See discussions, stats, and author profiles for this publication at: https://www.researchgate.

net/publication/324032853

Accounting for differences in species frequency distributions when

calculating beta diversity in the fossil record

Article  in  Methods in Ecology and Evolution · March 2018

DOI: 10.1111/2041-210X.13007

CITATIONS READS

12 231

3 authors:

Neil Brocklehurst Michael O. Day

University of Oxford Natural History Museum, London
82 PUBLICATIONS   437 CITATIONS    46 PUBLICATIONS   460 CITATIONS   

SEE PROFILE SEE PROFILE

Jörg Fröbisch
Museum für Naturkunde - Leibniz Institute for Research on Evolution and Biodiver…
134 PUBLICATIONS   1,646 CITATIONS   

SEE PROFILE

Some of the authors of this publication are also working on these related projects:

The mid-late Permian transition and the Capitanian mass extinction among tetrapods View project

Permocarboniferous actinopterygian fishes from Brazil. View project

All content following this page was uploaded by Neil Brocklehurst on 09 May 2018.

The user has requested enhancement of the downloaded file.

 |
Received: 28 November 2017    Accepted: 16 March 2018

DOI: 10.1111/2041-210X.13007

RESEARCH ARTICLE

Accounting for differences in species frequency distributions

when calculating beta diversity in the fossil record

Neil Brocklehurst1  | Michael O. Day2,3 | Jörg Fröbisch1,2,4

1
Leibniz-Institut für Evolutions- und
Biodiversitätsforschung, Museum für Abstract
Naturkunde, Berlin, Germany 1. Beta diversity is a measure of the taxonomic differentiation between habitats/
2
Evolutionary Studies Institute & School
localities within an assemblage, and is normally calculated as a set of pairwise
of Geosciences, University of the
Witwatersrand, Johannesburg, South Africa taxonomic “distances” between the localities.
3
Department of Earth Sciences, The Natural 2. Due to incomplete sampling, beta diversity estimates for fossil assemblages will
History Museum (NHMUK), London, UK
always be higher than the true value. However, the difference between the ob-
4
Institut für Biologie, Humboldt-
Universitätzu Berlin, Berlin, Germany served and true distances will vary greatly depending on differences in the shape
of the relative abundance distribution.
Correspondence
Neil Brocklehurst 3. Using simulations, it is shown that incomplete sampling of a homogenous fauna
Email: neil.brocklehurst@mfn-berlin.de with more even relative abundances of taxa produces higher beta diversity than

Funding information one with very few extremely common taxa.

Deutsche Forschungsgemeinschaft, Grant/
Award Number: FR 2457/5-1; South
African Agency for Science and Technology
Advancement; Department of Science
and Technology, Republic of South Africa;
Palaeontological Scientific Trust; DST/
NRF Centre of Excellence in Palaeoscience;
National Research Foundation
Handling Editor: Daniele Silvestro
4. A new procedure is proposed for calculating beta diversity in the fossil record,
whereby the observed distances are compared to the distance obtained by ran-
domly resampling a homogenous fauna with the same abundance distribution.
This procedure is named Relative Abundance Corrected beta diversity. Simulations
indicate that this method outperforms raw beta diversity estimates, providing
beta diversity estimates closer to the true values even when the assumptions of
the method are violated.
5. This method is applied to an empirical dataset: Permian–Triassic tetrapods from
the Karoo Supergroup of South Africa. Increased provincialism is found across the
Permian–Triassic boundary in contrast to uncorrected beta diversity patterns.

KEYWORDS
abundance, beta diversity, Karoo, provinciality, sampling, tetrapod

1 |  I NTRO D U C TI O N
Since the seminal paper of Whittaker (1960), species richness has
been discussed in terms of alpha, beta and gamma diversity. Gamma
diversity represents the total diversity of an assemblage, which is de-
termined by the richness within each locality or habitat (alpha diver-
sity) and the differentiation between these localities (beta diversity).
Beta diversity is normally calculated as a set of pairwise taxonomic
“distances” between the localities ranging between 0 and 1, where a
distance of 0 indicates an identical set of taxa in two localities and 1
represents no taxa shared between the localities (for a summary of
the various distance metrics, see Koleff, Gaston, & Lennon, 2003).
When studying macroevolutionary patterns, particularly in the fos-
sil record, one must account for the incomplete sampling of taxa, and
beta diversity is no exception. Even if two localities hosted an identi-
cal set of taxa, the fact that numerous taxa will be missing from both
makes it probable that the true taxonomic distance of 0 will not be
obtained (Chao, Chazdon, Colwell, & Shen, 2005; Lande, 1996; Wolda,
1981). The worse the sampling, the fewer taxa are likely to be sampled
in both localities and the higher the observed distance will be. Thus,

