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Since the 1980s, many have suggested we are in the midst of a massive extinction crisis, yet only 799 (0.04%) of the 1.9 million known recent species are recorded as extinct, questioning the reality of the crisis. This low figure is due to the fact that the status of very few invertebrates, which represent the bulk of biodiversity, have been evaluated. Here we show, based on extrapolation from a random sample of land snail species via two independent approaches, that we may already have lost 7% (130,000 extinctions) of the species on Earth. However, this loss is masked by the emphasis on terrestrial vertebrates, the target of most conservation actions. Projections of species extinction rates are controversial because invertebrates are essentially excluded from these scenarios. Invertebrates can and must be assessed if we are to obtain a more realistic picture of the sixth extinction crisis.
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Mass extinction in poorly known taxa
Claire Régnier
, Guillaume Achaz
, Amaury Lambert
, Robert H. Cowie
, Philippe Bouchet
and Benoît Fontaine
Institut de Systématique, Evolution, Biodiversité, UMR 7205 CNRS Muséum national dHistoire naturelle (MNHN), Université Pierre et Marie Curie (UPMC),
Ecole pratique des hautes études (EPHE), Muséum national dHistoire naturelle, Sorbonne Universités, 75231 Paris Cedex 05, France;
UMR 7138, CNRS
Evolution Paris Seine, Université Pierre et Marie Curie, 75252 Paris Cedex 05, France;
Atelier de Bioinformatique, Université Pierre et Marie Curie, 75252
Paris Cedex 05, France;
UMR 7241, INSERM U1050, Center for Interdisciplinary Research in Biology, Collège de France, 75005 Paris, France;
UMR 7599
Laboratoire de Probabilités et Modèles Aléatoires, Université Pierre et Marie Curie, CNRS, 75252 Paris Cedex 05, France;
UMR 7599 Laboratoire de
Probabilités et Modèles Aléatoires, Université Paris Diderot, CNRS, 75252 Paris Cedex 05, France;
Pacific Biosciences Research Center, University of Hawaii,
Honolulu, HI 96822; and
UMR 7204, Département Ecologie et Gestion de la Biodiversité, Muséum National dHistoire Naturelle, 75231 Paris Cedex 05, France
Edited by Peter M. Kareiva, The Nature Conservancy, Seattle, WA, and approved May 5, 2015 (received for review February 5, 2015)
Since the 1980s, many have suggested we are in the midst of a
massive extinction crisis, yet only 799 (0.04%) of the 1.9 million
known recent species are recorded as extinct, questioning the
reality of the crisis. This low figure is due to the fact that the status
of very few invertebrates, which represent the bulk of biodiver-
sity, have been evaluated. Here we show, based on extrapolation
from a random sample of land snail species via two independent
approaches, that we may already have lost 7% (130,000 extinc-
tions) of the species on Earth. However, this loss is masked by the
emphasis on terrestrial vertebrates, the target of most conserva-
tion actions. Projections of species extinction rates are controver-
sial because invertebrates are essentially excluded from these
scenarios. Invertebrates can and must be assessed if we are to
obtain a more realistic picture of the sixth extinction crisis.
biodiversity crisis
IUCN Red List
Status of Invertebrates in the International Union for the
Conservation of Nature Red List
Biodiversity decline has been of concern for several decades (1
3). However, the International Union for the Conservation of
Nature (IUCN) Red List, the most widely used tool to measure
this decline at a global level (4), lists fewer than 800 modern
extinctions (5), an infinitesimal fraction of the total number of
extant species, commonly estimated at 510 million (6, 7). Al-
though the Red List is primarily a tool for identifying those
species that are most threatened and thus most in need of con-
servation action, and not a rigorous catalog of extinctions, re-
actions to this low number of documented extinctions have
ranged from eco-skepticism (8) to eco-satisfaction, the low
number seen by some as a measure of the success of conservation
programs (9). However, there is a bias in estimates of bio-
diversity decline, because most of them focus on mammals and
birds (10). Assessment of a speciesconservation status accord-
ing to the IUCN criteria requires robust data on geographic
range, population trends, threats, habitat, and ecology, such that
the evaluation is rigorous and unassailable. This quality of data is
available essentially for only a handful of remarkable species,
almost exclusively vertebrates. By 2013, all 15,528 known bird
and mammal species had been evaluated against the IUCN Red
List criteria (5), with only 5.8% ranked as data deficient (not
allocable to one of the other IUCN categories: extinct, extinct in
the wild, critically endangered, endangered, vulnerable, near
threatened, and least concern). We thus have a fairly good pic-
ture of how the biodiversity crisis is impacting mammals and
birds, especially large charismatic ones (e.g., rhinos, large ceta-
ceans, tigers, and condors), but we are still in the mist for most
invertebrate taxa, a consequence of their poorly documented
conservation status (11, 12). Only 15,911 invertebrate species of
1.4 million described (13) are listed by IUCN. Of these, only
28% are categorized as data deficient, a proportion that may
seem low (i.e., the conservation status of almost three-quarters
of the invertebrate species evaluated could indeed be assessed).
However, the invertebrate species that have gone through the
Red List process belong to relatively charismatic and well-stud-
ied groups, such as butterflies, dragonflies, reef-building corals,
and certain snails. Because of the lack of information on threats
to invertebrates, the vast majority of species are not addressed by
the Red List process (14). If, instead, IUCN evaluated randomly
chosen invertebrates, the proportion of species that could not be
assessed would be much higher. The fact is that after more than
four decades of IUCN Red Lists, invertebrates are still essen-
tially unevaluated overall, because for many of these species, the
only useful data are, at best, collection dates and localities,
sometimes only type localities (13, 15).
