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Two major extinction events in the evolutionary history of turtles: one caused by a
meteorite, the other by hominins
Anieli G. Pereira1,2,3,*; Alexandre Antonelli1,2,4,5; Daniele Silvestro1,2,6,7,†; Søren Faurby1,2,†
Affiliations: 1Department of Biological and Environmental Sciences, University of Gothenburg,
Box 461, SE 40530, Göteborg, Sweden; 2Gothenburg Global Biodiversity Centre, Box 461, SE
40530 Göteborg, Sweden; 3Department of Biology, FFCLRP, University of São Paulo, Ribeirão
Preto, São Paulo, Brazil; 4
Royal Botanic Gardens, Kew, Richmond, Surrey, TW9 3AE, U.K.;
5Department of Plant Sciences, University of Oxford, South Parks Road, OX1 3RB Oxford,
U.K.; 6Department of Biology, University of Fribourg, 1700 Fribourg, Switzerland; 7Swiss
Institute of Bioinformatics, Quartier Sorge, 1015 Lausanne, Switzerland
† Both authors contributed equally
emails: AGP: anieligpereira@gmail.com; AA: a.antonelli@kew.org; DS:
daniele.silvestro@unifr.ch; SF: soren.faurby@bioenv.gu.se.
*Correspondence: Anieli G. Pereira: anieligpereira@gmail.com
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ABSTRACT
We live in a time of highly accelerated extinction, which has the potential to mirror past
mass extinction events. However, the rarity of these events and the restructuring of
diversity that they cause complicate direct comparisons between the current extinction
crisis and earlier mass extinctions. Among animals, turtles (Testudinata) are one of few
groups which both have a sufficient fossil record and a sufficiently stable ecological
importance to enable meaningful comparisons between the end Cretaceous mass
extinction and the ongoing extinction event. In this paper we analyze the fossil record of
turtles and recover three significant peaks in extinction rate. Two of these are in the
Cretaceous, the second of these took place at the Cretaceous–Paleogene transition (K-
Pg), reflecting the overall patterns previously reported for many other taxa. The third
major extinction event started in the Pliocene and continues until now. This peak only
affected terrestrial turtles and started much earlier in Eurasia and Africa lineages than
elsewhere. This suggests that it may be linked to co-occurring hominins rather than
having been caused by global climate change.
Keywords: biodiversity crisis; extinction; hominins; K-Pg; mass extinction; PyRate;
Testudines; turtles.
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INTRODUCTION
The ongoing biodiversity crisis is characterized by strong increases in extinction rates
observed across diverse taxa, including plants [1] and vertebrates [2-3]. Some researchers
have proposed that the magnitude of this increase is such that we currently live in a sixth
mass extinction [4-5], following the five mass extinction events known from the fossil
record [6-7]. Such a comparison is however difficult and indirect, because in most cases
the analytical framework and underlying data are substantially different between studies
focusing on recent versus ancient extinction events. Discussions on the potential sixth
mass extinction tend to focus on vertebrates, but vertebrate clades rarely have both a
sufficient fossil record, and a stable ecological importance extending back past the most
recent mass extinction (66 Ma) and comparisons between the anthropogenic elevated
extinction rate and paleontological mass extinctions are therefore difficult. For instance,
the mammalian fossil record is good but their ecological relevance increased drastically
following the end-Cretaceous extinction of non avian dinosaurs, effectively making
mammalian diversity before and after the K-Pg extinction incomparable. The ecological
niches of birds may on the other hand have been similar before and after the end-
Cretaceous extinction but their fossil record is scarce. One of the few exceptions to this
among vertebrates is turtles, a clade currently comprising c. 350 species distributed in all
continents except Antarctica, in both terrestrial and marine ecosystems. The long
evolutionary history of turtles, coupled with abundant fossils, allow for a direct
comparison between recent extinction dynamics and those of the Cretaceous–Paleogene
(K–Pg) boundary.