Methods Ecol Evol. 2018;1–12. © 2018 The Authors. Methods in Ecology and |  1
wileyonlinelibrary.com/journal/mee3  
Evolution © 2018 British Ecological Society
 | Methods in Ecology and Evolu
on
2       BROCKLEHURST et al.
when comparing the beta diversity of two assemblages/time bins, one
must account for the fact that the assemblages (and localities within)
may not have been sampled equally (Chao et al., 2005).
However, sampling standardization does not mitigate another
issue: the impact of incomplete sampling will vary depending on differ-
ences in the relative abundances of the taxa in the assemblage. Since
beta diversity is a taxonomic comparison of assemblages, the identi-
ties of the taxa drawn during subsampling will affect the result. All else
being equal, an extremely common taxon should have a higher prob-
ability of making it into the fossil record and being sampled (Kidwell,
2001, 2002). Therefore, when comparing localities that hosted an
identical set of taxa, if a small number of these are highly abundant
there is a greater probability of most of these making it into the fos-
sil record at each locality sampled, thus keeping the inferred beta di-
versity low. However, if there is a more even abundance distribution,
there is a higher probability that each locality would preserve a differ-
ent set of taxa and inferred beta diversity would be higher. In short,
beta diversity values calculated for two different fossil assemblages
with different abundance patterns will not be directly comparable,
even if sampling standardization is employed, as the null expectation
(the expected beta diversity value at a particular level of sampling in a
homogenous set of localities) will be different each time.
The effect of variation in abundance distributions on inferences
of alpha and gamma diversity in the fossil record has long been ac-
knowledged and discussed (Alroy, 2000; Alroy et al., 2001; Bush,
Markey, & Marshall, 2004), and methods more robust to its influ-
ence have been suggested (e.g., Alroy, 2010; Chao & Jost, 2012).
However, its effect has received limited discussion in relation to
beta diversity. Although Beck, Holloway, and Schwanghart (2013)
demonstrated reduced accuracy of beta diversity estimates when
more even abundance distributions are undersampled, but they did
not suggest a solution. This paper demonstrates the influence of
variations in relative abundances of taxa on a variety of taxonomic
distance measures using both simulated data and empirical data
from the Karoo Supergroup of South Africa. A method of correcting
for this influence is described and tested via simulations.
2 |  M ATE R I A L S A N D M E TH O DS
2.1 | Dataset
The empirical palaeontological data is derived from the Karoo
Supergroup, a South African basin with a record covering the Middle
Permian until the Middle Triassic. Within the Karoo sequence, the
Beaufort Group represents by far the best-­sampled record of ter-
restrial vertebrates from the Permian–Triassic, and has a well-­
established biostratigraphy recently correlated with radiometric
dates (Day et al., 2015; Rubidge, Erwin, Ramezani, Bowring, & de
Klerk, 2013). Apart from the extensively studied taxonomy and spe-
cies richness patterns (e.g. Day et al., 2015; Fröbisch, 2013, 2014;
Irmis, Whiteside, & Kammerer, 2013), the Karoo is a particularly
good subject for examination of the issues under study as it is a sin-
gle basin with a consistent mode of preservation throughout, thus
allowing one to identify issues of sampling and evenness relatively
unhampered by confounding factors such as variations in preserva-
tion potential (see “Discussion”).
A comprehensive database of specimens from the museum col-
lections of South Africa was used, modified from Day et al. (2015),
which indicates the taxonomic affinity of each specimen, its biostra-
tigraphic assemblage zone (AZ; used as time bins) and the farm from
which it was collected (these represent the localities). The taxonomy
was updated based on the published literature and direct examina-
tion of the specimens. Specimens of uncertain affinity or stratigra-
phy were discarded, as were single-­t axon localities. The datasets for
each assemblage-­zone are presented in Data S1–S8.
2.2 | Assessing the impact of changes in the
abundance distribution
The Karoo dataset was used as the basis for simulations designed to
test the impact of changes in the relative abundances of taxa on in-
ferences of beta diversity. For each time bin, a dataset was simulated
with the same sample size as the original data from that bin, but the
specimens present in each locality were drawn at random from the
original frequency distribution, i.e. the probability of drawing a spec-
imen of a particular taxon is that taxon’s frequency in the original
dataset. Thus, the fauna was assumed to be homogenous, and any
differences between the localities in the time bin would simply be
due to the incomplete sampling. Having created a simulated dataset,
four distance metrics were used to infer the pairwise taxonomic dis-
tance between each locality, the mean of the pairwise distances rep-
resenting the beta diversity: the Sørenson index (Sørenson, 1948);
the Lennon index (Lennon, Koleff, Greenwood, & Gaston, 2001); a
recent modification of the Forbes index, hereafter the Forbes* index
(Alroy, 2015); and the Bray–Curtis index (Bray & Curtis, 1957). The
first three of these are based on presence–absence data, while the
Bray–Curtis index uses the observed abundances. The Forbes* and
Sørenson indices are similarity measures, so to convert them to a
distance measure the values were subtracted from 1. For each time
bin, 100 of the above simulations were run.
Another set of simulations was run using an identical procedure
to that described above, but incorporating subsampling, in order to
ascertain whether differences in beta diversity between the time
bins were due to differences in sampling heterogeneity or the abun-
dance distributions. As suggested by Alroy (2010) and Chao and Jost
(2012), the samples were standardized to fixed coverage rather than
a fixed sample size using the algorithm proposed by Alroy (2014). For
each locality within the dataset, individuals are drawn one at a time
until the sample is complete, each time calculating the coverage of
the sample using Good’s u (the proportion of singletons relative to
the total number of individuals, Good, 1953). Beta diversity is cal-
culated at each point where u crosses the specified coverage. The
data were standardized to a coverage of 0.6 (the highest coverage
allowing inclusion of all AZs), with 10,000 subsampling trials.
To test how changes in the relative abundance distribution af-
fect the result, the mean of the values obtained by the simulations
BROCKLEHURST et al.
on |
was compared to the Evar evenness index each AZ. A fauna with a
high value of Evar index contains a set of species with very similar
relative abundances (Smith & Wilson, 1996). The correlation of mean
simulation values for each AZ with the respective Evar values was
assessed using the Pearson product moment correlation coefficient,
calculated in r version 3.3.2 (R Core Team, 2016).
2.3 | A new procedure for calculating beta diversity
We propose that when calculating the beta diversity of an assem-
blage, one should not simply use the raw mean pairwise distance
value calculated; instead, one should ascertain how much higher this
raw value is than that which would be expected were a homogenous
assemblage with the same relative abundance distribution to be
sampled to the same extent as the empirical data. The simulations
described above provide an excellent framework for this calculation.
The following procedure is therefore proposed for or each
­assemblage/time bin:
1. Calculate the raw beta diversity using one of the available
distance metrics.
2. For each locality within the assemblage draw the same number of
specimens present at random from a frequency distribution rep-
resenting the observed relative abundances of the taxa.
3. Calculate beta diversity of the simulated dataset.
