Research article 1
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The dynamics underlying avian extinction trajectories forecast a wave of extinctions 3
Melanie J. Monroe1,2,3, Stuart H. M. Butchart4,5, Arne O. Mooers2, Folmer Bokma1,6* 4
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1Center for Ecological and Evolutionary Synthesis (CEES) Department of BioSciences, University of 6
Oslo, PO Box 1066, Blindern, 0316 Oslo, Norway.
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2Department of Biological Sciences and the IRMACS Center for Interdisciplinary Research, Simon Fraser 8
University, 8888 University Drive, V5A 1S6, Burnaby, BC, Canada.
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3Department of Ecology and Genetics, Evolutionary Biology Center (EBC), Uppsala University, 10
Norbyvägen 18D, 752 36 Uppsala, Sweden.
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4BirdLife International, David Attenborough Building, Pembroke Street, CB2 3QZ, UK.
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5Department of Zoology, University of Cambridge, Downing Street, CB2 3EJ, UK.
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6Department of Ecology and Environmental Science and IceLab, Umeå University, 90187 Umeå, 14
Sweden. Current address: 1.
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*Corresponding author. Email: [email protected].
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Abstract 17
Population decline is a process, yet estimates of current extinction rates often consider just the final step 18
of that process by counting numbers of species lost in historical times. This neglects the increased 19
extinction risk that affects a large proportion of species, and consequently underestimates the effective 20
extinction rate. Here we model observed trajectories through IUCN Red List extinction risk categories for 21
all bird species globally over 28 years, and estimate an overall effective extinction rate of 2.17 x10-4 22
/species/year. This is six times higher than the rate of outright extinction since 1500, as a consequence of 23
the large number of species whose status is deteriorating. We very conservatively estimate that global 24
conservation efforts have reduced the effective extinction rate by 40%, but mostly through preventing 25
critically endangered species from going extinct rather than by preventing species at low risk from 26
moving into higher risk categories. Our findings suggest that extinction risk in birds is accumulating 27
much more than previously appreciated, but would be even greater without conservation efforts.
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1. Introduction 30
Recent global biodiversity loss is estimated to be at least one hundred times pre-human levels [1–3].
31
However alarming, these estimates may be too optimistic [4]. Estimates of current or recent extinction 32
rates have typically been based on the numbers of species within a particular group that we know or 33
suspect to have gone extinct over a set period of time [5,6]. However, this simple calculation combines 34
species that are currently not at risk with those whose populations are declining but that have not yet been 35
lost [7]. Given that species must decline from "not at risk" through various levels of risk before 36
extinction, including these trajectories in calculations would offer a more comprehensive measure of 37
ongoing extinction dynamics. Here we estimate the overall effective extinction rate from changes in the 38
IUCN Red List [8] categories of extinction risk for all 11 064 recognized avian species over 28 years 39
(1988-2016), and assess the impact of conservation efforts on this rate.
40 41
2. Methods 42
The IUCN Red List uses seven categories to classify extinction risk: least concern (LC), near threatened 43
(NT), vulnerable (VU), endangered (EN), critically endangered (CR), extinct in the wild (EW) and extinct 44
(EX). The classification of a species changes if it becomes more or less threatened over time, and we 45
assume that this process can be modelled as a time-homogeneous Markov process with annual transition 46
matrix Q. (We found no evidence of a trend over time that suggests a more complex model to better 47
describe the data.) This process has EX as the absorbing state, because once a species is extinct, it will not 48
re-appear.
49 50
The ongoing rate of extinction is calculated from Q, using standard Markov chain theory [9], as follows:
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Let R denote the 6x6 transient segment of Q, that is, Q without the row and column EX (Table 1). The 52
matrix F=(I-R)-1, where I is the identity matrix, is the fundamental matrix of Q: entry fij of F is the 53
expected number of times that a species currently in the i-th category will be in the j-th category before 54
going extinct. The expected time until extinction for each transient starting state is therefore T=Fc, where 55
c is a 6x1 column vector of ones. Let K be a 1x6 vector with fractions describing the current distribution 56
of species over the transient extinction risk categories (K=1; Table 1). The average time to extinction is 57
then KT, and the rate of extinction is the inverse of the average time to extinction: (KT)-1. Thus, we can 58
calculate the scalar extinction rate from transition matrix Q, which is based on transitions between all 59
extinction risk categories, not just between the most threatened categories and EX.
