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Methods in Ecology and Evolution 2010, 1, 3844 doi: 10.1111/j.2041-210X.2009.00003.

Comparing measures of species diversity from

incomplete inventories: an update
Jan Beck* and Wolfgang Schwanghart
Department of Environmental Sciences, University of Basel, Basel, Switzerland

1. Measuring biodiversity quantitatively is a key component to its investigation, but many meth-
ods are known to be biased by undersampling (i.e. incomplete inventories), a common situation in
ecological eld studies.
2. Following a long tradition of comparing measures of alpha diversity to judge their usefulness,
we used simulated data to assess bias of nine diversity measures some of them proposed fairly
recently, such as estimating true species richness depending on the completeness of inventories
(Brose, U. & Martinez, N.D. Oikos (2004) 105, 292), bias-corrected Shannon diversity (Chao, A. &
Shen, T.-J. Environmental and Ecological Statistics (2003) 10, 429), while others are commonly
applied (e.g. Shannons entropy, Fishers a) or long known but rarely used (estimating Shannons
entropy from Fishers a).
3. We conclude that the eective number of species based on bias-corrected Shannons entropy
is an unbiased estimator of diversity at sample completeness c. >05, while below that it is still
less biased than, e.g., estimated species richness (Brose, U. & Martinez, N.D. Oikos (2004) 105,
4. Fishers a cannot be tested with the same rigour because it cannot measure the diversity of com-
pletely inventoried communities, and we present simulations illustrating this eect when sample
completeness approaches high values. However, we can show that Fishers a produces relatively sta-
ble values at low sample completeness (an eect previously shown only in empirical data), and we
tentatively conclude that it may still be considered a good (possibly superior) measure of diversity if
completeness is very low.
Key-words: alpha diversity, effective number of species, Shannons entropy, simulation,
species richness, undersampling bias

A common problem in many biodiversity studies is the

incompleteness of species inventories due to limited eld sam-
Biodiversity is a multifaceted phenomenon, and the existence pling particularly in very speciose systems such as tropical
of a plethora of methods to measure quantitatively some of its invertebrates. Only for sessile organisms, relating inventories
aspects is therefore not surprising (Purvis & Hector 2000). to the area of (complete inventoried) sampling plots allows
Evaluations of the usefulness and reliability of various mea- circumventing the problem. It is well known that undersam-
sures have a long history in ecological research (e.g. Hurlbert pling biases some diversity measures, hereby hindering a cor-
1971; May 1975; Taylor 1978; Kempton 1979; Wolda 1981; rect assessment of biodiversity patterns. Since the 1990s a
Peterson & Slade 1998; Brose, Martinez, & Williams 2003; variety of undersampling-corrections to species richness counts
Walther & Moore 2005; Beck & Kitching 2007; Chao et al. became popular (Colwell & Coddington 1994; Chazdon et al.
2009) as they promise to guide ecologists to the most appropri- 1998), aided by easy-to-use and free software (Chao & Shen
ate method for their respective data sets and research 2006; Colwell 2006).
questions. Recently, further methods have been made available that
address the issue of controlling diversity measures for under-
*Correspondence author. E-mail: sampling bias. Although these new methods (see below) were
Correspondence site: tested in their original descriptions for achieving the proposed