4. Repeat steps two and three 100 times or more, and calculate the
mean of the results. This value will represent the null expecta-
tion: the beta diversity to be expected if the fauna was homoge-
nous but sampled as incompletely as the observed data. 95%
confidence intervals around the mean are also calculated.
5. Subtract the values obtained in step four from that in step one.
Since at this point the maximum possible beta diversity value will
equal one minus the result of step four, and will therefore be dif-
ferent for each dataset, the values are rescaled using the equa-
tion: (O − N)/(1 − N), where O is the observed beta diversity, and
N is the result of step 4.
The procedure produces a beta diversity metric where the
maximum value (obtained when no overlap is observed between
species) is 1 and a homogenous fauna will have confidence inter-
vals bracketing 0. This entire procedure has been automated in r To illustrate the accuracy of the reconstructions of raw and RAC
using functions from the package vegan (Oksanen et al., 2017). The
code for the function is provided in Data S9. The function allows
the option of carrying out standardization of the coverage of the
localities (both in the empirical and simulated datasets). Hereafter
this method is called Relative Abundance Corrected beta diversity
(RAC beta diversity).
2.4 | Testing the performance of RAC beta diversity
in simulations
Two classes of simulation were carried out to test the performance
of RAC beta diversity relative to raw beta diversity. The first class is
Methods in Ecology and Evolu
      3
designed to illustrate the ability of RAC beta diversity to correctly
identify when assemblages exhibit no difference in provinciality, and
the second to illustrate the ability of RAC beta diversity to correctly
identify the presence and extent of differences.
Under the first class, an assemblage containing up to 1,000,000
individuals in 50 species spread across two localities is generated.
The evenness of the relative abundance distribution is controlled by
drawing numbers of individuals of each species from a log-­normal
distribution, the variance of which represents an inverse measure of
the evenness. Species are assigned to localities, with the proportion
of species shared between the two localities being a controlled pa-
rameter. A fixed proportion of the individuals are sampled from each
locality, representing the incompleteness of sampling. The raw beta
diversity and the RAC beta diversity between the two localities is
calculated, (both using Forbes* distances).
In such simulations where the proportion of shared species and
the individual sampling probabilities are identical, the beta diversity
estimates of all should be identical. In practice, the raw beta diver-
sity values are expected to decrease with decreasing evenness (i.e.
higher variances of the log-­normal distribution). Thus, a regression
line between the variance and the raw beta diversity estimates ob-
tained is expected to have a negative slope. For the RAC beta di-
versity to be considered to outperform the raw beta diversity in
the context of these simulations (correctly identifying when assem-
blages have identical beta diversities), the slope the regression line
between the variance and the RAC beta diversity estimates should
be reduced (ideally 0).
One potential concern might be that the RAC method assumes
that the observed species frequency distribution is representative
of the true species frequency distribution i.e. that the probability of
fossilisation and sampling of each taxon is identical and therefore
the probability of a species being sampled is entirely dependent on
its abundance. The impact of inaccurate abundance distributions
was tested by assigning each taxon a probability of individual pres-
ervation drawn from a normal distribution. Simulations were also run
allowing the preservation probability of each taxon to differ depend-
ing on which locality was being sampled by drawing the preservation
probabilities separately; thus, the relative abundance distributions
observed will potentially not only differ from the true distribution
but also differ from each other.
beta diversity estimates at various levels of coverage (proportion of
species sampled), abundance distributions at fixed levels of even-
ness were generated as described above, and all species assigned
to both localities (true beta diversity of zero). Specimens were then
drawn from the species pool one by one until fixed levels of coverage
were reached, at which point raw and RAC beta diversity estimates
were calculated.
2.5 | Beta diversity of the Karoo
The RAC beta diversity through time was calculated for the Karoo
Supergroup to examine the changes in faunal provinciality through
 | Methods in Ecology and Evolu
on
4       BROCKLEHURST et al.
time. Beta diversity was inferred using both the raw data and data
with coverage standardized to 0.6 (the highest coverage allowing
inclusion of all AZs), with 10,000 subsampling trials.
3 |   R E S U LT S
3.1 | Assessing the impact of evenness on inferred
beta diversity
The simulated beta diversity null expectation calculated for each
Karoo AZ, despite the simulations assuming a homogeneous fauna
in each, show considerable variation (Figure 1). Although the ab-
solute numbers differ, each distance measure produces the same
pattern: the highest values in the Tapinocephalus and Daptocephalus
AZs and the lowest values in the Eodicynodon, Pristerognathus and
Tropidostoma AZs. This is not changed by subsampling.
The simulated beta diversity values, both with and without
subsampling, exhibit an extremely strong, highly significant cor-
relation with the Evar index (Table 1, Figure 2), indicating that the
variation in mean pairwise distances is strongly influenced by the
structure of the relative abundance distribution, and the issue is
not solved by coverage standardization. The correlation is positive,
supporting the predictions made in the Introduction: a more even
relative abundance distribution results in higher beta diversity
estimates.
F I G U R E   1   Mean beta diversity values
of the 100 simulated datasets drawn
from a homogenous fauna with the
relative abundance distributions of each
assemblage zones (AZ) from the Karoo
Supergroup. (a) Raw; (b) subsampled. Beta
diversity estimate represents the mean
pairwise distance using four distance
metrics. Eod, Eodicynodon AZ; Tap,
Tapinocephalus AZ; Prist, Pristerognathus
AZ; Trop, Tropidostoma AZ; Cist,
Cistecephalus AZ; Dapt, Daptocephalus AZ;
Lyst, Lystrosaurus AZ; Cyn, Cynognathus
AZ
3.2 | Assessing the performance of the RAC beta
diversity method
Under all simulations, the RAC beta diversity method was shown
to outperform the raw beta diversity estimate. The first class of
simulations indicate that it is better to be able to infer a lack of
difference in beta diversity in assemblages of different evenness
(Table 2). When sampling is 10%, in fact, the regression line com-
paring evenness to the RAC beta diversity estimate is almost flat
(Figure 3a,b), even when the preservation potential of the taxa
varies (Figure 3e), indicating the method is consistently identify-
ing that assemblages with different evenness have the same beta
diversity. At poorer levels of sampling (Figure 3c,d,f,h), the slope
of the regression line increases, indicating that resilience of the
method to variations in the relative abundance distribution is de-
creasing, but in no set of parameters tested does the slope exceed
that of the raw estimate. However, even though the method is
robust to different taxa having different preservation potentials,
it is less robust to having differing preservation potential between
the two localities (Figure 3g,h), albeit still outperforming raw beta
diversity.
The second class of simulations demonstrates that the RAC
method produces results closer to the true beta diversity at all levels
of coverage. When evenness is high, raw beta diversity estimates
show an almost linear relationship with coverage (Figure 4a). As
BROCKLEHURST et al. Methods in Ecology and Evolu
on |
      5

