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Avoiding (Re)extinction

DOI:10.1126/science.1250953
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Ben A Minteer
Ben A Minteer
Ben A Minteer
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James P Collins
James P Collins
James P Collins
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Karen E Love
Karen E Love
Karen E Love
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Robert Puschendorf at University of Plymouth
Robert Puschendorf
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Alternative methods of identification should be used to avoid collection of voucher specimens of threatened or rediscovered species.
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DOI: 10.1126/science.1250953
, 260 (2014);344 Science
et al.Ben A. Minteer
Avoiding (Re)extinction
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18 APRIL 2014 VOL 344 SCIENCE www.sciencemag.org
260
PERSPECTIVES
F
ield biologists have traditionally col-
lected voucher specimens to con-
fi 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
rediscovery.
The concern about overcollection goes
well beyond the case of rediscovered spe-
Avoiding (Re)extinction
ECOLOGY
Ben A. Minteer ,
1
James P. Collins ,
1
Karen E. Love ,
1
Robert Puschendorf
2
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.
PHOTO CREDIT: JUAN G. ABARCA ALVARADO
1
School of Life Sciences, Arizona State University, Tempe,
AZ 85287, USA.
2
School of Biological Sciences, Plymouth
University, Drake Circus, Plymouth, Devon PL4 8AA, UK.
E-mail: ben.minteer@asu.edu
Published by AAAS
www.sciencemag.org SCIENCE VOL 344 18 APRIL 2014
261
PERSPECTIVES
G
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
applications.
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
MATERIALS SCIENCE
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.
1
Nanomedicine Laboratory, Faculty of Medical and Human
Sciences, University of Manchester, Manchester, UK.
2
School
of Physics and Astronomy, University of Manchester, Oxford
Road, Manchester, M13 9PL, UK.
3
National Graphene Insti-
tute, University of Manchester, Oxford Road, Manchester
M13 9PL, UK. E-mail: kostas.kostarelos@manchester.ac.uk;
kostya@manchester.ac.uk
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
fi 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.
References
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).
10.1126/science.1250953
Published by AAAS
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  • Jun 2022
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.
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Good news! Sampling intensity needed for accurate assessments of dung beetle diversity may be lower in the Neotropics
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  • Oct 2022
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.
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Erasing the extinct: the hunt for Caribbean monk seals and museum collection practices
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  • Dec 2021
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.
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Do pathogens become more virulent as they spread? Evidence from the amphibian declines in Central America
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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.
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Over-Collecting: An Overlooked Factor in the Decline of Plant Taxa
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Full-text available
  • May 1994
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.
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Blood puncture as a nondestructive sampling tool to obtain DNA in frogs: Comparison of protocols and survival analysis
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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.
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Where are the survivors? Tracking relictual populations of endangered frogs in Costa Rica
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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.
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Rare, Fragile Species, Small Populations, and the Dilemma of Collections
Article
  • May 2006
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.
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Skin swabbing as a new efficient DNA sampling technique in amphibians, and 14 new microsatellite markers in the alpine newt (Ichthyosaura alpestris)
Article
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.
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