Gathering All Available Information on Poorly Known
Here, we suggest two alternative methods to assess the conser-
vation status of poorly known species. We test these methods on
a sample of land snail species from around the world. Mollusks
are particularly suitable for this evaluation, being the group the
most impacted by extinction according to the IUCN Red List
(16, 17). Moreover, a large community of both professional and
amateur scientists has long been involved in recording locality
data and vouchering specimens in reference collections. A ran-
dom worldwide sample of 200 pulmonate land snail species
was drawn from the literature and data relevant for evaluating
their conservation status were compiled from (i) the literature
Since the 1980s, many biologists have concluded that the earth is
in the midst of a massive biodiversity extinction crisis caused by
human activities. Yet fewer than 1,000 of the planets 1.9 million
known species are officially recorded as extinct. Skeptics have
therefore asked Is there really a crisis?Mammals and birds
provide the most robust data, because the status of almost all
has been assessed. Invertebrates constitute over 99% of species
diversity, but the status of only a tiny fractionhas been assessed,
thereby dramatically underestimating overall levels of extinc-
tion. Using data on terrestrial invertebrates, this study estimates
that we may already have lost 7% of the species on Earth and
that the biodiversity crisis is real.
Author contributions: C.R., G.A., A.L., P.B., and B.F. designed research; C.R. performed
research; G.A. and A.L. contributed new reagents/analytic tools; C.R. and G.A. analyzed
data; and C.R., R.H.C., and B.F. wrote the paper.
The authors declare no conflict of interest.
This article is a PNAS Direct Submission.
Freely available online through the PNAS open access option.
C.R. and G.A. contributed equally to this work.
To whom correspondence should be addressed. Email:
This article contains supporting information online at
1073/pnas.1502350112/-/DCSupplemental. PNAS Early Edition
(SI Discussion), including gray literature, (ii) museum collec-
tions, and (iii) consultation with experts (SI Discussion). The
literature search resulted in 932 references, of which 80% fo-
cused primarily on taxonomy, 32% provided localities, 26%
provided dates of collection, and 11% gave information on
habitat, range, abundance, and ecology. The collections of five
major natural history museums were searched, either via their
online databases or directly, to gather additional unpublished
data on collection dates and localities. Experts with local
knowledge of regional faunas or with global knowledge on par-
ticular groups of species were consulted if available. Of the 200
species, nine (4.5%) were already on the Red List (three as ex-
tinct, two as threatened, two as near threatened, one as least
concern, and one as data deficient). Sixty-one (30.5%) had not
been recorded in the field since their original description, and 79
(39.5%) had not been recorded in the previous 50 y (Fig. 1).
Sixty-seven species (33.5%) are known from one locality only,
and for 37 species (18.5%) we did not find a precise locality
(geographic coordinates or named locality that could be pin-
pointed on a map to within a few kilometers).
Experts Assess 10% of the Sampled Species As Extinct. Data on
ecology and distribution, of the robustness required for standard
IUCN assessments (SI Discussion), were found for only 31 spe-
cies; thus, according to the IUCN criteria, 84.5% of our sample
wouldbelistedasdatadeficientintheRedList(Fig. S1).
However, based on expert knowledge of species and threat levels,
we suggest an alternative assessment method (SI Discussion), and
provide the following two examples of the approach. Amastra
baldwiniana, endemic to the Hawaiian island of Maui (and
member of the endemic Hawaiian family Amastridae), would not
be listed as extinct under the IUCN criteria because no targeted
surveys have been conducted to search for the species and be-
cause no confirmed date of extinction is known. However, it is
well understood (16, 18, 19) that amastrids have declined dras-
tically in the Hawaiian Islands through loss of habitat and in-
troduction of invasive species; and, given the taskforce of both
professional land snail researchers and amateur shell collectors in
Hawaii, and the manageable size of the area to be searched, it is
very unlikely that this species would not have been found in the
last few decades if it still survived. Consequently, the experts are
reasonably sure that this species is extinct, and we would classify it
as such. Conversely, Eucalodium moussonianum (Urocoptidae),
from Mexico, has not been recorded since its original description
in 1872 from the State of Vera Cruz, and there are no data on its
distribution or habitat preferences. Given the paucity of field
surveys in Mexico, the possibility that the species still survives
cannot be excluded, and we would classify it as impossible to
assess. Based on this approach, 91 species (45.5%) would be
assessed as not threatened, seven (3.5%) as threatened, 20 (10%)
as extinct, and 82 (41%) as impossible to assess. Note that these
categories are parallel but not identical to the IUCN categories
(Materials and Methods).
Stochastic Modeling Approach Is Congruent with Expert Approach.
Because the method outlined above relies mostly on supposition
derived from interpretation of data and expert opinion and
therefore is somewhat subjective, we compared the results with
those from a mathematical modeling approach that uses collec-
tion records. Similar approaches have been implemented to as-
sess extinction dates of well-known extinct mammal and bird
species (20, 21). We inferred an extinction probability for each of
our 200 species by comparing dates of collection of a species with
overall land snail sampling effort. Dates of sampling of land
mollusks were compiled from the entire collections of four major
museums (SI Discussion), and the number of collection dates was
used as a proxy for sampling effort. The dataset was split into 14
geographic areas (Fig. S2) according to their similarities in terms
of biogeography, history of sampling, and factors driving species
to extinction. A discrete probabilistic model was built (Materials
and Methods and SI Discussion) to estimate three parameters for
each species: a global date of extinction rate shift (S), after which
extinctions become possible, and, for each geographic area, a
probability of extinction per year (μ) and a probability of col-
lecting the species when field work took place (λ) (Fig. 2).