 2010 The Authors. Journal compilation  2010 British Ecological Society

Measuring diversity from incomplete inventories 39

goals, an updated comparison of method performances, Fishers a (Fisher, Corbet, & Williams 1943; sometimes also
including established ones, is lacking up to now. referred to as Williams a) was often recommended as the most
Using simulated data, we compare a number of still infre- reliable assessment of alpha diversity (e.g. Hayek & Buzas
quently applied methods for the measurement of alpha diver- 1997; Southwood & Henderson 2000; Magurran 2004),
sity to established techniques of particular interest (due to referring mostly to Taylor (1978) who used empirical data on
either to their widespread use and or their perceived applica- British moths to show superior discrimination ability between
bility to undersampled inventories). A similar assessment of sites and, most relevant to this study, no relationship (above a
measures for beta diversity is under way and will be published relatively low threshold) with sample size (n) in replicates from
separately. Table 1 provides an overview on the measures the same site. However, due to its inherent assumption of a log-
included in this study. arithmic series-type rank abundance structure of communities
Observed species richness is the most straightforward mea- (often corroborated empirically, but poorly understood; see
sure of alpha diversity, but it is also most clearly biased in the below) and because it is, rst and foremost, a curve-tting
presence of undersampling. Brose & Martinez (2004) suggested parameter without deeper implications and interpretations, it
that the performance of estimators of true species richness is disregarded by some biodiversity researchers. Even more
(Chazdon et al. 1998; Colwell 2006) for mobile organisms important is another limitation hinted in Taylor (1978, p. 10):
depends on the sample completeness (i.e. the proportion of it is an approximation [] justied by the small sample) that
observed species, related to those actually present at a site). is often not clearly appreciated. Because a is mainly (positively)
They formulated a decision framework that leads to the best aected by species numbers (Sobs) and (negatively) by individ-
species richness estimator for a given data set, based on a preli- ual numbers in a sample (n), the hypothetical, possibly unreal-
minary assessment of completeness. Note that Brose & Marti- istic (see Discussion) situation of a complete species inventory
nez (2004) used the term coverage to describe sample in a closed community inherently leads to decreasing a values
completeness, but this term had earlier been dened dierently if more individuals are sampled (and no new species can be
(Good & Toulmin 1956). found). Therefore, Fishers a cannot be used to assess the
Shannons measure of entropy has an excellent foundation diversity of a completely sampled community (corroborating
in information theory (see Ulanowicz 2001 for an insightful the limited theoretical foundation of this measure), and a val-
review). Recently, some of its properties have been rediscov- ues of incomplete samples cannot therefore be compared with
ered within the concept of eective number of species (Jost true values (see Discussion).
2006), which also facilitates its application to alternative Over 30 years ago Bulmer (1974) and May (1975) pointed
approaches of measuring beta diversity (Jost 2007). However, out that, with the assumption of a logseries species-abun-
as long as its sensitivity to undersampling persists (May 1975), dance distribution (SAD) in samples, Shannons entropy (H)
it is unwise to apply Shannons measure to many eld study- can be approximated from Fishers a. As true values for H
type biodiversity questions. In an attempt to solve this prob- are available, we can test the properties of this simple esti-
lem, bias-controlled Shannons entropy was introduced by mate, and therefore indirectly investigate the behaviour of
Chao & Shen (2003). Fishers a.

Table 1. Measures included in our methods comparison

Type Reference Remarks

Sobs: Observed species richness Species richness in samples; compared with STRUE
Sest: Estimated species richness Brose & Martinez Decision framework to use the best estimator of species
(coverage-based decision) (2004) richness for a data set; compared to STRUE.
H: Shannons entropy Ulanowicz (2001) Compared to HTRUE.
eH: Eective number of species Jost (2006) Exponent of Shannons entropy (eH); compared to eHTRUE.
Hbc: Bias-controlled Shannons entropy Chao & Shen (2003) Software by A. Chao available at;
compared to HTRUE.
eHbc: Bias-controlled eective number of Jost (2006) Exponent of bias-controlled Shannons entropy (eHbc);
species compared to eHTRUE.
Hfa: Estimating Shannons entropy from Bulmer 1974 Hfa 0577 + ln(a); compared to HTRUE.
Fishers a
eHfa: Estimated eective number of Jost (2006) Exponent of estimated Shannons entropy (eHfa), based on
species Fishers a; compared with eHTRUE.
FA: Fishers a Fisher et al. (1943) Curvature parameter of the expected species-abundance
relationship; see main text for properties.

Measures relating to the known, whole community of N individuals are indicated by the subscript TRUE (e.g. STRUE for true species
richness). Sample completeness (CompTRUE) is calculated as Sobs STRUE (note the discrepancy of this denition with estimated com-
pleteness = Sobs Sest in the Brose & Martinez (2004); termed coverage there) decision framework and some other publications.
Formulas for calculations, if not given in the table, can be found in the references.

 2010 The Authors. Journal compilation  2010 British Ecological Society, Methods in Ecology and Evolution, 1, 3844
40 J. Beck & W. Schwanghart

