Historical Biology

An International Journal of Paleobiology

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Lagerstätte effect drives notosuchian

palaeodiversity (Crocodyliformes, Notosuchia)

A. de Celis , I. Narváez , A. Arcucci & F. Ortega

To cite this article: A. de Celis , I. Narváez , A. Arcucci & F. Ortega (2020): Lagerstätte effect
drives notosuchian palaeodiversity (Crocodyliformes, Notosuchia), Historical Biology, DOI:
10.1080/08912963.2020.1844682

To link to this article: https://doi.org/10.1080/08912963.2020.1844682

Published online: 14 Nov 2020.

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HISTORICAL BIOLOGY
https://doi.org/10.1080/08912963.2020.1844682

ARTICLE

Lagerstätte effect drives notosuchian palaeodiversity (Crocodyliformes, Notosuchia)

a a b a
A. de Celis , I. Narváez , A. Arcucci and F. Ortega
a
Grupo De Biología Evolutiva, Facultad De Ciencias, UNED, Madrid, Spain; bLaboratorio De Paleobiología, Universidad Nacional De San Luis, San Luis,
Argentina

ABSTRACT ARTICLE HISTORY

Notosuchians are a crocodyliform clade with a rich Gondwanan fossil record, especially in Cretaceous South Received 3 August 2020
American deposits. More than half of all described species come from South America and, around one Accepted 28 October 2020
quarter, have been discovered in the Adamantina Formation (Bauru Group, Brazil). The large amount of KEYWORDS
notosuchian remains from this formation, along with its chronostratigraphic uncertainty, may be distorting Adamantina Formation;
notosuchian palaeodiversity estimates. In order to analyse how these factors could be biasing our inter­ Bauru Group; fossil record
pretations, palaeodiversity estimates were performed excluding and including the Adamantina Formation bias; Late Cretaceous;
occurrence data, as well as assigning them to the main age ranges that have been proposed for the Notosuchia; paleodiversity
formation (Turonian-Santonian and Campanian-Maastrichtian). Furthermore, as other factors might be
influencing palaeodiversity fluctuations, a modelling approach was performed to assess which abiotic
factors, sampling artefacts, or a combination of them, could be driving these palaeodiversity dynamics.
The results showed that the Adamantina Formation is causing a Lagerstätte effect that is distorting
palaeodiversity estimates and, depending on the age assigned to that formation, the tempo and magnitude
of the maximum palaeodiversity reached during the Late Cretaceous substantially changes. The results also
suggest that the temporal bias might affect palaeobiological reconstructions not only in notosuchians but
also in other groups.

Introduction In particular, the Cretaceous of South America accounts for

more than half of the known notosuchian species (Pol and
Notosuchia Gasparini, 1971 is a crocodyliform clade characterised
Leardi 2015) and the Adamantina Formation (Fm.) holds c.
by a high diversity in ecological and morphological terms. These
27% of all known notosuchian species. This formation, from
crocodyliforms inhabited freshwater and terrestrial habitats
the Upper Cretaceous Bauru Group of Brazil, has a dominant
(Wilberg et al. 2019) and displayed a wide variety of feeding stra­
crocodyliform fauna and thus, it has been hypothesised that
tegies, from carnivorous (e.g. Baurusuchus salgadoensis Carvalho,
some of these notosuchians (specifically baurusuchids) might
Campos and Nobre, 2005), to omnivorous (e.g. Uruguaysuchus
be occupying the niche of small to medium-sized theropod
aznarezi Rusconi, 1933; see Soto et al. 2011) and herbivorous (e.g.
dinosaurs in those palaeoecosystems (Riff and Kellner 2011).
Simosuchus clarki Buckley , Brochu, Krause and Pol, 2000). Their
However, other studies proposed that this apparent abundance
wide chronostratigraphic range comprehends an interval from the
of crocodyliforms and lack of theropods could be the result of
Middle Jurassic of Madagascar (Dal Sasso et al. 2017) to the middle
taphonomic bias and, therefore, does not represent the original
Miocene of Colombia, Peru and Venezuela (Langston 1965;
biocoenosis (Godoy et al. 2016; Bandeira et al. 2018).
Buffetaut and Hoffstetter 1977; Langston and Gasparini 1997;
Fossil-Lagerstätten, understood as sedimentary bodies that yield
Paolillo and Linares 2007). Although some notosuchians were pre­
an unusual amount of information through quantity or quality of
sent in Asia (Wu et al. 1995; Wu and Sues 1996) and Europe
fossil-preservation (Seilacher 1970), can sometimes distort our
(Antunes 1975; Rossman et al. 2000; Company et al. 2005; Rabi
interpretations of palaeodiversity dynamics causing
and Sebök 2015), most of them inhabited Gondwana landmasses.
a phenomenon called ‘Lagerstätte effect’ (Raup 1972; Benson and