The date Sof the extinction rate shift was estimated by pooling
all species and finding the mean of its a posteriori distribution.
1800 1850 1900 1950 2000
Field Surveys
Successfull Collections
Fig. 1. Collection dates for 200 randomly selected land snail species. Collection dates, recorded from the literature, museum collections, and consultation
with experts for 200 randomly selected land snail species, ordered by date of last collection. Each horizontal line represents all of the collection dates for a
single species from 1786 until 2012. Open circles (; top line) represent all collection dates of mollusks (i.e., proxy for sampling effort). Note the large
proportion of species known only from the original collection (e.g., most species between lines 150 and 200).
| Régnier et al.
The estimate of Sfound by this method is 1894 (Fig. S3). The
historical context can be invoked to explain this result. The end
of the 19th century was the time of the second industrial revo-
lution, that mostly happened in the Western world, but was
concomitant with extensive human colonization of preserved
natural habitat all over the world, such as in North America or in
the midelevation areas of oceanic islands. Because of the pre-
ponderant role of recent extinctions in Polynesia in our data, at
least the second explanation should be considered seriously.
The μand λparameters were estimated independently for
each of the 14 geographic areas. Then, for each species of each
geographic area, using the three estimated parameters, we
computed the ratio of the probability of being currently ex-
tant but not collectedto the probability of being extinctto
assess its status.
The expert and model approaches lead to the same general
result (Fig. 3; Fig. S1), that the number of extinct species is closer
to 7% of biodiversity (130,000 known nonmarine animal species
extinctions out of 1.9 million described species) than to the
0.04% currently suggested by the IUCN Red List [if we accept
the current figure of 799 extinct species in the Red List (5) and
1.9 million named species (13)].
Fig. 3 shows clear heterogeneity in extinction numbers among
geographic areas. In Polynesia, 75% of the sampled species are
considered extinct by both approaches. In North America, where
species have on average much larger ranges than in oceanic is-
lands and are thus less prone to extinction, more than 90% of the
sampled species are extant. Large-range species also occur in
Africa and in South America, but North America is compara-
tively more surveyed, hence the lower number of impossible-to-
assess species.
There are some discrepancies between the results of the two
approaches, but their explanation is straightforward (SI Discus-
sion). Generally, however, the model approach is more pessi-
mistic than the expert one: 25 species should be declared extinct
as opposed to 20, because for some species that were assessed as
extinct by the model, experts suggested that even with recent
surveys in the geographic area considered, lack of data on these
species could be due to lack of surveying effort. For instance, E.
moussonianum (see above) was evaluated as extinct by the model
because there have been unsuccessful surveys in Central Amer-
ica as recently as 2011. However, experts classify it as impossible
to assess because, despite these surveys, so much of Mexico and
Central America, generally, remains insufficiently explored for
mollusks, and recent data are limited regarding species status,
range, and availability of suitable habitat, knowledge that is not
incorporated by the model.
Conservation Status Must Be Assessed for Poorly Known Species.
Both approaches, using available data that cannot be in-
tegrated into the current IUCN evaluation methodology, suggest
that the status of most land snails (and probably nonmarine in-
vertebrates) can indeed be evaluated; if it exists, the expertise of
taxonomists should be used, and natural history museums offer a
wealth of data suitable for the evaluation of conservation status.
With appropriate models, it is possible to allocate a conservation
status to a major proportion of the invertebrate species that
currently languish in the shadows out of the conservation spot-
lights, provided that their biological and ecological characteris-
tics make them suitable for this kind of evaluations. Nonmarine
arthropods in general, and most specifically insects, share such
characteristics with land snails: size, restricted range, rarity, and
specific habitat requirements (22, 23). Moreover, most recorded
extinctions involve island endemic species, and range size and
level of endemism in marine species are poorly documented (24,
25): for these reasons, our approaches should only be extrapo-
lated to nonmarine fauna.
Some may argue that past and current extinction rate pre-
dictions have failed to forecast changes in biodiversity because
current figures do not reflect the dramatic losses that conserva-
tionists had expected to occur 30 y ago (9). Recently, several
studies have attempted to refine such predictions by developing a
better understanding of the major drivers of biodiversity changes
(26, 27), using process-based models and applying them to
groups for which sufficient data exist, i.e., mammals and birds.
The current Red List underestimates the actual number of ex-
tinct and threatened invertebrate species: there are almost seven
times as many extinctions in our sample as would have been
listed following the IUCN criteria, and we suggest that discrep-
ancies of this order of magnitude, or greater, given that mollusks
are one of the better known invertebrate groups, should be
expected for other invertebrate groups. We contend that pro-
jections of species extinction rates are controversial not because
of methodological challenges but because the other 99%of
biodiversity, i.e., invertebrates (11), are continually excluded
from these scenarios. With an extant until proven extinct(28)
approach, any poorly studied taxonomic group or geographic
region is bound to escape the conservation spotlight. However, a
number of studies (17, 29, 30) and our own work suggest that
invertebrate extinctions are mostly overlooked: we suggest that
we have probably already lost 7% of described living species of
the world. On oceanic islands, there is evidence that this per-
centage is much higher (17, 19, 31).
The Red List is primarily a tool for identifying those species
that are most threatened and thus most in need of conservation
action, and it works well for charismatic species (mainly terres-
trial vertebrates) for which it measures levels of threats and
time (in years)
Extinction rate shift (unkown)
Extinction year (unkown)
Last collect (observed)
Last eld survey (observed)
Unsuccessfull Collections (extant species)
Successfull Collections Unsuccessfull Collections (extinct species)
Years without eld survey
Fig. 2. Schematic representation of data used in the probabilistic model for a single hypothetical species. Black circles (), years in which the species was
found; open circles (), years when searches were undertaken but the species was not found; dashes, years in which there were no searches. The year in which
the species was last seen is designated t*, and the year of the last survey is T. Extinction can happen only after year S(year of extinction rate shift), and after
the last successful search. The extinction year (E) is unknown. Given the sampling effort before and after the last collection (number of searches, successful or
not), the model assesses whether not finding a species is due to extinction or to insufficient sampling.