Using data with known properties allowed us to assess bias ties (diering in diversity), and for each of four sampling eorts (i.e.
(Walther & Moore 2005) of the dierent measures in simu- numbers of sampled individuals). We then compared nine dierent
lated, repeated sampling. Our primary aims are to uncover (i) alpha diversity measures with true values of the respective whole com-
which method provides unbiased estimates of the true diversity munities.
Many more measures of alpha diversity were proposed (see e.g.
and (ii) how this judgement depends on sampling intensity (i.e.
Hayek & Buzas 1997; Magurran 2004), but we had to restrict our
the completeness of the samples). This should allow a recom-
comparison to a handful of methods. We did not, in particular,
mendation of best methods at least within the compared include rarefaction approaches (e.g. Hurlbert 1971; Simberlo 1978;
parameter ranges (see Methods for details). As we could not Mao, Colwell, & Chang 2005), as these, by denition, cannot be com-
explore in depth, and even less present, all possible combina- pared without relating to sampling eort. Lande (1996) pointed out
tions of modelling assumptions (see Methods for details), we that Simpsons index is an unbiased diversity measure with interesting
set several parameters to values of realistic magnitude from the properties for measuring beta diversity, but its use has been discour-
perspective of the rst authors eld work experience on tropi- aged with regards to alpha diversity because of its strong dependency
cal moths (cf. Beck & Chey 2006, 2008). on the few most common species (e.g. Southwood & Henderson
Although free software is available for most methods employed,
Methods we rewrote the calculation of all measures in matlab syntax (http:// and integrated these with
We created articial data of ecological communities based on realis-
sampling simulations, so that the whole routine can be carried out
tic, but highly simplied assumptions. SADs follow a log-normal dis-
within one run. The BiodivToolbox is available as Electronic Supple-
tribution, with parameters of mean (l = 0507) and SD (r = 1183)
ment in Appendix S1 and can be used, for example, to explore results
similar to those observed in large light-trapping samples of moths
for other parameter settings. statistica 8 (
from Borneo (>600 individuals each; see Beck & Chey 2008 for data
was used for further data analysis.
sources and details). Log-normals are widely used to describe SADs
We calculated the scaled mean error (SME) of sample diversity
(Nekola & Brown 2007), and while there is a wide discussion on SADs
measures, as compared with true values of the whole community, as a
regarding mechanism (e.g. Volkov et al. 2007) or eects of habitat
measure of bias (Walther & Moore 2005). Scaled error measures (i.e.
type (e.g. May 1975; Beck & Chey 2006), eld data are often equivo-
relative to true diversities) were applied to facilitate comparison
cal regarding the best distribution model representing the data (e.g.
between communities of dierent diversity. We calculated SDs of the
log-normal, logarithmic series, and other distributions of the same
(scaled) error (which is an assessment of precision) and the 95% con-
general shape). In any case, we expect that a good diversity measure is
dence interval of the mean, i.e. SME (as CIM = SME 1984
robust to small deviations of SADs, making it unnecessary to model,
SD 10; 1984 being the t-value associated with 99 degrees of freedom,
e.g., logarithmic series distributions for comparison. Note, however,
and 10 being the square root of the 100 samples drawn). We call a
that Fishers a cannot be interpreted as a diversity if empirical SADs
diversity measure unbiased if the CI of its SME includes zero.
are far from this assumption. Investigation of sample SADs prior to
diversity analysis has been advised as a standard procedure (e.g.
Southwood & Henderson 2000). Results
We dened a local community (all species combined) as consist-
ing of N  100 000 individuals (few individuals due to rounding Table 2 shows all assessments of bias for the dierent mea-
to integer values; Wolda 1981 used the same community size in sures. Figure 1 presents SME as a function of completeness for
simulations). This is admittedly arbitrary and simplifying (see Dis- the best candidates, in our view, of diversity measures. Sobs
cussion). As our simulation is not spatially explicit, we had to (not shown) is, naturally, negatively biased over almost the
assure that even for very species-rich communities each species whole range of completeness, whereas Sest loses negative bias
occurs in at least several individuals. We also dened the species
at completeness c. >05, but is positively biased in some data
richness of the community, using several values for comparisons
simulations with high levels of sample completeness. Biases
(50, 100, 200 and 300 species). Under the assumption of a log-nor-
mal SAD, we could therefore calculate the absolute abundance of
and their CIs in entropy estimates (i.e. Shannons values H and
individuals per species. their estimates; not shown) appear generally smaller than in
We randomly sampled a dened number of individuals (100, 500, associated eective numbers of species (eH and their esti-
1000 and 2000) from the community. As some measures required mates), but these are simply transformation eects (entropies
repeated sampling (i.e. species richness estimators), we split these are log-transformations of diversities; Jost 2006). Conven-
samples in 20 random, equally large (regarding individuals numbers) tional H and eH are negatively biased at almost all levels of
subsamples. For each parameter setting sampling was carried out 100 sample completeness. Hbc and its associated eective
times. For the whole community as well as for each sample, we calcu- numbers of species (eHbc) are unbiased in most simulations
lated the diversity measures listed in Table 1, as well as the complete- with completeness >05. Hbc is the measure with lowest bias
ness of samples related to the true species richness of the whole
of all diversity estimates included here (Table 2). Hfa and eHfa
community. Note that the various versions of the eective number of
show positive bias at low completeness, but strong negative
species (eH, eHbc and eHfa) and the estimation of Hfa are algebraic
transformations of respective measures of entropy and a. These trans-
bias at high completeness. The latter may be an eect associ-
formations (exponentials or logarithms respectively), however, may ated with the peculiarities of Fishers a (see below).
aect assessments of bias, which is why we included them separately As expected, SME of many diversity measures are positively
in our comparison. In summary, thus, we mimicked 100 independent correlated with sample completeness (irrespectively of commu-
samples (consisting of 20 subsamples each) for each of four communi- nity species richness STRUE), converging to near-zero values at