CONTACT A. de Celis ane.detecla@gmail.com Grupo De Biología Evolutiva, Facultad De Ciencias, Universidad Nacional de Educación a Distancia, Madrid, Spain
© 2020 Informa UK Limited, trading as Taylor & Francis Group

Published online 14 Nov 2020

2 A. DE CELIS ET AL.
Butler 2011). The intervals in which these exceptional sites appear,
seem to be much more diverse in comparison with other intervals
lacking exceptional sites, which seem depauperate as a result. This
has been the case with pterosaurs (Butler et al. 2009, 2013; Dean
et al. 2016) and Mesozoic marine tetrapods (Benson et al. 2010;
Benson and Butler 2011), among other vertebrate groups. Although
the Adamantina Fm. has not been defined as a Lagerstätte itself, the
wealth and abundance of notosuchian crocodyliforms found in this
formation in comparison to other notosuchian-bearing formations,
might be causing a ‘Lagerstätte or bonanza effect’ similar to those of
defined Lagerstätten in our analysis of notosuchian palaeodiversity
dynamics. Therefore, we use this permissive approach with the
Adamantina Fm., as an extension of the reasoning of Walker et al.
(2020) about the term Lagerstätte and its use in these studies.
Furthermore, the age of the Adamantina Fm. is still under
debate. Some authors have proposed a Turonian-Santonian age,
based on a combination of micropalaeontological (ostracods and
charophytes), isotopic and stratigraphic data (Dias-Brito et al.
2001), whereas others suggest a Campanian-Maastrichtian age
based on micropalaeontological (ostracods; Gobbo-Rodrigues
et al. 1999), stratigraphic (Batezelli 2017) and vertebrate fossil
data (Santucci and Bertini 2001; but see Martinelli et al. 2011;
Geroto and Bertini 2019). The radioisotopic U-Pb measurement
of Castro et al. (2018) from one outcrop of the Adamantina Fm.
depicted a post-Turonian age, probably late Coniacian to late
Maastrichtian in age. However, the absolute age of those outcrops
is still unknown (Martinelli et al. 2018).
The effect and extent to which the ‘Lagerstätte or bonanza effect’
and the chronostratigraphic uncertainty, exerted by the
Adamantina Fm., could be distorting our palaeodiversity estima­
tions and interpretations, has not been assessed yet. Therefore, the
present work aims to assess how the above-mentioned factors
might be influencing palaeobiological interpretations about this
crocodyliform group. To quantitatively analyse the data, palaeodi­
versity patterns with and without sample standardisation were
reconstructed, and a modelling approach using generalised least
squares was performed to assess the influence of several abiotic and
sampling variables on the fluctuations of the observed notosuchian
palaeodiversity.
Material and methods
Notosuchian occurrence dataset and management
Notosuchia is a clade that has been interpreted in a wide variety of
ways since its original description. In the most restrictive proposals,
Notosuchia just refers to a small group of forms closely related to
Notosuchus terrestris Woodward, 1896(e.g. Larsson and Sues 2007),
but in most phylogenetic hypotheses, depending on the topology of
the trees, Notosuchia includes a variable combination of clades such
as Uruguaysuchidae, Baurusuchidae, Sebecidae, Peirosauridae,
Sphagesauridae and other closely related forms (Zaher et al. 2006;
Pol et al. 2009; Geroto and Bertini 2019). However, all these clades
were included within Notosuchia in our database according to other
recent phylogenetic hypotheses (Pol et al. 2014; Fiorelli et al. 2016;
Martinelli et al. 2018; Coria et al. 2019).
Two hundred and twenty-one notosuchian body fossil occur­
rences were downloaded from the Palaeobiology Database (PBDB,
www.paleobiodb.org) on 3 July 2018. This raw data has been
reviewed and updated following the protocol described in de Celis
et al. (2019). The final dataset is composed of 140 occurrences from
81 species, including all valid taxa described until February 2019