Régnier et al. PNAS Early Edition
success of conservation measures, especially for conservation-
dependent large vertebrates such as the California condor,
mountain gorilla, or white rhino. For mammals and birds, the
IUCN Red List also documents extinction correctly, and the
figure it gives of 1.3% of mammal and bird species being extinct
is probably quite accurate, all these taxa having been thoroughly
evaluated. But the Red List does a poor job of estimating ex-
tinction on a global scale across all taxa and should not be used for
this purpose: there are many documented invertebrate extinctions
that are not in the Red List (17, 32). Our suggestion that 7% of
modern species are extinct is closer to the truth than the 1.3% that
is based only on the species evaluated in the Red List.
Data acquisition for invertebrates is far behind that for ter-
restrial vertebrates, yet the IUCN procedure for categorization
requires that the data processing should be based on the same
categories and criteria as for terrestrial vertebrates. For the bulk
of invertebrates, most of the data are locality and date of col-
lection information currently residing in museum collections and
the personal collections of professional and amateur taxono-
mists. Such data are not readily evaluated against the IUCN
criteria, unlike the ecological and demographic data that are
widely available for terrestrial vertebrates, which are often the
result of studies by numerous scientists on just one or a few species.
However, our aim is not to improve the IUCN Red List ap-
proach or to adapt its criteria for invertebrates. Instead, we
suggest an alternative approach, aimed at measuring levels of
extinction globally (and not at evaluating threats and conserva-
tion actions). Our approach accepts some level of uncertainty for
individual species, but at a large scale, it aims to provide an es-
timate of the true level of extinction, something which is neither
a priority of the Red List nor something that it is designed to
accomplish. The Red List and our approach are not mutually
Fig. 3. Number of mollusk species in our sample assigned to the different extinction risk categories. Assessments are given according to the model pre-
diction, the expert assessment, and the IUCN criteria. The IUCN categories are simplified in this figure such that endangered includes the categories critically
endangered, endangered, and vulnerable, and extant includes the categories least concern and near threatened. Color coding of the model assessments are
graded to reflect the probabilistic nature of the assessments.
| Régnier et al.
exclusive but represent complementary mechanisms for doc-
umenting the biodiversity crisis.
Because the expert and model approaches, which we developed
independently, are remarkably consistent in this study, our estimated
fraction of extinct species appears to be genuinely robust, and this
suggests that the current Red List approach grossly underestimates
the extinction crisis for invertebrates. Either we essentially only as-
sess vertebrates, butterflies, and a few snails using the strict IUCN
criteria, and accept that we have almost no idea for the rest of
biodiversity, or we accept some educated guesses by experts, often
based on museum collection data, and/or inferences made from
proxy data processed through suitable models, to get closer to the
real picture. Model-based analyses are reproducible, quantitative,
and can be rigorously evaluated. Because there has been a steady
effort to render IUCN criteria stricter, quantified, and objective (4),
we believe that adding the model approach to our study constitutes a
step forward in the evaluation of the extinction crisis.
Materials and Methods
Species Sampling. In the absence of a global checklist of the terrestrial
mollusks of the world, we used SchileykosTreatise on Recent Terrestrial
Pulmonate Molluscs (33). We first ordered the genera according to Schileykos
treatment, in which the number of species in every genus is given, allowing us
to generate a list of species numbers from 1 to 17,102. Species and subspecies
were treated similarly, because they both represent distinct, recognizable taxa,
and because subspecies rank is subject to change depending on authors and
species concepts. In the rest of the article, we use the term speciesfor ter-
minal taxa. We then generated 200 random numbers between 1 and 17,102.
For each genus in which one or more of these numbers fell, we generated a list
of all known species (from multiple sources, because Schileyko does not treat
all species individually) and ordered them alphabetically, each named species
in these genera thereby being given a number. We then selected those 200
species corresponding to the original set of 200 random numbers.
Data Compilation.
Bibliographic search. The following online databases were queried to accumu-
late as much published information as possible on the 200 species: Thomson
Reuters (formerly ISI) Web of Knowledge (including Zoological Record), Bio-
diversity Heritage Library, Google Books, Google Scholar supplemented by a
search on Google and manual search in the extensive malacological library at
the Museum National dHistoire Naturelle (MNHN) in Paris.
Museum collections. We augmented the bibliographic data with collection date
and locality information from the online collection databases of four US
natural history museums: Museum of Comparative Zoology, Harvard Uni-
versity; Field Museum, Chicago; National Museum of Natural History,
Washington, DC; Academy of Natural Sciences, Philadelphia. In addition, we
manually searched the collections of the MNHN on site.
For the model approach, we also compiled all of the known collection
dates globally for all terrestrial mollusks from the four museum collection
databases (above).
Consultation with experts. Experts (taxonomists specialized in a given molluscan
family or geographic region; list found in Acknowledgments) were asked
whether (i) they had personally collected the species in the field, (ii ) they
could make an educated guess regarding its conservation status, and (iii)they
were aware of recent indications, published or unpublished, of where and
when this species had been last seen: e.g., published records, museum or
personal collections, or personal field work.
Conservation Status Assessments.