 2010 The Authors. Journal compilation  2010 British Ecological Society, Methods in Ecology and Evolution, 1, 3844
Measuring diversity from incomplete inventories 41

Table 2. Scaled mean error (SME, in percent; see Walther & Moore
2005) for alpha diversity measures from sampling simulations of
dierent species richness and sampling intensity (n = number of
individuals sampled, all other parameters held constant at
N  100 000, l = 0507, r = 1183; see Table 1 for other

STRUE = 50 n = 100 n = 500 n = 1000 n = 2000

Sobs )261 )109 )19 )01

Sest 105 63 )02 )01
H )74 )17 )07 )04
eH )233 )55 )23 )13
Hbc )03 )03 )03 )03
eHbc )07 )09 )12 )11
Hfa )05 )87 )148 )187
eHfa )11 )251 )400 )474

Fig. 1. Sample completeness (CompTRUE) and scaled mean error

STRUE = 100 n = 100 n = 500 n = 1000 n = 2000 (SME), condence intervals of the mean (CIM) and the range of
2 SDs of the (scaled) error (i.e. the expected range for >95% of sam-
Sobs )532 )252 )95 )66 ple values). We show data only for selected diversity measures (see
Sest )101 53 49 28 main text and Table 2 for other results). If CIM include zero, the mea-
H )109 )30 )12 )06 sure can be considered unbiased.
eH )351 )103 )48 )20
Hbc )12 04 )01 00
eHbc )39 17 )03 )01
Hfa 24 30 )60 )36 Fishers a appear highly inaccurate and positively biased if
eHfa 113 118 )212 28 compared in the same manner as the other measures (data
not shown), but this is, at least partly, the consequence of its
STRUE = 200 n = 100 n = 500 n = 1000 n = 2000 denition (see Introduction). In the absence of a true a
value, we can only assess the criterion of independence from
Sobs )728 )337 )217 )95 sample completeness. We simulated communities of 50, 100,
Sest )351 39 )10 58
200 and 300 species (individual numbers and all other set-
H )157 )46 )24 )11
eH )497 )190 )99 )50 tings as above) and drew 100 replicate samples each of 500
Hbc )42 )03 03 )01 varying sample sizes (n). To our knowledge this is the rst
eHbc )158 )10 13 )03 time a was tested on simulated data (note that with constant
Hfa 13 15 42 )42 TRUE, CompTRUE is monotonically related to n; (cf. Taylor
eHfa 82 71 203 )175
1978, p. 15; for empirical results). In order to compare the
behaviour of this measure to the supposedly best measure
STRUE = 300 n = 100 n = 500 n = 1000 n = 2000
in our comparison, we calculated eHbc for the same data.
Figure 2 shows that Fishers a yields a relatively constant
Sobs )765 )403 )239 )168
Sest )414 )32 19 )16 value over a large range of sample completeness (with a
H )195 )57 )30 )17 slight negative trend), but starts to drop increasingly at a
eH )632 )254 )143 )80 completeness c. >08. eHbc, on the other hand, is positively
Hbc )39 )04 01 00 related to completeness c. <07 (as indicated in Fig. 1), but
eHbc )172 )21 04 02
produced constant values for sample completeness above
Hfa 23 12 )06 04
eHfa 143 65 )32 20 that level.

Good measures have SME close to zero (no bias). Note that large
SME of Fishers a were not reported because they are meaning- Discussion
less as true error estimates (see main text).
For a comprehensive understanding of biodiversity, including
its importance in conservation and ecosystem management, it
high completeness (Spearmans rank correlations, N = 16, is important that erroneous assessments are avoided along the
P < 001: R = 067 for Sest, R > 098 for Sobs, H and eH). whole chain of evidence from choice of taxon, sampling site
These measures are also signicantly related to sample size and sampling technique, to assurance of quality in taxonomy
(even though STRUE vary) at R > 058. However, no relation- (Bortolus 2008), to an unbiased measurement of diversity and
ship was found for Hbc and eHbc (|R| < 05), while Hfa and a sound interpretation of what can be inferred from it. Our
eHfa are negatively related to completeness (R < )083, comparison has been strictly limited to the question of under-
P < 001). Sest, Hfa and eHfa are the only measures where we sampling biases in measuring alpha diversity, whereas other
observed (signicant) positive bias, i.e. overestimation of true properties of diversity measures may also be relevant to judge
diversity. their usefulness in relation to the research question at hand.