(see Appendix S1 and Supplementary materials). Currently,
Razanandrongobe sakalavae Dal Sasso, Pasini, Fleury and
Maganuco, 2017 from the Middle Jurassic of Madagascar is
regarded as the oldest known notosuchian and has been included
in our database. However, as it is a unique occurrence and there are
no further species-level notosuchian occurrences until the
Barremian (Amargasuchus minor Chiappe, 1988 from the La
Amarga Fm., Argentina), it has not been included in the analyses.
Thus, the analyses performed range from the Barremian onwards.
Palaeodiversity estimates
To analyse how palaeodiversity estimations might be biased by the
age uncertainty, and the possible Lagerstätte effect driven by the
Adamantina Fm., two different approaches to estimate palaeodiver­
sity were performed. In each approach, palaeodiversity was esti­
mated at a global scale and also in regions with enough data (South
America and Africa, see Supplementary materials, Table S1) in
three different sets: (1) excluding notosuchian occurrences from
the Adamantina Fm.; (2) assigning a Turonian-Santonian age to
notosuchian occurrences from the Adamantina Fm.; (3) assigning
a Campanian-Maastrichtian age to notosuchian occurrences from
the Adamantina Fm.
The first approach was to perform taxonomic diversity estimates
(TDE), counting species present in each geological stage (International
Chronostratigraphic Chart v. 2018/08; Cohen et al. 2013), to ease
comparisons with previous studies (i.e. Pol and Leardi 2015).
The second approach was to do subsampling estimations of
notosuchian palaeodiversity with the shareholder quorum subsam­
pling method (SQS, Alroy 2010). The SQS method, a coverage-
based sample-standardisation method, is a widely used method to
account for the uneven sampling of the fossil record (e.g. Mannion
et al. 2015; Nicholson et al. 2015; Tennant et al. 2016; Cleary et al.
2018; Dunne et al. 2018).
Because geological stages from the Barremian to Serravallian
have an uneven duration, ranging from 12.50 million-years (myr)
in the Albian to 2.15 myr in the Langhian, and to lessen any
cumulative effects that might be present in longer geological stages
(Sepkoski and Koch 1996; Benson and Butler 2011), notosuchian
occurrences were rearranged into time-bins of approximately the
same duration. Owing to the poorly constrained ages of some
formations (i.e. the Kem Kem beds, the Elrhaz Fm. or the
Adamantina Fm.), it was necessary to group occurrences into 20
myr time-bins as follows: early Lower Cretaceous (ELK, Berriasian-
Barremian), late Lower Cretaceous (LLK, Aptian-Albian), early
Upper Cretaceous (EUK, Cenomanian-Santonian), late Upper
Cretaceous (LUK, Campanian-Maastrichtian), early Palaeogene
(EPg, Danian-Ypresian), late Palaeogene (LPg, Lutetian-Chattian),
Neogene (Ng, Aquitanian-Messinian). Specific dates for these time-
bins can be found in the supplementary materials (Table S2). Only
occurrences whose range of age was entirely contained within these
time-bins were included in SQS estimates. A new method to
develop a time-binning scheme, called formation binning, has
been recently published by Dean et al. (2020). However, c. 38% of
the formations analysed in this study (containing 41% of all noto­
suchian occurrences) lack a sufficiently precise dating to effectively
apply this novel methodology.
Palaeodiversity estimates were conducted in R v.3.5.0 (R Core
Team 2017) with the SQS script v3.3 by J. Alroy (available at http://
bio.mq.edu.au/~jalroy/SQS-3-3.R) and modified by J. Tennant to
include bootstrapping and calculate 95% confidence intervals
(available at https://github.com/Protohedgehog). SQS was carried
out with a quorum ranging from 0.1 to 0.9 and 1000 iterations per
run in each dataset (global, South American and African with the 3
sets abovementioned), reporting the mean subsampled notosuchian
palaeodiversity (full results available in Appendix 2). Furthermore,