60 61
We estimated Q from the extinction risk categories of 11 064 bird species in 1988, 1994, 2000, 2004, 62
2008, 2012, and 2016 (the years in which the status of all species has been assessed;) according to the 63
IUCN Red List, which is based on data provided by BirdLife International [10,11]. Improved knowledge 64
about taxonomy or threat factors was retroactively applied [10,12] (Supplementary Data). We used a 65
Bayesian algorithm (Supplementary Material), which allowed us to take into account uncertainty about 66
the status of species, including those tagged as ‘possibly extinct’ or ‘possibly extinct in the wild’.
67 68
3. Results 69
From our estimate of the full matrix Q (Table 1), we estimate the expected time to extinction per species 70
and therefore its inverse, the per-species, per-year extinction rate: the global average across all birds in 71
2016 was 4780 years (95% credible interval: 3418-7093). (Henceforth, intervals following estimates are 72
95% credible intervals.) This corresponds to an overall extinction rate of 2.17∙10-4 (1.41-2.92∙10-4) sp-1y-1 73
(≈ 2090 E/MSY [13] but see Supplementary Methods). Because times to extinction are exponentially 74
distributed, the median time to extinction is considerably shorter than the mean: 50% of present-day 75
species would be lost already after loge(2)∙4780=3313 (2369-4917) years. This is a 1000-fold shorter than 76
the 3 My estimate for pre-human avian species durations [14].
77 78
Prob. (x 10-4 yr-1) of transition to category: Lifetime T (years)
From: LC NT VU EN CR EW EX #spp K(%) with conserv. without conserv.
LC 9993 5 2 0 0 0 0 8417 76.0 5161 (3770 – 7502) 3347 (2736 – 4287) NT 6 9967 24 1 3 0 0 1017 9.2 3959 (2544 – 6230) 2161 (1578 – 3062) VU 1 11 9950 33 5 0 0 786 7.1 3432 (2090 – 5664) 1691 (1140 – 2566) EN 0 6 18 9937 37 1 0 461 4.2 3054 (1696 – 5253) 1371 (839 – 2241) CR 1 1 6 57 9898 32 5 222 1.8 2503 (1226 – 4612) 1015 (537 – 1849) EW 2 2 4 14 142 9679 156 5 0.1 1366 (482 – 2997) 598 (252 – 1249)
EX 0 0 0 0 0 0 104 156 0 0
weighted average: 4780 (3418 – 7093) 2985 (2400 – 3893)
Table 1. Annual rates at which bird species moved between IUCN Red List categories. The values are based on 79
genuine movements between categories (see text for abbreviations) from the years 1988-2016. For example, the 80
value in row NT and column VU is the probability (0.0024) that a species currently classified as NT will next year 81
be classified as VU. Thus, values across each row sum to one (with rounding errors). Shading intensity indicates the 82
magnitude of transition rates, with reds denoting movement to higher, and greens denoting movement to lower, risk 83
levels. #spp gives the numbers of currently recognized species per category in 2016, including extinct species, and 84
K is the distribution of species over categories in 2016 excluding species already extinct. CR includes CR(PE) and 85
CR(PEW). Lifetime T is the expected time to extinction in years for a species currently in a given category (see 86
Methods). “with conserv.” is the scenario where rate estimates include both up- and down-listings between 87
extinction risk categories. “without conserv.” is the scenario where estimates exclude those down-listings that were 88
the result of conservation efforts.