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On-going biodiversity loss is primarily linked to human activities, which led
researchers to propose a new geological epoch named the Anthropocene [4,8,9]. Previous
studies have pointed at Homo sapiens as responsible for these extinctions since the Late
Pleistocene [10-12], but it remains unclear if that is indeed the beginning of
anthropogenic influence on biodiversity. An increase in anthropogenic extinctions may in
fact have started already by the early hominins in the Late Pliocene and Early
Pleistocene, as suggested by a postulated causal relationship between increase in brain
size and increased extinction rate in large African carnivores ([13]). Hominins originated
in East Africa about four million years ago (Mya), later dispersing to Eurasia, during the
Late Pliocene or Early Pleistocene [14-15]. Based on anecdotal patterns in the fossil
record, recent extinction patterns of terrestrial tortoises appear to follow the hominin
route from their African origin to Eurasia during the Late Pliocene or Early Pleistocene
[16]. However, to the best of our knowledge, this pattern has not been formally tested.
This potential anthropogenic effect appears to have increased with time, and today, more
than half of extant turtle species are threatened with extinction [17-18].
In the K–Pg mass extinction, Earth experienced a significant loss in biodiversity
across all taxa. Among vertebrates, it caused the demise of all non-avian dinosaurs, in
addition to substantial extinctions in many other lineages, including mammals, birds,
lizards, teleost fish and insects [19-25]. Many studies suggest that the cause of the mass
extinction was the asteroid impact at Chicxulub [26-29], although other studies suggest
that sulfurous and toxic gases emitted by voluminous eruptions from the Deccan Traps
about 72–66 Mya may also have played a role [30-32].
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The global effect of the K–Pg mass extinction on turtles has been seldom
explored [33]. The event is often thought to have been of limited importance for the
clade, with few reported extinct families and genera [34-35], although many other
families went extinct soon after, during the early Paleocene [36-37]. Analyses based on
the fossil record [33,38,39] or on molecular phylogenies of extant taxa [40-41] have
failed to find signs of increased extinction globally. Some authors, however, found
evidence of local extinctions, e.g., in European species [42] and South American taxa,
which are thought to have lost half of their diversity [43].
In order to test whether the ongoing pace of extinction in turtles is comparable in
magnitude to the extinction they may have experienced at the K–Pg event, we analyzed a
comprehensive dataset comprising ancient and recent fossil data in a Bayesian analytical
framework to estimate the temporal dynamics of extinction rates.
METHODS
Data
We analyzed publicly available fossils of Testudinata – the clade containing all extant
turtles as well as a number of extinct relatives since the Late Cretaceous (145 Mya).
Occurrences were obtained using the R package ‘paleobioDB’ [44] to access
paleontological data of the Paleobiology Database (PBDB, paleobiodb.org, in September
2021) at species level. We manually investigated all records to remove synonyms and
misspelling, to avoid overestimating species numbers. We excluded species with dubious
terminologies (e.g. ‘?’, sp., aff., cf.). All marine taxa were removed, since their extinction
dynamics and fossilization may have been governed by different processes compared
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with terrestrial taxa. We further removed all species from islands, because islands have a
short lifespan over geological time scales and generally lack any exposed area older than
a few million years. Since evolutionary processes and anthropogenic impact can be quite
different on islands compared to continents [45], inclusion of island species could
otherwise generate a false signal, with extinction dynamics in the last few million years
drastically different to earlier periods. We also excluded fossil occurrences with a high
temporal uncertainty, defined here as an age range greater than 15 Mya. The extant
species were classified according to The Reptile Database [46]. The final dataset included
82 extant (~22% of the living turtles) and 908 extinct species, represented by a total of
3,385 fossil occurrences of terrestrial and freshwater continental turtles since the
Cretaceous (145 Mya).