Assessment according to the IUCN categories and criteria. All 200 species were
evaluated according to the IUCN criteria and placed in the appropriate
category (34) (Fig. S1). Even if some relevant informatione.g., indicating a
range reductionwas available for a species, it was considered as data de-
ficient unless we had the minimum set of information required to place it in
one of the other formal IUCN categories. These data included countries of
occurrence, maps showing the geographic distribution, rationale for the
listing (including any numerical data, inferences or uncertainty that relate to
the criteria and their thresholds), current population trends, habitat pref-
erences, major threats, and conservation measures.
Assessment according to the experts. Expert opinion was available for 54 species.
Based on expert field work experience, the species were categorized as not
threatened, threatened, extinct, or impossible to assess (if experts estimated
that not finding a species was possibly due to insufficient search effort and
not to the probable extinction of the species). Note that these categories
differ from the IUCN categories.
For species for which no expert opinion was available, our assessment was
based on the number of dated records and information on their habitat, as
follows: (i) species collected alive at least five times between 1962 and 2012
(i.e., in the previous 50 y) and with no specific habitat threat identified were
evaluated as not threatened; (ii) species not collected in the last 50 y but
with insufficient information on range size and habitat quality were eval-
uated as impossible to assess; and (iii) species not collected in the last 50 y
and occurring in a highly disturbed or vanished habitat shared by other
species already listed by the IUCN as critically endangered or extinct were
evaluated as extinct (Fig. S1).
Assessment according to the probabilistic model.
Data compilation. Collection years were compiled for each species in each
geographic area (Fig. S2). We use the term Polynesiafor the sake of
simplicity, although our data are from both Polynesia and Micronesia. In
addition, for each geographic area A, all years in which mollusk sampling
occurred were listed. These two lists were taken from the databases of the
four US museums listed previously. For each species, each survey date twas
then tagged by a 1 if the species was collected, or a 0 if otherwise.
Model. The model is diagrammed for one species in one geographic area in Fig.
2. We define Sas the date at which extinction becomes possible. Each species
extant at year ySin geographic area Acan independently become extinct
between year yto year y+1 with a constant probability μ
probability of extinction is assumed to be 0. Sis therefore the date of the ex-
tinction rate shift. We also assume that, at each survey date t, each extant species
in the geographic area A, independently, is successfully collected with a constant
probability λ
. We assume that λ
and μ
only depend on the geographic area A
and that Sis identical for all species and all geographic areas. A species that has
been observed most recently at date t* is necessarily extant up until t*.In
mathematical terms, we have E>t*,whereEis the unknown date of extinction
of this species. There are two reasons why a species is not observed in a survey
subsequent to t*: the species is extant but was not collected (i.e., the survey
preceded E)orthespeciesisalreadyextinct(i.e.,Epreceded the survey). We
define Tas the date of the last survey (successful or not). We define n
as the
number of survey dates on which the species has been collected, and n
as the
number of survey dates prior or equal to year yon which the species was not
collected; given this, the likelihood of the data for one species is given by
E=maxðt+1, SÞ
Pooling species within the same geographic area A, the likelihood of the
data are the product of the above likelihoods over all species in A(this as-
sumes species are independent replicates).
Statistical inference. Our goal was to infer a single Sfor all data together
and (λ,μ) for each geographic area. We first estimated jointly
S,^μ, and
all geographic areas pooled (i.e., using worldwide information). Second, we
fixed Sto
S, and estimated for each geographic area ^μAand
λA. To compute
S, we explored parameter space by Markov chain Monte Carlo (MCMC) with
all geographic areas pooled. We used a uniform prior for Sin [1800, 1950]
and a uniform prior in [0, 1] for both λand μ. We selected as proposal dis-
tributions of the MetropolisHastings algorithm the uniform distribution in
[0, 30] for Sand the uniform distribution in the log-scale between 0.1 and
0.0001 for λand μ. We performed an optimization by maximum likelihood
before running the MCMC to focus on the interesting region of parameter
space. We discarded the first 100 steps of the chain as burn-in, and sampled
1,000 values every 20 steps. We checked the convergence of the distributions
visually. The posterior Sdistribution showed a clear mode around 1900 and a
mean of the distribution of 1893.96 (Fig. S3). Consequently, we set Sto 1894
for all further parameter estimation. We were not able to retrieve Sfor each
geographic area independently, presumably because of a lack of signal. For
each area, we then ran an independent MCMC to estimate λ
and μ
To characterize the probability of being extant or extinct, we computed,
for each species, the likelihood ratio (LR) of the chance it went extinct since it
was observed at t* to the chance of being extant but not found since t*.
More precisely, LR is defined as
Régnier et al. PNAS Early Edition
LR =1ð1^μAÞTt*
LR is a continuous positive variable, and gives an indication of the current
conservation status of the species: the higher it is, the higher is the probability
that the species is extinct. However, to assign conservation status, two thresholds
were arbitrarily chosen for LR: when LR is above 10 (i.e., there is a 10×greater
probability that the species is extinct than that it is extant but not found), we
suggest that the species should be declared extinct; when LR is below 0.1 (i.e.,
there is a 10×greater probability that the species is extant but n ot found than
that it is extinct), we suggest that the species should be declared extant.
Between 0.1 and 10, we declare the species impossible to assess.
To check the MCMC algorithm performance, we built 10 random replicates
of time series, for each species, keeping the survey dates as they are, but
randomlydrawing the extinction dates (using a geometric distribution with the
estimated μ
) and subsequently the successful surveys (using Bernoulli trials of
parameter λ
before the extinction date). The results show that the MCMC
algorithm performs well, estimating values (λ
) that are close to those set
in the simulations (Fig. S4).