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90
Importantly, our Q-based estimate of the time to extinction, which takes into account transition rates 91
between all categories from LC through EX, is much shorter than traditional estimates that only count 92
transitions to EX. To illustrate the underestimation of the extinction rate caused by lumping all non-EX 93
categories and considering only transitions between “non-EX” and EX, we can sum the product of the 94
columns labelled “EX” and “K” in Table 1 to get the per-year extinction probability of an average 95
species: 1/24 492 (1/42 788 - 1/15 983) sp-1y-1. Thus, lumping all non-EX categories causes a 96
24492/4780=5-fold (3.4-8.5) overestimation of the time to extinction, because it neglects the net tendency 97
for species at low risk to move into higher risk categories. More directly, consider that during the past 500 98
years, about 187 of 11 064 avian species are documented to have gone extinct[15]. If the per species per 99
year probability of extinction is pe, then the fraction of species expected to be extinct after 500 years is 1- 100
(1- pe)500. Equating that fraction to 187/11 064 yields an expected time to extinction of pe-1 = 29 333 101
years: six times longer (4.1-8.6) than our current estimate based on Q.
102 103
To illustrate how the tendency for low-risk species to move to higher risk categories affects the extinction 104
rate, we used the matrix product QK (see Methods) to project the classification of the present-day species 105
far into the future (Fig.1). We emphasize that this is an illustration of the process currently taking place 106
and not a prediction of what will happen in the future, because Q would not remain constant over such 107
long time periods. During the next 500 years, this approach suggests that 471 (226-589) species would go 108
extinct, about three times as many as we have lost over the past 500 years. About 109 of these are 109
projected to be species currently classified as “least concern”. The graver problem is that most species 110
become more threatened. This build-up of extinction risk [16] then causes a sharp increase in the number 111
of extinctions. Using the current Q, this would last for about 2000 years, after which the wave gradually 112
fades as ever fewer species remain under this illustrative model.
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< Figure 1 goes here >
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116
To gain insight into the overall effect of global conservation efforts [3,17] from 1988 to 2016, we 117
estimated Q excluding category changes for species whose status, owing to conservation action, improved 118
sufficiently to qualify for down-listing to a lower Red List category, but including category changes for 119
six species down-listed due to natural factors (Supplementary Table 1). As expected, conservation has had 120
the largest impact on the most threatened categories (Table 1). For instance, the fate of species 121
categorized as CR may seem less dire based on recent trajectories than their category implies, because 122
they are twice as likely to improve as to deteriorate (Table 1). Without conservation, however, these 123
species are twice as likely to deteriorate as to improve (Supplementary Table 2). Conservation efforts 124
resulting in the “down-listing” of a single species from CR to EN extend that species’ expected time to 125
extinction by 551 years, from 2503 to 3054 years under our model (Table 1). Efforts targeting CR species 126
increase the expected time to extinction of LC species as well, because these will become CR before 127
going extinct. Thus, global conservation efforts have increased the projected time to extinction of the 128
world’s bird species by 1795 (44-4045) years per species, from 2985 to 4780 years (Table 1), resulting in 129
40% (1.4-60%) reduction of the effective extinction rate. These estimates (Supplementary Table 2) are 130
very conservative because they consider only conservation efforts that resulted in improvements in status 131
that were of sufficient magnitude to down-list species to lower categories of risk, while conservation 132
actions presumably more often allow species to remain in their current category or to transition to more 133
threatened categories at a lower rate [18].
134 135
4. Discussion 136
Red List assessments of extinction risk are based on a broad literature on population demography [19] so 137
that different species may qualify under a particular IUCN Red List category for very different reasons 138
and may have substantially different population sizes, range extents, and threatening factors. Due to 139
inaccurate estimates of e.g. population size, rate of decline or extent of occurrence, or due to time-lags in 140
information reaching Red List assessors, some assessments will be erroneous. It is challenging to model 141
such error. We assumed that species may be erroneously classified in a category adjacent to the true 142
category, including the distinction between CR and EX, although Red List assessors are very cautious 143
about assigning taxa to EX. (Most media stories about ‘lazarus’ bird species relate to species still 144
classified as Critically Endangered, rather than Extinct.) Compared with assuming that assessments are 145
error-free, our modelling of error yields lower estimates of extinction rate (Supplementary Material).