TA B L E   1   Results of correlation tests between mean pairwise

distances between localities in homogenous faunas simulated from
the Karoo data and the evenness of the assemblages

Correlation test Pearson’s R p value

Forbes* distance (raw) ~ Evenness .837 .010

Forbes* distance (subsampled) .706 .050
~ Evenness
Sørenson distance (raw) ~ Evenness .868 .004
Sørenson distance (subsampled) .798 .031
~ Evenness
Lennon distance (raw) ~ Evenness .823 .004
Lennon distance (subsampled) .798 .031
~ Evenness
Bray–Curtis distance (raw) .836 .010
~ Evenness
Bray–Curtis distance (subsampled) .731 .049
~ Evenness
RAC Forbes* beta diversity (raw) .080 .850
~ Evenness
RAC Forbes* beta diversity .002 .996
(subsampled) ~ Evenness

RAC, Relative Abundance Corrected.

evenness decreases, the beta diversity inferred at low levels of cov-
erage is closer to the true value of zero, but the rate of improvement
as coverage increases is not so rapid (Figure 4b–d). This supports the
results of Beck et al. (2013), who suggested that it was at low lev-
els of evenness that beta diversity estimates were most inaccurate
when sampling is poor. RAC beta diversity gives similar results at all
levels of evenness; at all coverage levels, RAC beta diversity is closer
to the true value of zero than raw beta diversity, and the variation in
the values obtained is lower (Figure 4). The rate of improvement as
coverage increases is not so fast as that observed in the raw diversity
estimate until a coverage of about 0.9 is reached, at which point the
curves show an inflection.
F I G U R E   2   Comparison of the mean beta diversity values (mean
pairwise taxonomic distance) obtained from the homogenous
datasets simulated from the Karoo data using the Forbes* distance
metric, and the evenness of each assemblage measured. (a) Raw;
(b) subsampled. Dashed lines represent regression lines.
Abbreviations as in Figure 1
curves indicate a rise in RAC beta diversity across the Permian/
Triassic boundary.
4 | D I S CU S S I O N

4.1 | Abundance and beta diversity

3.3 | Empirical analyses
The empirical beta diversity estimates for the Karoo, calculated as
the mean pairwise Forbes* distances between localities (Figure 5;
see Data S10 for results from other distance metrics), both with
and without subsampling, show similar trends to the curve pro-
duced by simulating homogenous faunas. This indicates that a
large amount of the variation observed when raw beta diversity
is calculated is a result of variations in the relative abundance
distribution rather than variation in provinciality. No significant
correlation is found between RAC beta diversity and evenness
(Table 1).
Both raw and subsampled data indicates a fall in RAC beta
diversity between the Eodicynodon and Pristerognathus AZs
(Figure 6). The subsampled data indicates RAC beta diversity sta-
bilized at this point until the end of the Permian, while the raw data
suggests the decrease continued until the Cistecephalus AZ. Both
The study of variations in faunal provinciality through geological
time is of great significance in studying macroevolutionary patterns,
with some studies suggesting that beta diversity may have had
more influence than alpha diversity on changes in gamma diversity
(Bambach, 1977; Sepkoski, 1988). Several studies have highlighted
substantial changes in beta diversity coinciding with major radia-
tions and mass extinctions (e.g., Button, Lloyd, Ezcurra, & Butler,
2017; Clapham, Shen, & Bottjer, 2009; Na & Kiessling, 2015; Sahney
& Benton, 2008; Sahney, Benton, & Falcon-­L ang, 2010; Sidor et al.,
2013). When considering this, the impact of changes in relative
abundance distributions on estimates of beta diversity in the fos-
sil record is particularly concerning. It is during such environmental
and faunal upheavals that significant changes in abundance distribu-
tions occur (Preston, 1948; McKinney & Lockwood, 1999; McElwain
& Punyasena, 2007; Wilson, 1992) e.g. the prevalence of pioneer/
disaster taxa following environmental upheaval (Hallam & Wignall,
 | Methods in Ecology and Evolu
on
6       BROCKLEHURST et al.

TA B L E   2   Slope (m) of the regression line comparing beta diversity estimates of simulated faunas to using the Forbes* distance metric to
the variance of the log-­normal distribution used to simulate the abundance distribution (an inverse measure of evenness); ideally slope
should be 0

Sampling probability of Sampling probability Proportion of taxa shared m of raw beta m of RAC beta
individuals of each taxon varies by locality? between localities diversity ~ variance diversity ~ variance

10% NA 1 −0.022 −0.005

10% NA 0.5 −0.024 −0.005
5% NA 1 −0.061 −0.032
5% NA 0.5 −0.067 −0.040
Drawn from normal distribution No 1 −0.021 −0.005
(M = 0.1)
Drawn from normal distribution Yes 1 −0.034 −0.019
(M = 0.1)
Drawn from normal distribution No 1 −0.057 −0.028
(M = 0.05)
Drawn from normal distribution Yes 1 −0.083 −0.058
(M = 0.05)

RAC, Relative Abundance Corrected.

1997; Harries, Kauffman, & Hansen, 1996; Pielou, 1975; Rodland &
Bottjer, 2001; Schubert & Bottjer, 1995).
When simulating homogenous faunas from Karoo data, the
lowest mean pairwise distances are produced when drawing spec-
imens from Eodicynodon, Pristerognathus and Tropidostoma AZ fau-
nas. These AZs also have the lowest evenness, being characterized
by single overwhelmingly abundant taxa. In the Pristerognathus and
Tropidostoma AZs, the taxon is Diictodon feliceps, of which more than
200 specimens are known from each; the second most abundant taxa
in the two AZs have produced 39 and 54 specimens respectively. On
the other hand, high mean pairwise distances are produced when
drawing from the Tapinocephalus and Daptocephalus AZ faunas,
where no such dominance is present. In the former Diictodon is still
the most abundant taxon, but there is not such a gap between it
and the other species, while in the latter the dicynodonts Oudenodon
bainii, Dicynodon lacerticeps and Diictodon feliceps assemblages with
two localities have very similar abundances. The simulations based
on assemblages of two localities support these results; under all
sampling regimes tested, raw beta diversity will vary heavily accord-
ing to the evenness of the relative abundance even when the true
provinciality does not.
These results bear out the predictions made in the
Introduction: when homogenous assemblages with more even
abundance distributions are subjected to incomplete sampling,
beta diversity estimates will be higher than similarly sampled less
even assemblages; thus, the two are not directly comparable. In
fact, the beta diversity curves simulated from Karoo data but
assuming homogenous faunas in each time bin, show very simi-
lar trends to the actual beta diversity estimates (Figure 5). This
would indicate that much of the observed variation in faunal pro-
vinciality is actually a result of the shift in null expectation rather
than variation in provinciality. What is particularly surprising is
that the same pattern is observed when using the Bray–Curtis
distances, incorporating the absolute frequencies rather than
presence–absence data.
The fact that incomplete sampling means that a homogenous as-
semblage will not produce the true beta diversity value of 0 is not a
new observation (Chao et al., 2005). Nevertheless, all studies of beta
diversity still make comparisons where 0 is treated as the null ex-
pectation. RAC beta diversity accounts for the fact that the null ex-
pectation is unique to each assemblage, and the faunal provinciality
of an assemblage should be measured as deviation of the observed
beta diversity value from the null expectation of that specific assem-
blage. The simulations show that under all sampling regimes tested,
the RAC beta diversity estimate show a weaker relationship with the
evenness of the relative abundance distribution than the raw esti-
mate (although the strength of the relationship does increase when
sampling levels are lowered). Moreover, at all levels of coverage, the
RAC beta diversity estimate produces more accurate results than
the raw estimates. It should, however, be noted that at lower cover-
age levels (below 0.9), the simulations suggest that the RAC method
will still overestimate beta diversity, albeit not to the same degree as
a raw estimate.
The RAC beta method starts with certain assumptions, perhaps
the most important of which is that the abundance distribution pre-
served in the fossil record is the same or similar shape to the original
distribution. This is an issue that has been discussed extensively in
the published literature (e.g. Bambach & Bennington, 1996; Kidwell,
2001, 2002; McKinney, 1997; McKinney, Lindgard, Sepkoski, &
Taylor, 1998; Vermeij & Herbert, 2004). While it does seem reason-
able that more abundant species will have a higher probability of
making it into the fossil record, thus preserving the distribution, po-
tential confounding issues including variable preservation potential
of different biogenic material in different environments (e.g. Cherns
& Wright, 2000, 2009; Wright, Cherns, & Hodges, 2003), differ-
ent preservation potential of different body sizes (Brocklehurst,
BROCKLEHURST et al. Methods in Ecology and Evolu
on |
      7