Rates through time analyses
We estimated macroevolutionary rates through time based on fossil occurrence data,
using a Bayesian framework implemented in PyRate [47]. Within PyRate, we jointly
estimated the origination and extinction times for each lineage based on a Poisson
process of preservation and origination, and extinction rates through time based on a
birth-death process of diversification. Markov chain Monte Carlo (MCMC) analyses
were run for 50 million generations sampling every 5,000 generations. We used a
reversible jump MCMC algorithm to jointly estimate the number and timing of rate shifts
in origination and extinction rates and the rates between shifts. The analyses were
replicated on 20 datasets, in which the ages of all occurrences were resampled from their
stratigraphic range to account for dating uncertainties. Preservation rates were estimated
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as independent parameters within each geological epoch. We restricted the analyses of
extinction rates to the time frame encompassing the Cretaceous and the Cenozoic (145–
0.012 Mya). We excluded the Holocene, which is characterized by a significantly denser
sampling of fossil data compared to earlier periods, which could lead to biases. We
examined the stationarity of chain using the ‘coda’ R package [48], by calculating all
effective sample sizes (ESS) of the log-likelihood and other parameters. All ESS values
were higher than 200. We summarized the results after excluding the first 5M iterations
as burn-in and computing the posterior mean and 95% credible intervals of the extinction
rates through time. Significance of the rate shifts was calculated using the Bayes Factor
value (logBF).
Potential hominin effect
Early hominin effects on extinction have been proposed for turtles, but not explicitly
tested [16]. An alternative trigger of major extinction events is global climate change,
which is tightly linked to large-scale changes in terrestrial systems [49-51]. Since climate
has changed considerably in the last few million years, with the onset of the temperature
fluctuations associated with Pleistocene glacial-interglacial cycles, it could be difficult to
discern between a hominin and a climatic cause. However, climatically driven extinctions
should be detected consistently across the world, whereas if early hominins were the
main drivers of extinctions, elevated extinction rates should only be detectable in species
that co-occurred with hominins. Since hominins did not occupy Oceania and the
Americas until about 50 and 15 thousand years ago, respectively [52-54], earlier
increases in extinction rates should be restricted to Eurasia and Africa. For turtles, we
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would also expect higher extinction of terrestrial species since the earliest evidence for
hominin utilization of freshwater food resources was about 2 Mya [55].
In order to test a potential hominin effect, the occurrences since the Oligocene
(33.9 Mya) were categorized into two groups, according to the occupation of hominins
before the Late Pleistocene: (i) Eurasia and Africa (with hominins); and (ii) Americas and
Oceania (without hominins). To do this, we first assigned all occurrence coordinates to
countries and continents occupied, using the ‘SpeciesGeoCoder’ R package [56]. We also
classified the taxa according to the environment occupied (see the number of occurrences
and species in table 1 and full details in Supporting information 1). Many of the species
were assigned to habitat based on taxonomy, for example with all tortoises and horned
tortoises (Testudinidae and Meiolaniidae) classified as terrestrial. For species without a
habitat classification or belonging to more generalist families, literature searches were
carried out at the level of genus or species. When no information about the species was
found, we adopted the type of site where the fossils of that species were found.
Table 1. Number of occurrences of each category and, in parentheses, the species number
in the Neogene or Pleistocene (the last 23 Ma).
Eurasia and
Africa
Americas
and Oceania
Freshwater Terrestrial Total
Extinct 468 (195) 344 (148) 367 (185) 445 (158) 812 (343)
Extant 257 (42) 252 (40) 331 (64) 178 (18) 509 (82)
Total 725 (237) 596 (188) 698 (249) 623 (176) 1321 (425)
The assignment of poorly known genera to habitat can be difficult, particularly in
families with ecological variation. We therefore compiled alternative datasets to
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investigate the robustness of results in the face of certain uncertain assignments. Details
of these datasets and the results can be found in the Supplementary File 1.
RESULTS
Our results reveal three statistically significant phases of increased extinction. The first
phase occurred at the first age of the Late Cretaceous: Berriasian, the second around the
Cretaceous-Paleogene (K-Pg) transition and the last one during the Pliocene (Fig. 1).
The first significant extinction rate increase was strongly supported (LogBF>6) to
have occurred in the Late Cretaceous (96-94 Mya), when rates are inferred to have
increased almost 3-fold (from 0.13 to 0.42 Mya-1 between 98 and 93 Ma). Extinction
rates increased again in the Late Cretaceous (LogBF>6), during the Maastrichtian age
(~72-70 Ma). This time the rates increased almost 5-fold (from 0.06 to 0.29 Mya-1
between 74 and 66 Ma).
The estimated net diversification rates confirm the results (Supplementary File 1).
