vary strongly through time. While cyclical variation in virulence is regularly observed, directional shifts in virulence are less commonly observed and are typically associated with decreasing virulence of biological control agents through coevolution. It is increasingly appreciated, however, that spatial effects can lead to evolutionary trajectories that differ from standard expectations. One such possibility is that, as a pathogen spreads through a naive host population, its virulence increases on the invasion front. In Central America, there is compelling evidence for the recent spread of pathogenic Batrachochytrium dendrobatidis (Bd) and for its strong impact on amphibian populations. Here, we re-examine data on Bd prevalence and amphibian population decline across 13 sites from southern Mexico through Central America, and show that, in the initial phases of the Bd invasion, amphibian population decline lagged approximately 9 years behind the arrival of the pathogen, but that this lag diminished markedly over time. In total, our analysis suggests an increase in Bd virulence as it spread southwards, a pattern consistent with rapid evolution of increased virulence on Bd's invading front. The impact of Bd on amphibians might therefore be driven by rapid evolution in addition to more proximate environmental drivers.
Full-text available
Norton, D. A., Lord, J. M., Given, D. R. & De Lange, P. J.: Over‐collecting: an overlooked factor in the decline of plant taxa. – Taxon 43: 181‐185. 1994. – ISSN 0040‐0262. Botanists, both professional and amateur, can have a substantial impact on uncommon plant taxa through over‐collecting, and in some cases this may result in extinction of uncommon taxa. This paper reviews examples of over‐collecting, mainly from the New Zealand flora, and suggests five guidelines to reduce its impact: (1) to use photographs where possible, especially as a preliminary record, (2) not to collect whole plants unless there are more than 20 plants, or more than 5 % of any one plant, (3) not to collect flowers or fruits if only a few present, (4) not to collect duplicates, and (5) to use seeds or cuttings for cultivation. Awareness of the effects of over‐collection and adoption of these collecting guidelines should contribute significantly to the conservation of uncommon plants.
Full-text available
In molecular biology studies of Anura, nondestructive methods to obtain genetic material are needed as alternatives to toe clipping. This work evaluates a nondestructive method for sampling DNA from blood puncture, comparing the performance of three different extraction protocols (Qiagen Kit, Salting-out and Chelex). We collected 134 individuals of Eleutherodactylus johnstonei, extracting blood via puncture of the medial vein using commercial-grade glucometer lancets. We extracted 100-1880 ng DNA, finding no differences between the extraction protocols. We compared the quality of the resulting DNA through amplification and sequencing of the 16S mitochondrial gene. Amplification was successful for the three extraction protocols, although Chelex showed better performance, making it the most recommendable protocol for extraction of DNA from blood. The resulting sequences corresponded to those registered in the GenBank for this species. Additionally, we found no significant differences in survival or weight change between the individuals that were manipulated and a control group (mean survival 66.7% treated, 62.9% untreated). Data reveal that blood samples obtained by puncture are a convenient alternative to other tissues (phalange, buccal swab, liver) that have traditionally been used as DNA sources for anurans. The technique is applicable to small and large species, covering most anuran diversity, provides enough DNA for many genetic applications and produces no noticeable effect on the survival or performance, given that it does not affect the motor parts or the dexterity of the animals.
Aim We used abiotic environmental variables and historical locality records to infer distributions of endangered anuran species of Costa Rica to promote efficient strategies for future amphibian surveys. Location Costa Rica. Methods We used a Maximum Entropy Algorithm (Maxent) to predict potential distribution maps for 17 species of endangered anurans and create a consensus map of species richness. We compared the environmental conditions from localities where relictual amphibian populations were recently rediscovered with the conditions across their historical range to evaluate the possibility that these relictual populations might occur in specific climatic conditions that could explain their persistence. We used a multicriteria analysis considering the following factors: the intersection zones between the consensus map, conservation areas, potential Batrachochytrium dendrobatidis (Bd) distribution, collecting effort and areas within the precipitation range at which reappearances had occurred to locate sites for future surveys. Results The resulting predictions suggest that suitable areas for the highest number of species occur between 1300 and 2500 m.a.s.l and are concentrated along the Pacific slopes of the Cordillera de Talamanca and Cordillera Volcánica Central. Around 45% of the high potential richness area is under protection. Relictual populations of declined species seem to persist mainly in highly humid localities (2500–3500 mm of mean annual precipitation). Around 240 km2 has an ideal environment for the rediscovery of relictual populations. The multicriteria analysis showed that around 0.5% of the Costa Rican territory should be surveyed exhaustively for frogs. Main conclusions Many of the potential refugia we identified here have not been surveyed since 2000, the areas identified by the best model predictions correspond well with the localities of the relictual populations recently reported. We suggest future surveys of missing amphibian species should focus on these areas. The discovery of populations of endangered species can be used to propose conservation areas.
Considerable sums of money are aimed at biodiversity conservation programs at present, and although collection of specimens is necessary for the advancement of taxonomy and systematics, we detected a dilemma between conservation and collection of rare species with small populations. Collecting may act synergistically with other factors to increase the risk of, or even drive species to extinction. We present some examples we believe show the conflict between collecting rare species with a small population and the conservation programs for those species. We also stress the need to review the Minimum Viable Population Size concept as it can be used as a justification for collecting small, rare, and declining population species.
This study introduces a novel DNA sampling method in amphibians using skin swabs. We assessed the relevancy of skin swabs relevancy for genetic studies by amplifying a set of 17 microsatellite markers in the alpine newt Ichthyosaura alpestris, including 14 new polymorphic loci, and a set of 11 microsatellite markers in Hyla arborea, from DNA collected with buccal swabs (the standard swab method), dorsal skin swabs and ventral skin swabs. We tested for quality and quantity of collected DNA with each method by comparing electrophoresis migration patterns. The consistency between genotypes obtained from skin swabs and buccal swabs was assessed. Dorsal swabs performed better than ventral swabs in both species, possibly due to differences in skin structure. Skin swabbing proved to be a useful alternative to buccal swabbing for small or vulnerable animals: by drastically limiting handling, this method may improve the trade-off between the scientific value of collected data, individual welfare and species conservation. In addition, the 14 new polymorphic microsatellites for the alpine newt will increase the power of genetic studies in this species. In four populations from France (n=19-25), the number of alleles per locus varied from 2 to 16 and expected heterozygosities ranged from 0.04 to 0.91. Presence of null alleles was detected in two markers and two pairs displayed gametic disequilibrium. No locus appeared to be sex-linked.