ACKNOWLEDGMENTS. We acknowledge contributions and data sharing from
G. M. Barker, A. S. H. Breure, A. C. van Bruggen, C. C. Christensen, D. J. D. Chung,
R. Clements, J. Espinosa, A. Fernández Velázquez, J. Gerber, E. Gittenberger,
J. Grego, O. Griffiths, M. G. Hadfield, D. Herbert, Y. Kano, W. Maassen, B. Marshall,
F. Naggs, E. Neubert, T. A. Pearce, D. Raheem, B. Roth, B. Rowson, R. J. Rundell,
M. Severns, J. Stanisic, F. G. Thompson, R. Ueshima, D. Uit de Weerd, A. J. de
Winter, and M. Wu. R. Cameron and R. Hershler reviewed an earlier draft of the
manuscript. We thank H. Annoni for the design of Fig. 3. We thank C. Fontaine,
S. Languille, and H. Le Guyader for comments that improved the manuscript. This
work was supported by French National Research Agency Losers Project Grant
ANR-09-PEXT-007 (to P.B.).
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| Régnier et al.
... Rapid biodiversity loss in association with anthropogenic impact, including habitat fragmentation, habitat loss, invasive species, over-exploitation, and environmental change (Shaffer 1981;Butchart et al. 2010) are contributing to an alarming increase in numbers of species that require conservation management (Régnier et al. 2009(Régnier et al. , 2015. A necessary component for effective conservation is the accurate detection and delineation of species diversity (Mace 2004). ...
... Strategic use of genomic methods can be used to answer key conservation questions that could impede conservation management decisions (Allendorf et al. 2010;Ouborg et al. 2010;Cook and Sgrò 2017), especially in species that are rare, cryptic, or non-charismatic as they are often largely data deficient (Howard and Bickford 2014;Régnier et al. 2015;Cowie et al. 2017). For instance, although molluscs have been determined to one of the most at risk taxa (Régnier et al. 2009;Johnson et al. 2013;Cowie et al. 2017;Böhm et al. 2020), only a small proportion of mollusc species (~10%) have been assessed by the International Union of Conservation of Nature (IUCN) and of these ~35% were deemed data deficient to make a formal assessment (Cowie et al. 2017). ...
Full-text available
Determining cryptic species and diversity in at-risk species is necessary for the understanding and conservation of biodiversity. The endangered Banff Springs Snail, Physella johnsoni, inhabits seven highly specialized thermal springs in Banff National Park, Alberta, Canada. However, it has been difficult to reconcile its species status to the much more common Physella gyrina using ecology, morphology and genetics. Here we used pooled whole-genome sequencing to characterize genomic variation and structure among five populations of P. johnsoni and three geographical proximate P. gyrina populations. By comparing over two million single nucleotide polymorphisms, we detected substantial genetic distance (pairwise FST of 0.27 to 0.44) between P. johnsoni and P. gyrina, indicative of unique gene pools. Genetic clusters among populations were found for both species, with up to 10% for P. johnsoni and 30% for P. gyrina of genetic variation being explained by population structure. P. johnsoni was found to have lower genetic diversity compared to P. gyrina, however, no patterns of were observed between genetic diversity and population minimums. Our results confirm that designation of P. johnsoni as an endangered species is warranted and that both P. johnsoni and P. gyrina exhibit microgeographic population genomic structure suggestive of rapid local adaptation and/or genetic drift within environments. This study showcases the utility of genomics to resolve patterns of cryptic species and diversity for effective conservation management. Future studies on the functional genomic diversity of P. johnsoni populations are needed to test for the possible role of selection within this thermal spring environment.
... Even so, this approach only considers species with readily available information; it is therefore biased. To overcome this bias, Régnier et al. (2015a) developed an alternative approach using a random global sample of land snails. They found that, based on expert opinion and a probabilistic model, respectively, 10% and 12.5% of land snail species in the random sample should be classified as Extinct. ...
... In 1983, 123 mollusc species were evaluated for the IUCN Red List, 6 of them deemed Extinct. By 2019, 300 of 8664 species evaluated were deemed Extinct (IUCN, 2019), although more realistic estimates of the number of extinctions are much higher (Régnier et al., 2009(Régnier et al., , 2015aCowie et al., 2017). Molluscs face diverse threats but because most are not 'charismatic', efforts to stem the rate of extinction and ameliorate the threats face an uphill battle. ...
Since 1970, there has been an overall decline in wildlife populations in the order of 52%. Freshwater species populations have declined by 76%; species populations in Central and South America have declined by 83%; and in the Indo-Pacific by 67%. These are often not complete extinctions, but large declines in the numbers of animals in each species, as well as habitat loss. This presents us with a tremendous opportunity, before it is too late to rescue many species. This book documents the present state of wildlife on a global scale, using a taxonomic approach, and serving as a one stop place for people involved in conservation to be able to find out what is in decline, and the success stories that have occurred to bring back species from the brink of extinction - primarily due to conservation management techniques - as models for what we might achieve in the future.
... It is particularly effective for assessing the diversity of little known invertebrate groups and for detecting cryptic species (Vieites et al., 2009;Janzen et al., 2017). Efficient species identification and monitoring are critical for accurate monitoring of species loss, as unrecorded diversity can lead to substantial underestimation of extinction (Régnier et al., 2015;Cowie et al., 2022). However, DNA barcodes sometimes fail, so it is essential understand the cause of misidentifications in order to be able to apply these tools more effectively. ...