bootstrapping was performed setting 1000 trials and a quorum level
of 0.4, reporting the median and 95% confidence intervals per
analysed dataset and also palaeodiversity estimates considering
only occurrences from the Adamantina Fm.
Model-based evaluation with generalised least squares
The methodology depicted in the previous section is a useful
approximation to address the impact of Adamantina Fm. on
notosuchian palaeodiversity estimates. However, the differences
found do not necessarily imply that notosuchian palaeodiversity
dynamics are solely driven by the presence or absence of data
from the Adamantina Fm., as other factors might be contribut­
ing to those palaeodiversity fluctuations. To test the relationship
between several variables and notosuchian global palaeodiversity
we followed Benson and Butler (2011), developing a model-
based evaluation. Therefore, several variables were compiled
(data available in Appendix S1) to be analysed against notosu­
chian global palaeodiversity (TDEs): non-marine tetrapod bear­
ing collections (TBCs; PBDB), non-marine tetrapod bearing
formations (TBFs; PBDB), Adamantina (binary variable indicat­
ing presence or absence, adapted from Benson and Butler 2011),
palaeotemperature (δ18O; Prokoph et al. 2008), sea level (Miller
et al. 2005), non-marine area (NMA; Smith et al. 2004).
Following previous analyses (Marx and Uhen 2010; Benson
and Butler 2011), the duration of each time-bin (stages in this
case) was included as a non-optional variable in all models to
account for uneven temporal lengths. The relationship between
palaeodiversity (TDEs) and these variables was tested from
Barremian to Maastrichtian (both included), because palaeodi­
versity is too scarce outside this interval.
Besides that, and to test for any possible influence of the
Adamantina Fm. age uncertainty, we analysed these relationships
in two different modes: using TDEs with notosuchian occurrences
from the Adamantina Fm. as Turonian-Santonian (TDE1) or either
as Campanian-Maastrichtian in age (TDE2). Forty-six models, cov­
ering each possible combination of the dependent and independent
variables, were analysed per each TDE. These ninety-two models
were tested for normality, homoscedasticity and non-
autocorrelation before modelling, applying autoregressive models
where necessary. The best-fitting models were identified with the
Akaike’s Information Criterion for small sample sizes (AICc) and
Akaike weights (AICw) (Akaike 1973, 1978). The overall perfor­
mance of these models with respect to the null model was assessed
with the pseudo-R2 of Cox and Snell (1989). All these analyses were
done in R v.3.5.0 (R Core Team 2017) with the packages lmtest
v.0.9–36 (Zeileis and Hothorn 2002), MuMIn v.1.43.6 (Barton
2019) and nlme v.3.1–137 (Pinheiro et al. 2018).
Results
Palaeodiversity estimates
The observed patterns of species-richness, or TDEs Figure 1(A, C, E;
Appendix S2), depict different scenarios depending on the treatment
of notosuchian occurrences from the Adamantina Fm. All TDEs
Figures 1(A, C, E) show an initial increase in the number of species
from the Barremian to the Aptian and a slight decrease towards the
Albian, with a major contribution from Africa in this interval.
However, these TDEs depict a completely different outline in the
Upper Cretaceous after the Cenomanian stage, which has almost the
same number of species as the preceding stage. If notosuchian occur­
rences from the Adamantina Fm. are excluded Figure 1A or consid­
ered as Campanian-Maastrichtian Figure 1E, there is a substantial
HISTORICAL BIOLOGY 3
decrease in the number of species during the Turonian and
Coniacian, followed by an increase towards the Santonian that doubles
the number of species. On the other hand, if we consider the
Adamantina Fm. notosuchian occurrences as Turonian-Santonian
Figure 1C, there is not a decrease but a great increase from the
Cenomanian to the Turonian, posteriorly reaching its maximum
number of species in the Santonian. Notably, the global curves in the
Turonian-Santonian interval are dominated by South American noto­
suchian occurrences. Afterwards, if notosuchian occurrences from the
Adamantina Fm. are excluded Figure 1A or regarded as Turonian-
Santonian Figure 1C, the latest Cretaceous stages show a two-step
decrease in which there is a first decrease towards the Campanian, an
increase to the Maastrichtian and a decrease towards the Cretaceous-
Palaeogene boundary. However, in the first case Figure 1A the decrease
towards the Campanian is slight, whereas in the second case Figure 1C
that decrease is much more pronounced, and the increase from the
Campanian to the Maastrichtian is reversed, being much more pro­
nounced in the first case Figure 1A in comparison with the second one
Figure 1C. In contrast, if notosuchian occurrences from the
Adamantina Fm. are regarded as Campanian-Maastrichtian Figure
1E, there is a sheer increase from the Santonian to the Maastrichtian,
reaching its maximum number of species, and then there is a steep
decrease towards the end of the Cretaceous.
The post-Cretaceous scenario is also shared between these
three TDEs Figures 1(A, C, E) and depicts an increase in the
number of species during the Palaeocene. In this interval, the
global curve entirely reflects the South American record. After
the Palaeocene, there is a decrease towards the Ypresian, but
the species diversity recovers during the Lutetian, matching
the late Palaeocene levels. After the Bartonian there are no
records of species-level notosuchian occurrences until the mid­
dle Miocene of South America, in which the last known noto­
suchian occurrences are recorded (Langston 1965; Buffetaut
and Hoffstetter 1977; Langston and Gasparini 1997; Paolillo
and Linares 2007).
The subsampled palaeodiversity estimates Figures 1(B, D, F)
only retrieved results for the late Lower Cretaceous (LLK), the
Late Cretaceous (EUK and LUK) and the ‘late Palaeogene’ (LPg),
as notosuchian occurrences in the remaining time-bins are
scarce and/or are comprised of singletons (i.e. taxa that appear
once in a time-bin). The outline of the subsampled palaeodiver­
sity without the Adamantina Fm. notosuchian occurrences
Figure 1B highly resembles that of the approach in which
those occurrences were arranged as Turonian-Santonian Figure
1D, although in the latter the increase during the early Upper
Cretaceous (EUK) is more pronounced. The subsampled palaeo­
diversity regarding notosuchian occurrences from the
Adamantina Fm. as Campanian-Maastrichtian Figure 1F shows
successive slight increases from LLK to LUK, reaching the max­
imum palaeodiversity in the late Upper Cretaceous. In all these
global subsampled palaeodiversity estimates Figures 1(B, D, F) is
visible that the contribution of Africa is smaller than the con­
tribution of South America, and that the post-Cretaceous
palaeodiversity can be regarded as scattered and residual.
Multiple regressions
The main results drawn from the analysis of the ninety-two models,
in which palaeodiversity depended upon the combination of two or
more variables, are depicted in Table 1. This table only shows the
models that accounted for 90% of the total AICw in the two
approximations (TDE1 and TDE2); full results of the ninety-two
models are available in Appendix S2. The best-fitted models in both
approaches are the same and have similar AICc and AICw values.
4 A. DE CELIS ET AL.