F I G U R E   3   Raw and Relative Abundance Corrected (RAC) beta diversity estimates of simulated data compared to evenness of the fauna.
Coloured points represent the beta diversity estimates of individual simulations, and the lines represent the regression line between beta
diversity and evenness. The true proportion of taxa shared between the two localities is 100% (a,c,e,f,g,h) and 50% (b,d). a, b, c and d have
fixed sampling probabilities of 1% (a,b) and 0.5% (c,d). In e–h, the sampling probabilities of each taxon are drawn from a normal distribution
with a mean of 0.01 (e,g) or 0.005 (f,h). In g and h, the sampling probabilities of each taxon differs by locality
 | Methods in Ecology and Evolu on
8       BROCKLEHURST et al.

F I G U R E   4   Raw (red) and Relative Abundance Corrected (RAC) beta diversity estimates of simulated datasets, sampled to different
coverages. True beta diversity in each case is 0. Variance of log-­normal distribution used to determine evenness of abundance distribution
(high variance = low evenness): (a) 1; (b) 2; (c) 3; (d) 4; (e) 5

Upchurch, Mannion, & O’Connor, 2012; Brown, Evans, Campione,
O’Brien, & Eberth, 2013; Kammerer, 2016) and the human collecting
biases e.g. preference for collection of impressive specimens for mu-
seums (Brown et al., 2013). Nevertheless, several studies have exam-
ined ecology in the fossil record assuming the observed distributions
are accurate (e.g. Codron, Botha-­
Brink, Codron, Huttenlocker, &
Angielczyk, 2016; Jernvall & Fortelius, 2002; Kidwell & Brenchley,
1994, 1996).
Such assumptions have been justified by studies suggesting
that relative abundance distributions are preserved reasonably ac-
curately, even with the vagaries of the fossil record (Kidwell, 2001,
2002). Another point worth mentioning is that the confounding fac-
tors potentially impacting the abundance distribution are not nec-
essarily confounding the estimates of RAC beta diversity. If there
is a bias towards the preservation of larger specimens in the Karoo
(Kammerer, 2016), then variability in body size will affect the raw
beta diversity estimates in the same way as variability in abundance
would. That is, one very large species would have the same effect as
one very abundant species: being more likely to be preserved in all
localities and thus lowering the beta diversity.
It might be more accurate to state that the RAC beta diversity
method is correcting for variable fossilisation potential of the spe-
cies, although much of our discussion has assumed that this is due
to different relative abundances due to the studies cited above sug-
gesting that this is a large factor in preservation potential. It should
be noted that the assumptions would likely not hold in a study based
on a wider geographical spread, potentially containing multiple as-
semblages with varying modes of preservation. Nevertheless, the
BROCKLEHURST et al. Methods in Ecology and Evolu
on |
      9

F I G U R E   5   Comparison of the beta

diversity calculated from the empirical
data from the Karoo dataset to the mean
values obtained from the homogenous
simulated datasets using the Forbes*
distance metric. Narrow lines represent
95% confidence intervals.
(a) raw; (b) subsampled (coverage = 0.6).
Abbreviations as in Figure 1

F I G U R E   6   Relative Abundance
Corrected (RAC) beta diversity through
time within the Karoo. The thick lines
represent the RAC beta diversity
estimate, the narrow lines represent 95%
confidence intervals. Abbreviations as in
Figure 1