DNA barcoding often fails to identify species despite its undisputed advantages. Hybridization, sample contamination, incomplete lineage sorting and nuclear copies of mitochondrial genes (NUMTs) are often put forward as explanations but have seldomly been tested. Here I used available RNA-sequencing data to explore this issue in four Chorthippus grasshopper species. I was able to exclude NUMTs, contamination and recent hybridization as probable causes of the low barcoding performance. Using a phylogenetic method, I estimated the nuclear and mitochondrial mutation rates as 1.31 × 10−9–2.27 × 10−9 and 8.1 × 10−9–1.4 × 10−8 mutations/site/year, respectively. These grasshoppers therefore did not exhibit a particularly low mitochondrial mutation rate compared to other insect species. Using coalescence simulation, I was able to show that two simple demographic scenarios, with a divergence period of 1–3 Myr, provided a good fit to the mitochondrial genealogies in three of the four target species. Interestingly, the mitochondrial genealogy of Chorthippus mollis was inconsistent with a neutral evolution pattern, suggesting that it had undergone adaptive selection.
... But despite invertebrates accounting for over 95% of all animal diversity (Cardoso et biodiversity hotspots, but there have been mass extinctions in many groups (e.g. Solem et al. 1990; Cowie 1992Cowie , 2001Régnier et al. 2009Régnier et al. , 2015aRégnier et al. , 2015bSartori et al. 2012;Richling & Bouchet 2013). Conservation efforts have been insu cient because of inadequate knowledge of species diversity, distributions and biology; these inadequacies must be addressed to better conserve the remaining species (Solem 1990 There has been interest in developing non-lethal sampling methods for rare snails, but studies to date have only tested a few species. ...
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Sampling the DNA of rare animal species should have minimal impacts on individual health. This can be accomplished through non-lethal/non-invasive sampling. Few of these methods have been developed for invertebrates, including the Mollusca, which are in global decline. Tissue clipping the foot is a common non-lethal method for gastropods. However, it causes permanent damage and is inappropriate for smaller snails. This study used Flinders Technology Associates (FTA) cards to sample DNA from snail mucus for species of different sizes and habitat types, and across evolutionarily distant lineages. In a survival assay, the death rate of individuals sampled with FTA cards (12.1%) was greater than in the controls (3.7%), but the difference was not significant. Of 224 individuals representing 27 snail species (17 Hawaiian native, ten non-native) sampled using both FTA cards and tissue clipping, 80.4% of FTA samples and 91.6% of tissue samples amplified for COI, a significant difference. COI sequencing success did not differ significantly between the two methods. For individuals that failed to produce a COI sequence, an attempt was made to sequence 16S. For 16S, amplification and sequencing rates did not differ significantly between FTA and tissue samples. Habitat type and shell size did not affect FTA sampling success. Phylogenetically basal taxa exhibited lower success rates, but this may have been because of difficulty in sampling operculate taxa, and not because of identity. These results indicate that the FTA sampling is a viable non-lethal alternative to tissue clipping and can be used for diverse gastropods.
... However, in many regions of the world, the necessary our understanding of the biology and systematics of these animals' ranges from absent in many areas [8]. Many Asian River basins have never been surveyed and home to numerous undescribed genera and species (e.g., [9,10]) that may even g before being described or studied [11][12][13][14]. Despite being poorly known, the fre mussel fauna of Asia has recently attracted intense research interest, especially i omy, phylogeny, and biogeography (e.g., [8,10,[15][16][17][18][19][20][21][22][23][24][25]). ...
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The basic knowledge of freshwater bivalves in the Unionida in some regions of the world is still limited, hindering potential conservation efforts, including in Vietnam. A subset of these mussels, the freshwater bivalve tribe Anodontini, is especially difficult to properly identify morphologically due to intraspecific shell similarity. This study aims to define the species of Anodontini in Vietnam and describe their evolutionary relationships and distributions by estimating phylogenies and analyzing collected specimens. The Anodontini are represented in Vietnam by five species divided among three genera: Sinanodonta, Cristaria, and Pletholophus. Sinanodonta woodiana, a large species complex, is represented in Vietnam by Sinanodonta jourdyi. Cristaria is confirmed to include the widespread Cristaria plicata and substantiates the validity of Cristaria truncata. Finally, Pletholophus is here recognized as distinct from Cristaria, containing two species in Vietnam, Pletholophus tenuis, and a species new to science. Our study is an important baseline for future studies on Vietnamese freshwater mussels and highlights the importance of surveys, molecular work, and taxonomic expertise to describe the biodiversity of understudied regions.
... The threats to species are not equal, and largebodied species [3], as well as species with narrow spatial ranges [4], are principally impacted. The toll on species is staggering [5], and between 900 and 130,000 species have become extinct since the 1500s (; accessed on 3 May 2023). ...
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Simple Summary What does not have a name is difficult to understand and protect. Upon the unexpected discovery of an Hynobius salamander in Fujian province, China, we worked on understanding its relationship with other species and ultimately describing it. Please welcome the Fujian Bamboo Salamander to science, a segregated species based on genetics and morphology. While it is related to other southern mainland Chinese species, it may have diverged earlier and share some similarities with morphology and behavior with the Anji salamander. The Fujian Bamboo Salamander is special as it produces vocalization when under threat. The species is, however, incredibly rare, fitting the definition of Critically Endangered in the IUCN Red List of Threatened Species. Abstract It is important to describe lineages before they go extinct, as we can only protect what we know. This is especially important in the case of microendemic species likely to be relict populations, such as Hynobius salamanders in southern China. Here, we unexpectedly sampled Hynobius individuals in Fujian province, China, and then worked on determining their taxonomic status. We describe Hynobius bambusicolus sp. nov. based on molecular and morphological data. The lineage is deeply divergent and clusters with the other southern Chinese Hynobius species based on the concatenated mtDNA gene fragments (>1500 bp), being the sister group to H. amjiensis based on the COI gene fragment, despite their geographic distance. In terms of morphology, the species can be identified through discrete characters enabling identification in the field by eye, an unusual convenience in Hynobius species. In addition, we noted some interesting life history traits in the species, such as vocalization and cannibalism. The species is likely to be incredibly rare, over a massively restricted distribution, fitting the definition of Critically Endangered following several lines of criteria and categories of the IUCN Red List of Threatened Species.