The analyses pointed to three moments in the evolutionary history of turtles in which they
showed a negative net diversification rate (extinction higher than speciation). The first
two occurred also in the Late Cretaceous (the first between 97-87 Mya, reaching -0.23
Mya-1, and the second between 71-59 Mya, reaching -0.06 Mya-1). The last one was in
the Pliocene (4-2 Mya, reaching -0.12 Mya-1).
Our analyses at a global geographic scale revealed an increase in the global higher
posterior density of extinction rates in the Pliocene (Supplementary Figure 1). However,
after dividing the dataset geographically (continental areas with long-term hominin
presence vs without hominins) and by environment (freshwater vs terrestrial), we
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detected that this rate increase was markedly higher in terrestrial turtles of Eurasia and
Africa (Fig. 1B). The results were consistent across the different classifications of turtle
ecology (for alternative datasets results see Supplementary File 1). Extinction rates of
terrestrial turtles were found to have increased in this group almost 5-fold during the
Pliocene (between 6 and 3 Mya the rates increased from 0.13 to 0.60 Mya-1), with strong
support (logBF > 2). Since the Pliocene, terrestrial extinction rates have been higher than
the freshwater ones, reaching the Pleistocene almost 3-fold higher. The extinction rates in
this group were so remarkable that their diversification rates have been negative since the
Pliocene (reaching the mean rate of -0.4 Myr-1 at the end of the Pliocene), even though
the 95% credible intervals show some uncertainty around the exact timing and magnitude
of the events. Concurrently, freshwater turtles from Eurasia and Africa suffered an
increase of lesser magnitude in the extinction rates (from 0.19 to 0.21 Myr-1 between 5 to
3 Ma, logBF > 2). Diversification rates in this group were negative during the last half of
the Pliocene (4-2 Mya, reaching -0.04 Myr-1). A strongly supported increase in extinction
rates was also found in the American and Oceanian terrestrial turtles, although it occurred
later than in the turtles from Eurasia and Africa, reaching a peak only about 1.1 Ma (from
0.30 to 0.57 Mya-1, logBF > 6). However we note that due to the age uncertainty around
the fossil occurrence data, the analysis setup did not allow rate shifts to occur more
recently than 1 Ma. Thus the timing of this shift may be overestimated and actually fall
within the last 1 Mya. Increasing rates of extinction in this group were accompanied by
even greater increases in speciation rates (from 0.26 to 0.70 Myr-1 at 2 Ma, logBF > 6).
Even with higher extinction rates, diversification rates never reached negative values,
contrariwise they grew from 0.03 Myr-1 (~3 Ma), reaching 0.33 Myr
-1 (~1.8 Ma). In
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contrast, the freshwater group in the Americas and Oceania displayed almost constant
rates of extinction in the last 10 Myr (~0.22 Myr-1) (Fig. 1).
DISCUSSION
Our results suggest that while turtles perhaps were not as affected as other clades
for the K-Pg event, they did experience a phase of increased extinction. In this regard, we
note that the dating of many fossils has uncertainties of several million years, so while
our inferred increase spans several million years, we cannot rule out that many
extinctions were in fact concentrated in a near instantaneous event at the K-Pg transition.
Yet, our results are in line with other studies showing that several turtle lineages survived
the K-Pg event [34,35,57-59] and suggesting an extended phase of diversity decline after
the K-Pg [43].
In more recent times, we recovered a 4-fold rate increase restricted to Eurasia and
Africa terrestrial turtles starting about 5 Ma, while terrestrial turtles for other regions
presented an increase a few million years later. In freshwater groups, the increase in the
rate of extinction affected only Eurasia and Africa species. The freshwater group in the
Americas and Oceania showed almost constant rates of extinction in the last 10 million
years. Since many records are only dated to the Pleistocene, it is possible that the
elevated extinction rate outside Eurasia and Africa is from the Late Pleistocene and
associated with the arrival of humans. At least some of the extinct species with accurately
estimated last appearance dates, like Hesperotestudo wilsoni, are known to have survived
as far as into the early Holocene [16]. According to our experimental design, if any major
extrinsic event is assumed to be a main driver of extinction rather than intrinsic (e.g.,
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ecological) factors, our results point towards a hominin cause of extinctions rather than
global climate change.