simulations indicate that such confounding factors do not appear to
render the RAC beta diversity estimate less accurate than the raw
beta diversity estimate.
One important consideration is the non-­independence between
abundance and range size. It has long been observed that locally
abundant species tend to have larger range sizes (Brown, 1984;
Gaston, 1994, 1996; Gaston, Blackburn, & Lawton, 1997; Lawton,
1993). The reason for this relationship is not clear, with suggested
mechanisms including the resource breadth hypothesis (species with
broader environmental tolerances will have higher local densities
and be less geographically restricted, Brown, 1984; Kotze, Niemelä,
O’hara, & Turin, 2003), resource availability (taxa which use wide-
spread and abundant resources will themselves be widespread and
abundant, Hanski, Kpiki, & Halkka, 1993; Gaston, 1994). Thus, an
assemblage with a less even relative abundance distribution will
genuinely have a lower beta diversity, as there are fewer taxa with
exceptionally high abundance and thus fewer taxa with large range
sizes. This fact emphasises that variation in the abundance distri-
bution is not merely a “nuisance parameter” whose signal needs to
be removed, but is indeed an important ecological characteristic
 | Methods in Ecology and Evolu
on
10       BROCKLEHURST et al.
(Chao & Jost, 2015). This consideration does not invalidate the RAC
method, since the method assesses the shift in null by assigning all
taxa to all localities rather than by treating abundant and rare taxa
differently or by rarefying the sample (which exaggerates the influ-
ence of common taxa, Alroy et al., 2001). Nevertheless, the issue
does highlight the fact that one cannot summarize the complexity of
an ecosystem with a single number (Chao & Jost, 2015).
4.2 | Faunal provinciality in the Karoo
The Karoo Supergroup has produced an unparalleled sample of late
Palaeozoic–early Mesozoic tetrapods, and provides near-­continuous
sedimentation across the end-­Permian mass extinction (Rubidge,
1995; Rubidge, 2005). It is the primary source of data on macroevo-
lutionary patterns in terrestrial vertebrates during this crucial time,
although recent studies have suggested that treating the Karoo as
representative of the global pattern is problematic (Brocklehurst,
Day, Rubidge, & Fröbisch, 2017; Sidor et al., 2013).
It has been suggested that tetrapod-­bearing formations across
Gondwana show an increase in faunal provinciality across the
Permian–Triassic boundary (Sidor et al., 2013). However, Button
et al. (2017), employing a method accounting for the phylogenetic
non-­independence of the taxa in each locality, inferred increased
cosmopolitanism following the extinction. In these studies, the fau-
nas being compared were tetrapod-­bearing basins or bioregions, and
so the Karoo was treated as a single entity. However, the fossilifer-
ous localities cover an area of more than 160,000 km2 and it is not
unreasonable to expect separate faunal provinces within this basin,
driven by differences in habitats or geographical barriers limiting
dispersal.
The RAC beta diversity method with subsampling applied
indicates an increase in beta diversity of the Karoo across the
Permian/Triassic boundary. This contradicts the results obtained
by Button et al. (2017), who suggested a more homogenous fauna
at this time. While it is possible that the differences are due to the
different scale of the analyses (global vs. regional), another pos-
sibility is that the results of Button et al. (2017) were influenced
by the increased unevenness of the tetrapod faunas following the
extinction and the prevalence of disaster taxa like Lystrosaurus
(Fröbisch, 2014; Wignall, 2007). Unfortunately, due to the lack of
abundance data in the Button et al. dataset, this cannot be tested.
It should be noted that, while the networking statistics employed
by Button et al. (2017) are in theory subject to the same influ-
ence of variations in the relative abundance distributions, their
study also incorporated a correction for the phylogenetic non-­
independence of the taxa. Further study is required to examine
how the phylogenetic networking method responds to the influ-
ence of the abundance distribution.
AC K N OW L E D G E M E N T S
We would like to thank Roger Benson, John Alroy, Roger Close and
two anonymous reviewers for helpful comments and discussion.
This study was funded by Deutsche Forschungsgemeinschaft grant
number FR 2457/5-­1, awarded to J.F. Data collection was funded by
the DST/NRF Centre of Excellence in Palaeoscience, the National
Research Foundation (NRF) and the Palaeontological Scientific Trust
(PAST) and its Scatterlings of Africa programmes.
AU T H O R S ’ C O N T R I B U T I O N S
N.B., designed the methods, analyses and simulation, wrote the
manuscript; M.O.D., collected the data, wrote the manuscript; J.F.,
collected the data, wrote the manuscript.
DATA AC C E S S I B I L I T Y
Data deposited in the Dryad Digital Repository (http://datadryad.
org/resource/doi:10.5061/dryad.gh0q91j) (Brocklehurst, Fröbisch,
& Day, 2018).
ORCID
Neil Brocklehurst  http://orcid.org/0000-0003-2650-5480
REFERENCES
Alroy, J. (2000). New methods for quantifying macroevolutionary
patterns and processes. Paleobiology, 26, 707–733. https://doi.
org/10.1666/0094-8373(2000)026<0707:NMFQMP>2.0
.CO;2
Alroy, J. (2010). Geographical, environmental and intrinsic biotic con-
trols on Phanerozoic marine diversification. Palaeontology, 53,
1121–1235.
Alroy, J. (2014). Accurate and precise estimates of origination and extinc-
tion rates. Paleobiology, 40, 374–397. https://doi.org/10.1666/13036
Alroy, J. (2015). A new twist on a very old binary similarity coefficient.
Ecology, 96, 575–586. https://doi.org/10.1890/14-0471.1
Alroy, J., Marshall, C. R., Bambach, R. K., Bezusko, K., Foote, M., Fürsich,
F. T., … Jacobs, D. K. (2001). Effects of sampling standardization
on estimates of Phanerozoic marine diversification. Proceedings of
the National Academy of Sciences of the United States of America, 98,
6261–6266. https://doi.org/10.1073/pnas.111144698
Bambach, R. K. (1977). Species richness in marine benthic habitats
through the Phanerozoic. Paleobiology, 3, 152–167. https://doi.
org/10.1017/S0094837300005236
Bambach, R. K., & Bennington, J. B. (1996). Do communities evolve? A
major question in evolutionary paleoecology. In D. Jablonski, D. H.
Erwin, & J. H. Lipps (Eds.), Evolutionary paleobiology (pp. 123–160).
Chicago, IL: University of Chicago Press.
Beck, J., Holloway, J. D., & Schwanghart, W. (2013). Undersampling and
the measurement of betadiversity. Methods in Ecology and Evolution,
4, 370–382. https://doi.org/10.1111/2041-210x.12023
Bray, J. R., & Curtis, J. T. (1957). An ordination of the upland forest com-