Figure 1. Taxonomic diversity estimates and subsampled notosuchian species palaeodiversity from the Barremian to the Serravallian. The left column depicts the TDEs and
the right column the subsampled palaeodiversity with 95% confidence intervals. A) TDE excluding the Adamantina Fm. notosuchian occurrences. B) Subsampled
notosuchian palaeodiversity excluding the Adamantina Fm. notosuchian occurrences. C) TDE regarding the Adamantina Fm. as Turonian-Santonian. D) Subsampled
notosuchian palaeodiversity regarding the Adamantina Fm. as Turonian-Santonian. E) TDE regarding the Adamantina Fm. as Campanian-Maastrichtian. F) Subsampled
notosuchian palaeodiversity regarding the Adamantina Fm. as Campanian-Maastrichtian. The grey shading in C) and E) depicts the position of the Adamantina Fm. in those
TDEs, whereas the black star symbol in D) and F) depicts the subsampled palaeodiversity of the Adamantina Fm. alone. Key to colours and symbols: blue circles, global;
green squares, Africa; red hexagons, South America. Some points have been moved slightly sideways to allow proper visualisation of the data. Alt Text. Six graphs plotting
notosuchian palaeodiversity through geologic time. Notable changes between these graphs occur during the Late Cretaceous interval, depending on the presence or
absence of data from the Adamantina Formation, age of the Adamantina Formation (Turonian-Santonian or Campanian-Maastrichtian) and method used to calculate
palaeodiversity (species counts or subsampled species).