Rhodin et al. (2015) [16] noted that 106 known species, most of which were
terrestrial tortoises, have gone extinct since the Pleistocene. Our results, although aligned
with these findings, suggest that the most likely cause of the second extinction event in
turtles is co-occurring hominins, in line with previous findings on mammalian carnivores
[13]. Recent observations revealing the ability of modern chimpanzees to hunt and kill
tortoises [60], support the hypothesis that hominin ancestors would have had similar
skills. Hunting of freshwater species may on the other hand have been more difficult. The
earliest evidence of consumption of freshwater food resources is only 2 Ma [55] while the
earliest evidence of stone tool use is 3.3 Ma [61].
Hominins may have experienced an ecological transition to a more carnivorous
lifestyle about 2 Ma, and tortoises probably were part of their diet [9,62-64]. Even though
hominins likely did not consume a large proportion of meat before this time point, a
higher hominin population density could have the same or worse effect than a smaller
population of hyper-carnivores. Therefore, hyper-carnivores are not necessarily the most
important carnivores in a system. Strict carnivores normally occur in much lower
densities than omnivores [65]. For instance, in some contemporary systems, bears may be
the most important carnivores, even though only a small of their calory intake is from
meat [66].
Our results can be interpreted as supporting the findings of Smith et al. (2018)
[67] that the recent biodiversity crisis is fundamentally different from earlier extinction
events in terms of the types of organisms affected. The large number of invasive and
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exotic turtle species introduced around the world and their long lifespans may disguise
the impact of the extinction that this group has been suffering ([68]). However, more than
half of all extant turtle species are threatened, and the order contains the highest number
of threatened species among all vertebrates [17,68]. The main threats identified include
over-exploitation for food and pets, often illegally, as well as the destruction of their
natural habitats and accelerating climate change [17,68,69]. As one of the oldest and most
distinctive groups among the amniotes, and one which survived the K–Pg transition and
other major events for more than 300 Mya of evolution, further extinctions in this group
would constitute an irreparable loss.
While the focus of this paper is on extinctions occurring earlier then the
Anthropocene as strictly defined [69,70], our finding that human ancestors probably led
to a decline in turtle diversity millions of years ago further highlights the magnitude of
the extinction crisis for this group and highlights how far back in time a negative hominin
influence on biodiversity extends. We therefore hope that our work may stimulate efforts
to conserve the remaining species in the group. It is still debatable whether the current
extinction rate is high enough to declare a sixth mass extinction, but if we do not act now
as a society, we risk reaching a point where this doubt will disappear.
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ACKNOWLEDGMENTS
We thank Walter Joyce and Serjoscha Evers for advice, and Rhian Smith for linguistic
help.
FUNDING
AGP was funded by Coordenação de Aperfeiçoamento Pessoal - CAPES
(88881.170106/2018-01). AA acknowledges financial support from the Swedish
Research Council (2019-05191) and the Royal Botanic Gardens, Kew. DS received
funding from the Swiss National Science Foundation (PCEFP3_187012; FN-1749) and
from the Swedish Research Council (VR: 2019-04739). SF is supported by the Swedish
Research Council (# ).
DATA AVAILABILITY
All input data are available in a Zenodo repository [doi:
10.5281/zenodo.6870030].
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FIGURE LEGENDS
Figure 1: Extinction rates for turtles. The lines and shaded areas show mean posterior
rates and 95% credible intervals, respectively, inferred from 20 replicated analyses. The
white and gray squares represent geological epochs. a) above: Global extinction rates for
turtles from the Lower Cretaceous to the Miocene, bellow: representatives of some extant
and extinct lineages of Testudinata; b–c) Extinction rates for terrestrial (red) and
freshwater (blue) species from the Early Miocene to the Pleistocene: b) species that co-
occurred with hominins (Eurasia and Africa); c) species that did not co-occur with
hominins until very recently in geological time (the Americas and Oceania).
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was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made
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.CC-BY 4.0 International licenseavailable under a
was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made
The copyright holder for this preprint (whichthis version posted July 21, 2022. ; https://doi.org/10.1101/2022.07.20.500661doi: bioRxiv preprint