munities of southern Wisconsin. Ecological Monographs, 27, 325–349.
https://doi.org/10.2307/1942268
Brocklehurst, N., Day, M. O., Rubidge, B. S., & Fröbisch, J. (2017). Olson’s
Extinction and the latitudinal biodiversity gradient of tetrapods
in the Permian. Proceedings of the Royal Society B, 284, 20170231.
https://doi.org/10.1098/rspb.2017.0231
Brocklehurst, N., Fröbisch, J., & Day, M. O. (2018). Data from: Accounting
for differences in species frequency distributions when calculating
BROCKLEHURST et al.
on |
beta diversity in the fossil record. Dryad Digital Repository, http://dx.
doi.org/10.5061/dryad.gh0q91j
Brocklehurst, N., Upchurch, P., Mannion, P. D., & O’Connor, J. (2012). The
completeness of the fossil record of Mesozoic birds: Implications for
early avian evolution. PLoS ONE, 7, e39056. https://doi.org/10.1371/
journal.pone.0039056
Brown, J. H. (1984). On the relationship between abundance and dis-
tribution of species. American Naturalist, 124, 255–279. https://doi.
org/10.1086/284267
Brown, C. M., Evans, D. C., Campione, N. E., O’Brien, L. J., & Eberth, D.
A. (2013). Evidence for taphonomic size bias in the Dinosaur Park
Formation (Campanian, Alberta), a model Mesozoic terrestrial alluvial-­
paralic system. Palaeogeography, Palaeoclimatology, Palaeoecology,
372, 108–122. https://doi.org/10.1016/j.palaeo.2012.06.027
Bush, A. M., Markey, M. J., & Marshall, C. R. (2004). Removing bias from
diversity curves: The effects of spatially organized biodiversity on
sampling-­standardization. Paleobiology, 30, 666–686. https://doi.org
/10.1666/0094-8373(2004)030<0666:RBFDCT>2.0.CO;2
Button, D., Lloyd, G. T., Ezcurra, M. D., & Butler, R. J. (2017). Mass ex-
tinctions drove increased global faunal cosmopolitanism on the su-
percontinent Pangaea. Nature Communications, 8, 733. https://doi.
org/10.1038/s41467-017-00827-7
Chao, A., Chazdon, R. L., Colwell, R. K., & Shen, T. J. (2005). A new sta-
tistical approach for assessing similarity of species composition with
incidence and abundance data. Ecology Letters, 8, 148–159.
Chao, A., & Jost, L. (2012). Coverage-­based rarefaction and extrap-
olation: Standardising samples by completeness rather than size.
Ecology, 93, 2533–2547. https://doi.org/10.1890/11-1952.1
Chao, A., & Jost, L. (2015). Estimating diversity and entropy profiles via
discovery rates of new species. Methods in Ecology and Evolution, 6,
873–882. https://doi.org/10.1111/2041-210X.12349
Cherns, L., & Wright, V. P. (2000). Missing molluscs as evidence of large-­
scale, early skeletal aragonite dissolution in a Silurian sea. Geology, 28,
791–794. https://doi.org/10.1130/0091-7613(2000)28<791:MM
AEOL>2.0.CO;2
Cherns, L., & Wright, V. P. (2009). Quantifying the impacts of early diage-
netic aragonite dissolution on the fossil record. Palaios, 24, 756–771.
https://doi.org/10.2110/palo.2008.p08-134r
Clapham, M. E., Shen, S., & Bottjer, D. J. (2009). The double mass extinc-
tion revisited: Reassessing the severity, selectivity, and causes of the
end-­Guadalupian biotic crisis (Late Permian). Paleobiology, 35, 32–50.
https://doi.org/10.1666/08033.1
Codron, J., Botha-Brink, J., Codron, D., Huttenlocker, A. K., &
Angielczyk, K. D. (2016). Predator-­p rey interactions amongst
Permo-­ Triassic terrestrial vertebrates as a deterministic factor
influencing faunal collapse and turnover. Journal of Evolutionry
Biology, 30, 40–54.
Day, M. O., Ramezani, J., Bowring, S. A., Sadler, P. M., Erwin, D. H., Abdala,
F., & Rubidge, B. S. (2015). When and how did the terrestrial mid-­
Permian mass extinction occur? Evidence from the tetrapod record of
the Karoo Basin, South Africa. Proceedings of the Royal Society B, 282,
20150834. https://doi.org/10.1098/rspb.2015.0834
Fröbisch, J. (2013). Vertebrate diversity across the end-­ Permian
mass extinction – Separating biological and geological signals.
Palaeogeography, Palaeoclimatology, Palaeoecology, 372, 50–61.
https://doi.org/10.1016/j.palaeo.2012.10.036
Fröbisch, J. (2014). Synapsid diversity and the rock record in the
Permian-Triassic Beaufort Group (Karoo Supergroup), South
Africa. In C. F. Kammerer, K. D. Angielczyk, & J. Fröbisch
(Eds.), The early evolutionary history of the Synapsida (pp.
305–320). Dordrecht, The Netherlands: Springer. https://doi.
org/10.1007/978-94-007-6841-3
Gaston, K. J. (1994). Rarity. London, UK: Chapman & Hall. https://doi.
org/10.1007/978-94-011-0701-3
Methods in Ecology and Evolu
      11
Gaston, K. J. (1996). The multiple forms of the interspecific abundance-­
distribution relationship. Oikos, 75, 211–220. https://doi.
org/10.2307/3546192
Gaston, K. J., Blackburn, T. M., & Lawton, J. H. (1997). Interspecific
abundance-­range size relationships: An appraisal of mechanisms.
Journal of Animal Ecology, 66, 579–601. https://doi.org/10.2307/5951
Good, I. J. (1953). The population frequencies of species and the estima-
tion of population parameters. Biometrika, 40, 237–264. https://doi.
org/10.1093/biomet/40.3-4.237
Hallam, A., & Wignall, P. B. (1997). Mass extinctions and their aftermath.
Oxford, UK: Oxford University Press.
Hanski, I., Kpiki, J., & Halkka, A. (1993). Three explainations of the posi-
tive relationship between distribution and abundance of species. In
R. Ricklefs & D. Schulter (Eds.), Historical and geographical determi-
nants of community diversity (pp. 108–116). Chicago, IL: University of
Chicago Press.
Harries, P. J., Kauffman, E. G., & Hansen, T. A. (1996). Models for bi-
otic survival following mass extinction. Geological Society, London,
Special Publications, 102, 41–60. https://doi.org/10.1144/GSL.
SP.1996.001.01.03
Irmis, R. B., Whiteside, J. H., & Kammerer, C. F. (2013). Non-­ biotic
controls of observed diversity in the paleontologic record: An
example from the Permo-­Triassic Karoo Basin of South Africa.
Palaeogeography, Palaeoclimatology, Palaeoecology, 372, 62–77.
https://doi.org/10.1016/j.palaeo.2012.07.014
Jernvall, J., & Fortelius, M. (2002). Common mammals drive the evolu-
tionary increase of hypsodonty in the Neogene. Nature, 417, 538–
540. https://doi.org/10.1038/417538a
Kammerer, C. F. (2016). A new taxon of cynodont from the Tropidostoma
Assemblage Zone (upper Permian) of South Africa, and the early evo-
lution of Cynodontia. Papers in Palaeontology, 2, 387–397. https://doi.
org/10.1002/spp2.1046
Kidwell, S. M. (2001). Preservation of species abundance in marine death
assemblages. Science, 294, 1091–1094. https://doi.org/10.1126/
science.1064539
Kidwell, S. M. (2002). Time-­averaged molluscan death assemblages:
Palimpsests of richness, snapshots of abundance. Geology, 30,
803–806. https://doi.org/10.1130/0091-7613(2002)030<0803
:TAMDAP>2.0.CO;2
Kidwell, S. M., & Brenchley, P. J. (1994). Patterns in biolclastic accumu-