The first selected model represents a composite model in which
notosuchian palaeodiversity (either TDE1 or TDE2) depends on the
presence/absence of the Adamantina Fm. data and time-bin length,
and in both cases accounts for c. 75% of the total AICw with
a moderate to high pseudo-R2 value, ranging from 0.82 to 0.88.
The second selected model in both approaches represents a scenario
in which palaeodiversity depends on the presence/absence of the
Adamantina Fm. data, palaeotemperature fluctuations, and time-
bin length. This model accounts for 15 to 20% of the total AICw and
has a high pseudo-R2, c. 0.90. Noteworthy, all these models showed

Table 1. Summary results of the generalised least squares multiple regression models accounting for 90% of the total Akaike weights for notosuchian global TDEs (TDE1 and
TDE2) from the Barremian to the Maastrichtian (N = 9 stages). Abbreviations: AICc, Akaike’s information criterion for small sample sizes; AICw, Akaike weight; δ18O,
palaeotemperature proxy; GLS, generalised least squares; TDE1, Taxonomic Diversity Estimate from the Barremian to the Maastrichtian regarding Adamantina Fm.
notosuchian occurrences as Turonian-Santonian; TDE2, Taxonomic Diversity Estimate from the Barremian to the Maastrichtian regarding Adamantina Fm. notosuchian
occurrences as Campanian-Maastrichtian.
Dependent variable GLS regression model
Adamantina
TDE1 TDE1 ~ Adamantina (+duration) 0.0036**
TDE1 ~ Adamantina + δ18O (+duration) 0.0036*
TDE2 TDE2 ~ Adamantina (+duration) 0.0005**
TDE2 ~ Adamantina + δ18O (+duration) 0.0023*
that the variable representing the presence or absence of data from
the Adamantina Fm. is statistically significant (p-value<0.05).
Discussion
Gaps in the notosuchian fossil record
The observed taxic diversity estimates Figures 1(A, C, E) and palaeo­
geographical maps Figures 2(A- C) show that the notosuchian record
is exclusively associated with certain restricted areas in several stages,
hence depicting a spatiotemporally heterogeneous fossil record.
Although the Laurasian fossil record of many vertebrates is much
more abundant and extensively sampled than the Gondwanan record
(Benton 2015; Nicholson et al. 2015; Tennant et al. 2016; Cleary et al.
2018; de Celis et al. 2019), this is not the case with notosuchians (Pol
and Leardi 2015; Mannion et al. 2019). Notosuchian occurrences
(Appendix S1) depict that South America provides 58% of the total
sample, along with a lesser African income of 36%, whereas the
Laurasian record is scarce and scattered, representing only an income
of 6% (4% Europe, 2% Asia).
As shown in Figures 1 (A, C, E) the Aptian-Cenomanian record
has a higher African income, although the South American record
also provides notosuchian occurrences in this interval Figure 2A.
The subsampled palaeodiversity shows a similar income from both
continents in this first interval Figures 1(B, D, F), in which there
was a first registered increase, interpreted as a first diversification
step of the group (Bronzati et al. 2015; Pol and Leardi 2015).
However, as commented before, it should be noted that the first
known notosuchian comes from the Bathonian of Madagascar (Dal
Sasso et al. 2017) and there are no further notosuchian findings
until the Barremian of Argentina (Chiappe 1988). As Mannion et al.
(2019) indicated, this gap might be hiding an unsampled initial
notosuchian diversification prior to the seemingly sudden radiation
registered in the late Lower Cretaceous.
After the Cenomanian stage the African record does not provide
species-level notosuchian occurrences until the Maastrichtian, in
which the Maevarano Fm. provides a great amount of them Figures
2(B-C);3. It is still unknown how the notosuchian-dominated faunas
of the ‘middle Cretaceous’ of Africa derived into the dyrosaurid and
gavialoid dominated faunas of the latest Upper Cretaceous (Saber
et al. 2018). However, this Cenomanian-Maastrichtian gap does not
represent a true absence of notosuchians, as there are crocodyliform
remains with notosuchian affinities from the Coniacian-Santonian In
Beceten Formation in Niger, some of them originally referred to the
nowadays nomen dubium Trematochampsa taqueti (Buffetaut 1974,
1976; Meunier and Larsson 2018). Therefore, this observed bias
might be composed of a geological component (few known fossil-
bearing formations during the Turonian-Campanian interval in
Africa), and an anthropological component (these formations are
still poorly sampled and studied).
HISTORICAL BIOLOGY 5
p-value Pseudo-R2 Log Likelihood AICc AICw (%)
18
δ O Duration
- 0.5858 0.817 −20.86167 54.52334 74.15653
0.7363 0.7031 0.890 −18.57786 57.15571 19.80983
- 0.3102 0.882 −20.90288 54.60576 74.63846
0.8507 0.3491 0.924 −18.92294 57.84588 14.77085
The South American Upper Cretaceous record, excluding the
Adamantina Fm. ocurrences Figure 3, shows that the greater
incomes are from the Santonian of Argentina (the Bajo de la
Carpa Fm.; Figure 2B; Figure 3) and the Campanian-
Maastrichtian of Brazil and Argentina (e.g. the Marília Fm., the
Anacleto Fm.; Figure 2C; Figure 3). The post-Cretaceous notosu­
chian record is also dominated by South America, and it is exclu­
sively composed of sebecids. The Palaeocene diversity increase
Figures 1(A, C, E) has been interpreted as a sebecid radiation by
Bronzati et al. (2015). There is another gap into species-level
occurrences from the middle Eocene to the middle Miocene
Figures 1(A, C, E), although some remains attributable to sebecids
have been reported along this interval from several South American
localities (Langston 1965; Gasparini 1984; Antoine et al. 2016).
Therefore, that middle Eocene – middle Miocene gap does not
represent a true absence of sebecids in South America, but the
result of biases (anthropogenic, geological, taphonomic, or
a combination of them).
Palaeodiversity estimates and the influence of the
Adamantina Fm.
Mannion et al. (2015) and Pol and Leardi (2015), placed the
Adamantina Fm. as Turonian-Santonian to perform palaeodiver­
sity estimates. The TDE obtained in this study when assigning that
age to the Adamantina Fm. Figure 1C highly resembles the TDE of
Pol and Leardi (2015) with the sole exception of the Campanian to
Maastrichtian increase that our global curve shows. This deviation
might be attributed to the differences between datasets owing to
new notosuchian species descriptions since 2015 and some species
non-included in Pol and Leardi (2015) owing to their unknown or
unstable phylogenetic position.
The exclusion of the Adamantina Fm. data from palaeodiversity
estimates Figures 1(A-B) depicts different interpretations depend­
ing on the used method. From the raw estimates Figure 1A it can be
interpreted that palaeodiversity has a bimodal distribution, increas­
ing in the late Lower Cretaceous and especially in the latest Upper
Cretaceous. However, the subsampling approach Figure 1B depicts
that, instead, the early Upper Cretaceous was more diverse. This
can be directly related to the fact that the late Upper Cretaceous
notosuchian record from South America (excluding the
Adamantina Fm.) is entirely composed of singletons, and the
African record, although having abundant occurrence data from
the Maastrichtian Maevarano Fm., has a low number of species and
is dominated by one taxon: Simosuchus clarki, affecting SQS results
for this last Cretaceous interval. All this combined makes the late
Upper Cretaceous subsampled palaeodiversity estimates to seem
more depauperate than they are Figures 1(B, D, F).
The inclusion of the Adamantina Fm. occurrence data in the
estimations causes a great palaeodiversity increase associated with the
6 A. DE CELIS ET AL.