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Furthermore, deteriorations in status are more likely to go undetected than improvements, because species 147
benefiting from conservation action tend to be well monitored, such that our estimates of the rates at 148
which species are moving towards extinction may be conservative. Because some extinction risk 149
categories contain few species, estimates of their transition rates are also influenced by the choice of 150
prior. Appropriate choice of priors and modelling of assessment error will therefore likely be crucial to 151
better estimate current extinction rates.
152 153
Importantly, however, transitions of large numbers of species through broad classes of relative extinction 154
risk [19] provide useful information on the dynamics of extinction given the diversity and pattern of 155
human impacts on the natural world. As shown in the Supplemental Material, relaxing simplifying 156
assumptions of the model or using alternative priors on transition rates and classification error has little 157
effect on estimates of the extinction rate compared with estimates that treat all extant species as secure.
158
Comparatively few avian species are currently critically endangered [8] and many of these appear to be 159
benefiting from conservation efforts [5,12,20,21], so failure to account for species becoming more 160
threatened leads to considerable underestimation of effective extinction risk. We expect that analyses for 161
other taxa would show similar patterns. Most other taxa are less well studied than birds and contain a 162
significant proportion of data deficient species, which complicate risk assessment [22]. In such cases 163
information about e.g. ecology, geography[23], traits[24], and phylogeny[25] could be combined to 164
assign prior probabilities to the categorization of these species.
165 166
The build-up of potential future extinction should inform discussions underpinning international 167
conservation obligations such as through the UN Convention on Biological Diversity's Aichi Targets [26].
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Conservation efforts have mainly targeted species that are already threatened. According to our 169
calculations (Table 1), these efforts have considerably extended the projected time to extinction of all 170
avian species, because all species become threatened before going extinct. However, such efforts may not 171
be the most cost-effective strategy in the long term [27] because they do not prevent least concern species 172
from becoming more threatened, and thus do not prevent increasing numbers of species in immediate 173
need of conservation. Therefore, it is important that any post-2020 biodiversity framework negotiated 174
through the Convention includes a renewed target to prevent extinctions, but, as emphasized by our 175
analyses, also to prevent non-threatened species or those at low risk from moving into higher risk 176
categories, i.e. keeping common species common and improving the status of currently threatened 177
species. This latter emphasis would help dampen an ever-building wave of conservation need.
178 179
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Acknowledgements: We thank the many thousands of individuals and organizations who contribute to 248
BirdLife’s assessments of all the world’s birds for the IUCN Red List. We thank Karen 249
Magnusson-Ford for research assistance, and Giulio Della Riva and Simon Whelan for discussion, 250
as well as three reviewers for many valuable comments. Funding was provided by the Swedish 251
Research council (VR) (MJM, grant number 637-2013-274) and NSERC Canada (AOM).
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Author Contributions: MJM and FB conceived the study. SMB oversaw data collection and compiled 253
the data set. MJM prepared data for analysis. FB developed algorithms and analysed the data. AOM and 254
FB interpreted results and designed model comparisons. MJM, FB and AOM framed and wrote the 255
manuscript with input from SMB. All authors approved the final version and agree to be held accountable 256
for the work it presents.
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Accessibility: The data and code used in this study are available as supplementary information.
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Competing Interests: The authors declare no competing interests.
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Ethical Statement: This article does not present research with ethical considerations.
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Figure legend 261
Fig.1. Illustration of ongoing bird extinction dynamics as implied by the rate matrix Q, based on the rates 262
at which bird species have moved between IUCN Red List categories from 1988 to 2016. We project 263
these dynamics to illustrate how current bird species diversity would hypothetically decrease in the future 264
given recent trends, rather than to represent realistic predictions, because Q is unlikely to remain constant 265
over this time period. Solid lines: projected extinctions based on Q estimated using all observed category 266
transitions. Dashed lines: projected extinctions based on Q estimated without category transitions 267
attributed to conservation efforts. (A) Projected yearly number of extinctions, which first rise as the 268
extinction wave passes, and then ultimately falls as the pool of species shrinks. (B) Projected changes in 269
the numbers of species in each extinction risk category, with (C) showing magnified detail over the first 270
500 years during which many species become more threatened.
271