lation through the Phanerozoic: Changes in input or distruction?
Geology, 22, 1139–1143. https://doi.org/10.1130/0091-7613(1994)0
22<1139:PIBATT>2.3.CO;2
Kidwell, S. M., & Brenchley, P. J. (1996). Evolution of the fossil re-
cord: Thickness trends in marine skeletal accumulations and their
implications. In D. Jablonski, D. H. Erwin, & J. H. Lipps (Eds.),
Evolutionary paleobiology (pp. 299–336). Chicago, IL: University of
Chicago Press.
Koleff, P., Gaston, K. J., & Lennon, J. J. (2003). Measuring beta diversity
for presence-­absence data. Journal of Animal Ecology, 72, 367–382.
https://doi.org/10.1046/j.1365-2656.2003.00710.x
Kotze, D. J., Niemelä, J., O’hara, R. B., & Turin, H. (2003). Testing
abundance‐range size relationships in European carabid beetles
(Coleoptera, Carabidae). Ecography, 26, 553–566.
Lande, R. (1996). Statistics and partitioning of species diversity, and
similarity among multiple communities. Oikos, 76, 5–13. https://doi.
org/10.2307/3545743
Lawton, J. H. (1993). Range, population abundance and conserva-
tion. Trends in Ecology and Evolution, 8, 409–413. https://doi.
org/10.1016/0169-5347(93)90043-O
Lennon, J. J., Koleff, P., Greenwood, J. J. D., & Gaston, K. J. (2001). The
geographical structure of British bird distributions: Diversity, spatial
turnover and scale. Journal of Animal Ecology, 70, 966–979. https://
doi.org/10.1046/j.0021-8790.2001.00563.x
 |
Methods in Ecology and Evolu
on
12       BROCKLEHURST et al.
McElwain, J. C., & Punyasena, S. W. (2007). Mass extinction events and
the plant fossil record. Trends in Ecology & Evolution, 22, 548–557.
https://doi.org/10.1016/j.tree.2007.09.003
McKinney, M. L. (1997). How do rare species avoid extinction? A pale-
ontological view. In W. E. Kunin & K. J. Gaston (Eds.), The biology of
rarity (pp. 110–129). Dordrecht, The Netherlands: Springer. https://
doi.org/10.1007/978-94-011-5874-9
McKinney, F. K., Lindgard, S., Sepkoski, J. J., & Taylor, P. D. (1998).
Decoupled temporal patterns of evolution and ecology in two post-­
Paleozoic clades. Science, 281, 807–809. https://doi.org/10.1126/
science.281.5378.807
McKinney, M. L., & Lockwood, J. L. (1999). Biotic homogenization: A
few winners replacing many losers in the next mass extinction.
Trends in Ecology & Evolution, 14, 450–453. https://doi.org/10.1016/
S0169-5347(99)01679-1
Na, L., & Kiessling, W. (2015). Diversity partitioning during the Cambrian
radiation. Proceedings of the National Academy of Sciences of the
United States of America, 112, 4702–4706. https://doi.org/10.1073/
pnas.1424985112
Oksanen, J., Blanchet, F. G., Friendly, M., Kindt, R., Legendre, P., McGlinn,
D., … Wagner, H. (2017). vegan: Community Ecology Package. R
package version 2.4-6.
Pielou, E. C. (1975). Ecology diversity. New York, NY: John Wiley and Sons.
Preston, F. W. (1948). The commonness, and rarity, of species. Ecology,
29, 254–283. https://doi.org/10.2307/1930989
R Core Team. (2016). R: A language and environment for statistical comput-
ing. Vienna, Austria: R Foundation for Statistical Computing.
Rodland, D. L., & Bottjer, D. J. (2001). Biotic recovery from the end-­
Permian mass extinction: Behavior of the inarticulate brachio-
pod Lingula as a disaster taxon. Palaios, 16, 95–101. https://doi.
org/10.1669/0883-1351(2001)016<0095:BRFTEP>2.0.CO;2
Rubidge, B. S. (1995). Biostratigraphy of the Beaufort Group (Karoo Supergroup).
Pretoria, South Africa: South African Committee for Straticgraphy.
Rubidge, B. S., (2005). 27th Du Toit Memorial Lecture: Re-uniting lost con-
tinents–fossil reptiles from the ancient Karoo and their wanderlust.
South African Journal of Geology, 108, 135–172.
Rubidge, B. S., Erwin, D. H., Ramezani, J., Bowring, S. A., & de Klerk, W. J.
(2013). High-­precision temporal calibration of Late Permian vertebrate
biostratigraphy: U-­Pb zircon constraints from the Karoo Supergroup.
Geology, 41, 363–366. https://doi.org/10.1130/G33622.1
Sahney, S., & Benton, M. J. (2008). Recovery from the most profound
mass extinction of all time. Proceedings of the Royal Society B, 275,
759–765. https://doi.org/10.1098/rspb.2007.1370
Sahney, S., Benton, M. J., & Falcon-Lang, H. J. (2010). Rainforest collapse
triggered Carboniferous tetrapod diversification in Euramerica.
Geology, 38, 1079–1082. https://doi.org/10.1130/G31182.1
Schubert, J. K., & Bottjer, D. J. (1995). Aftermath of the Permian-­Triassic
mass extinction event: Paleoecology of Lower Triassic carbonates in
the western USA. Palaeogeography, Palaeoclimatology, Palaeoecology,
116, 1–39. https://doi.org/10.1016/0031-0182(94)00093-N
View publication stats
Sepkoski, J. J. (1988). Alpha, beta, or gamma: Where does all the di-
versity go? Paleobiology, 14, 221–234. https://doi.org/10.1017/
S0094837300011969
Sidor, C. A., Vilhena, D. A., Angielczyk, K. D., Huttenlocker, A. K., Nesbitt,
S. J., Peecook, B. R., … Tsuji, L. A. (2013). Provincialization of terres-
trial faunas following the end-­Permian mass extinction. Proceedings
of the National Academy of Sciences of the United States of America,
110, 8129–8133. https://doi.org/10.1073/pnas.1302323110
Smith, B., & Wilson, J. B. (1996). A consumer’s guide to evenness indices.
Oikos, 76, 70–82. https://doi.org/10.2307/3545749
Sørenson, T. (1948). A method of establishing groups of equal amplitude
in plant sociology based on similarity of species content and its appli-
cation to analyses of the vegetation on Danish commons. Biologiske
Skrifter, 5, 1–34.
Vermeij, G. J., & Herbert, G. S. (2004). Measuring relative abundance in
fossil and living assemblages. Paleobiology, 30, 1–4. https://doi.org/1
0.1666/0094-8373(2004)030<0001:MRAIFA>2.0.CO;2
Whittaker, R. H. (1960). Vegetation of the Siskiyou mountains, Oregon
and California. Ecological Monographs, 30, 279–338. https://doi.
org/10.2307/1943563
Wignall, P. B. (2007). The End-­ Permian mass extinction–how bad
did it get? Geobiology, 5, 303–309. https://doi.org/10.1111/j.
1472-4669.2007.00130.x
Wilson, E. O. (1992). The diversity of life. Cambridge, MA: Belnap Press.
Wolda, H. (1981). Similarity indices, sample size and diversity. Oecologia,
50, 296–302. https://doi.org/10.1007/BF00344966
Wright, P., Cherns, L., & Hodges, P. (2003). Missing molluscs: Field testing
taphonomic loss in the Mesozoic through early large-­scale aragonite
dissolution. Geology, 31, 211–214. https://doi.org/10.1130/0091-761
3(2003)031<0211:MMFTTL>2.0.CO;2
S U P P O R T I N G I N FO R M AT I O N
Additional Supporting Information may be found online in the
­supporting information tab for this article.
How to cite this article: Brocklehurst N, Day MO, Fröbisch J.
Accounting for differences in species frequency distributions
when calculating beta diversity in the fossil record. Methods
Ecol Evol. 2018;00:1–12. https://doi.org/10.1111/2041-
210X.13007