Figure 2. Palaeogeographical distribution of Cretaceous notosuchian occurrences at species level. A) late Lower Cretaceous (Aptian-Albian). B) early Upper Cretaceous
(Cenomanian-Santonian). C) late Upper Cretaceous (Campanian-Maastrichtian). The Adamantina Fm. notosuchian occurrence data in green. Data were plotted with
PaleoDataPlotter and GPlates, following Scotese (2016). Alt Text. Three palaeomaps depicting location and frequency of notosuchian occurrences. During the Aptian-Albian
(Figure 2A) most notosuchians come from Africa, with some occurrences from South America, whereas during the Cenomanian-Santonian interval (Figure 2B) this situation
is reversed. During the Campanian-Maastrichtian (Figure 2 C) most notosuchians come from South America and Africa (mostly Madagascar in the last case). Notosuchian
occurrences from the Adamantina Formation are indicated in both Figure 2B and 2C, due to its chronostratigraphic uncertainty.

time-bin in which those occurrences were placed Figures 1(C-F). intervals in which it is present to seem more diverse with respect to
Therefore, it is likely that a Lagerstätte effect linked with this formation the time-bins in which there are no exceptional sites yielding notosu­
is distorting notosuchian palaeodiversity estimates, making the chian remains. This effect has been reported to cause distorted
 HISTORICAL BIOLOGY 7

Figure 3. Chronostratigraphic ranges from notosuchian-bearing formations from the Cretaceous of South America and Africa. N represents the number of
notosuchian occurrences within each formation. The numbers in the Adamantina Fm. bar represent the two main age proposals: 1, Turonian-Santonian; 2,
Campanian-Maastrichtian. Alt Text. A graph depicting the chronostratigraphic range of formations from the Cretaceous of South America and Africa and the
number of notosuchian occurrences found in each of them. Many of these formations have poorly constrained ages, spanning several geological stages (e.g. the
Galula Fm., the Santana Fm, the Adamantina Fm.).

palaeodiversity estimates on other vertebrate groups such as Mesozoic Multiple regressions