... Hence, abundance data remain rare for many species, including threatened species (Cardoso et al., 2012;Bachman et al., 2019;Cowie et al., 2022). Species distribution models (hereafter, SDM), which offer the advantage of using only occurrence data, constitute the only basis for conservation status assessment in many species (Cardoso et al., 2012;Régnier et al., 2015). Here, we define SDMs as correlative models that relate species occurrence data to environmental variables. ...
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Habitat Suitability Index (HSI) derived from Species Distribution Model (SDM) has been used to infer or predict local demographic properties such as abundance for many species. Across species studied, HSI has either been presented as a poor predictor of abundance or as a predictor of potential rather than realized abundance. The main explanation of the lack of relationship between HSI and abundance is that the local abundance of a species varies in time due to various ecological processes that are not integrated into correlative SDM. To better understand the HSI-abundance relationship, in addition to the study of the association between HSI and mean abundance, we explored its variation over time. We used data from 10-years monitoring of a Houbara bustard (Chlamydotis undulata undulata) population in Morocco. From various occurrence data we modelled the HSI. From (independent) count data we calculated four local abundance indices: mean abundance, maximum abundance, the temporal trend of abundance and the coefficient of variation of abundance over the study period. We explored the relationship between HSI and abundance indices using linear, polynomial and quantile regressions. We found a triangular relationship between local abundance (mean and maximum) and HSI, indicating that the upper limit of mean and maximum abundance increased with HSI. Our results also indicate that sites with the highest HSI were associated with least variation in local abundance, the highest variation being observed at intermediate HSI. Our results provide new empirical evidence supporting the generalization of the triangular relationship between HSI and abundance. Overall, our results support the hypothesis that HSI obtained from SDMs can reflect the local abundance potentialities of a species and emphasize the importance of investigating this relationship using temporal variation in abundance.
Aim We aimed to apply ontological techniques to address semantic ambiguities in protected area and conservation informatics. By doing so, we aimed to create a coherent, machine‐actionable semantic representation of the biogeographic areas (which often overlap protected areas) to support more efficient and standardized informatics, supporting research and decision‐making. We present BIOREALM, the first informatic ontology for comparative biogeography. Location Global. Taxon Any taxon can be integrated in BIOREALM. Methods We convert a cladogram of biogeographic areas—generated by a process known as bioregionalization—into a series of ontological classes. Areas of endemism are treated as formal objects related by hierarchical relationships and constrained by a condition of monophyly. We use semantic web approaches to extend the Environment Ontology (ENVO) with classes for (often semantically confounded) biogeographic entities, including biogeographic areas, areas of endemism and endemic areas. We applied this approach to a bioregionalization of Australia as a case study. In all, 20 subregions which are part of the Austral Bioregionalisation Atlas have been selected for the study and integrated in BIOREALM. Results We have created an ontology—formatted in the Web Ontology Language and adhering to the practices of the Open Biomedical and Biological Ontology Foundry—which provides a rigorous, extensible and machine‐actionable framework that can improve biogeographic analyses and interoperability between systems. One main class and 20 individuals per class were implemented. Main Conclusions BIOREALM encodes a model‐theoretic view of endemism using semantic web approaches, offering new avenues to express and analyse biogeographic units. This approach offers a means to identify monophyletic biogeographic areas for conservation, based on specific combinations of monophyletic endemic taxa. Such an ontology provides knowledge representation solutions which supports interoperability along the FAIR (Findable, Accessible, Interoperable, Reusable) principles, thus fostering more consistent ecological informatics.
The current geologic era—the Anthropocene—is defined by human-driven transformation of landscapes and seascapes that has profoundly altered Earth’s climate and other life-support systems. This letter advocates for a landscape-scale regenerative tourism management strategy aimed at transforming coastal destinations into carbon sinks (meaning they sequester more carbon than they release). Specifically, coastal destinations can transform product offerings into a network of restoration projects that collectively seek the landscape-scale restoration of blue carbon ecosystems such as marshes, mangroves, and seagrass meadows. Restoration of blue-carbon ecosystems is a cost-effective way to mitigate the effects of climate change. Tourism has potential to overcome obstacles in large-scale restoration of blue carbon ecosystems and can play a foundational role by providing a long-term presence at restoration sites, logistical and human resources, and a business model dependent on restored ecosystems.
Most extinctions estimated to have occurred in the historical past, or predicted to occur in the future, are of insects. Despite this, the study of insect extinctions has been neglected. Only 70 modern insect extinctions have been documented, although thousands are estimated to have occurred. By focusing on some of the 70 documented extinctions as case studies, I considered ways in which insect extinctions may differ from those of other taxa. These case studies suggested that two types of extinction might be common for insects but rare for other taxa: extinction of narrow habitat specialists and coextinctions of affiliates with the extinctions of their hosts. Importantly, both of these forms of extinction are often ignored by conservation programs focused on vertebrates and plants. Anecdotal evidence and recent simulations suggest that many insect extinctions may have already occurred because of loss of narrow habitat specialists from restricted habitats and the loss of hosts. If we are serious about insect conservation, we need to spend more time and money documenting such extinctions. To neglect such extinctions is to ignore the majority of species that are or were in need of conservation.