marine tetrapods (Benson et al. 2010; Benson and Butler 2011), pter­
osaurs (Butler et al. 2009, 2013; Dean et al. 2016), lepidosaurs (Cleary
et al. 2018) and fishes (Lloyd and Friedman 2013; Romano et al. 2016).
On the other hand, the Adamantina Fm. is not only causing
a presumable Lagerstätte effect on notosuchian palaeodiversity
dynamics, but also is influencing palaeodiversity trend interpretations
through its poorly constrained age. The maximum palaeodiversity is
reached at different intervals depending on the age attributed to the
Adamantina Fm., early Upper Cretaceous Figures 1(C-D) or late Upper
Cretaceous Figures 1(E-F). In addition, the timing in conjunction with
the Lagerstätte effect influences the palaeodiversity peak magnitude,
being more than twice as big if the Adamantina Fm. is considered as
early Upper Cretaceous Figures 1(D, F). Therefore, the general palaeo­
diversity trends of the group during the Upper Cretaceous can be
interpreted in two very different ways: (1) a very large increase during
the early Upper Cretaceous, followed by a decrease of the same magni­
tude in the late Upper Cretaceous Figures 1(C-D); (2) a gradual increase
throughout the Upper Cretaceous Figure 1F.
The GLS modelling approach showed that in the best-fitting model
the observed notosuchian taxic diversity depends on the presence
or absence of the Adamantina Fm. data Table 1. The variable
presence or absence of Lagerstätten, comparable to our variable
‘Adamantina’, was part of the best-fitted models in Benson and
Butler (2011), Dean et al. (2016) and Lloyd and Friedman (2013).
The Adamantina Fm. chronostratigraphic uncertainty does not
affect the interpretation of these results, as the retrieved best-fitted
models between both approaches (TDE1 and TDE2) are the same
and have similar Akaike weights Table 1. These models include
other variables such as time-bin length and palaeotemperature,
although these variables are non-statistically significant in any of
these models. In contrast, the binary variable depicting the presence
or absence of the Adamantina Fm. data is statistically significant
(p-value<0.05) in all our best-fitting models and therefore it is
considered as the main factor driving the observed notosuchian
taxic diversity estimates. Therefore, the previous visual detection of
8 A. DE CELIS ET AL.
a possible Lagerstätte effect linked to the Adamantina Fm. is con­
gruent with these analytical findings.
Implications on palaeobiological reconstructions
The obtained results imply that not only palaeodiversity recon­
structions can be affected by the poorly constrained age of some
formations, such as the Adamantina Fm. in this case. This age
uncertainty can also bias time-calibrated phylogenies, palaeo­
biogeographical reconstructions, and in general, the reconstruc­
tion of macroevolutionary trends within this crocodyliform
group. Temporal biases in calibrated phylogenies can result in
a different temporary-framing and magnitude of notosuchian
radiations and extinctions. Regarding palaeobiogeographic
reconstructions, the great variance on the temporal-framing of
a substantial quantity of notosuchian occurences can result in
utterly different proposals of ancestral areas and subsequent
dispersal events. This biases are especially notable in those
groups whose fossil record is intimately related to the
Adamantina Fm. such as baurusuchids (Montefeltro et al.
2011; Marinho et al. 2013) and sphagesaurids (Iori et al. 2016;
Martinelli et al. 2018).
Although we have examined the particular case of notosu­
chians in this study, this temporal bias can also affect other
extinct organisms whose fossil record is intrinsecally related to
formations with a poorly constrained age. Therefore, we recom­
mend analysing and assessing the impact of this temporal bias
on palaeobiological reconstructions from any group that fits
with the case study presented here.
Conclusions
The notosuchian fossil record is spatiotemporally heterogeneous
and has several gaps that do not represent true absences (e.g.
early Upper Cretaceous of Africa). The palaeodiversity estimates
depicted that the highest palaeodiversity concurred with the
presence of the Adamantina Fm. in those time-bins. This fact,
coupled with the chronostratigraphic uncertainty of the
Adamantina Fm., showed that our interpretations on the
tempo and magnitude of the maximum increase of notosuchian
palaeodiversity in the Upper Cretaceous can follow two different
scenarios: 1) if the Adamantina Fm. is regarded as Turonian-
Santonian: there is a large increase during the early Upper
Cretaceous, twice as big as that of the second approach, fol­
lowed by a decrease of the same magnitude in the late Upper
Cretaceous; or 2) if the Adamantina Fm. is regarded as
Campanian-Maastrichtian: there is a gradual increase through­
out the Upper Cretaceous, reaching its maximum, half the
magnitude of the abovementioned approach, in the latest
Upper Cretaceous. Furthermore, the GLS results showed that
the presence or absence of the Adamantina Fm. data is the
main driver of the observed notosuchian taxic diversity during
the Cretaceous. The combined results support the existence of
a Lagerstätte, or bonanza effect, exerted by the Adamantina
Fm.; which is distorting the interpretation of notosuchian
palaeodiversity trends, among other palaeobiological reconstruc­
tions in which these crocodyliforms are involved. The results
also highlight that the impact of data with high chronostrati­
graphic uncertainty should be evaluated prior to any palaeobio­
logical reconstruction, as it could potentially bias them.
Acknowledgments
We thank PBDB members who entered notosuchian occurrence data (P.D.
Mannion, M. Carrano, J. Zijlstra, J. Tennant, J. Alroy; a comprehensive list of
authors can be downloaded from the PBDB website). We thank J. Alroy and
J. Tennant for sharing the R scripts for SQS in their websites. We thank C. Dean,
M. Rabi and an anonymous reviewer for their suggestions to improve the quality
of our manuscript.
Disclosure statement
The authors declare that they do not have competing interests.
Funding
This work was supported by the Ministerio de Ciencia, Innovación y
Universidades under an FPU fellowship (FPU 2016/01058; A.dC.).
ORCID
A. de Celis http://orcid.org/0000-0002-7362-7360
I. Narváez http://orcid.org/0000-0003-0114-7058
A. Arcucci http://orcid.org/0000-0001-8098-1512
F. Ortega http://orcid.org/0000-0002-7431-354X
Supporting information
Additional Supporting information can be found in the online version of this
article:
Appendix S1. Raw Paleobiology Database (PBDB) data, final dataset of
notosuchian occurrences and variables analyzed with generalised least squares
(GLS) regressions.
Appendix S2. Results of raw species counts (TDEs), shareholder quorum
subsampling estimates and generalised least squares (GLS).
Supplementary materials. Table S1 (countries composing each spatial region
analyzed), Table S2 (time-bin schemes) and a note about new published noto­
suchian specimens.
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