 2010 The Authors. Journal compilation  2010 British Ecological Society, Methods in Ecology and Evolution, 1, 3844
42 J. Beck & W. Schwanghart

and, not surprisingly, also in the eective number of species

(eH). Measures designed to reduce this bias, such as estimating
species richness (following the framework of Brose & Martinez
2004), and Chao & Shens (2003) bias correction for Shannons
entropy, were corroborated to have only a minimum of bias (if
any) at sample completeness c. >05 (i.e. if at least half of the
species were sampled). Furthermore, for the rst time to our
knowledge, we show that eective number of species calcu-
lated from bias-controlled entropy (eHbc) provides an unbi-
ased measure above this level of sample completeness. This
encourages, in combination with other preferential properties
(e.g. Jost 2006, 2007, 2009), the use of this measure in biodiver-
sity studies.
The low to intermediate bias of the simple estimates of
Hfa and eHfa, particularly at low to intermediate com-
Fig. 2. Fishers a (FA) and bias-controlled eective number of spe- pleteness, indirectly support the reliability of a (despite
cies (eHbc) for dierent numbers of individuals (n) sampled from the using a log-normal, not a logarithmic series, as underlying
same community (200 species; results for 50, 100 and 300 species look
SAD) at completeness well below 1, but with the availabil-
similar; not shown). Mean (grey and dashed lines respectively; this is
approximately the range of 95% of sample data) over 100 replicates ity of bias-controlled Shannons entropy there may be no
are shown, and robust locally weighted regressions were tted to need to use this measure except if very low completeness is
mean and 2 SDs to illustrate relevant patterns. Completeness suspected. In such cases, eHfa may provide a useful sec-
values (CompTRUE) are also means over 100 runs. Note that absolute ond opinion to eHbc.
value dierence between FA and eHbc are irrelevant to this
As pointed out in the Introduction, we cannot subject
Fishers a to the same rigour of comparison with true
values because these cannot, by denition, be calculated
under the simplifying assumption that a local community
Choosing measures of diversity, as well as other quantitative contains more than one individual even of the rarest spe-
metrics in ecology, must be guided by both the information cies. Simulations in Fig. 2 show that already before
required and the suitability of the metric to the available data. approaching full sample completeness, a values begin to
Various authors have pointed out that dierent measures actu- loose their stability displayed at low levels of completeness.
ally refer to dierent denitions of what we mean by diversity However, even in very large sampling programmes (e.g.
(e.g. Hurlbert 1971; May 1975; Southwood & Henderson Woiwod & Harrington 1994; Novotny & Basset 2000;
2000; Magurran 2004), and even more so if functional and Plotkin et al. 2000; Volkov et al. 2007) such data have not
phylogenetic aspects or the nonquantitative, colloquial mean- been found empirically, and the spatially structured nature
ings of the term are included (e.g. Purvis & Hector 2000). Vari- of real ecological communities (i.e. migration of individuals
ation in the diversity rank order of communities may be simply between neighbouring communities; Leibold et al. 2004)
a consequence of this. may indeed make our simulation unrealistic in this respect.
Concentrating on those measures relating to a character- Full sample completeness (i.e. 1 or anywhere near) is cer-
ization of the SADs (i.e. evenness), some authors con- tainly not likely in those systems where Fishers a is com-
cluded that indices that are mostly aected by species of monly applied, i.e. tropical invertebrate studies. Figure 2
medium abundance (such as Fishers a) are preferential conrms the stability of Fishers a through a range of
over those aected mostly by common species (e.g. Shan- incomplete sampling, and we found, upon visual inspec-
nons entropy) as they tend to produce stable values in tion, that value stability is equal or higher at low levels of
repeated sampling of the same community, but high completeness (i.e. <0507) that those of eHbc. Thus,
discrimination between dierent communities (Kempton & while our comparison cannot conrm the unbiased
Taylor 1974; Taylor 1978; Kempton 1979; using empirical character of Fishers a for technical reasons, we can
data), and many studies published since found good dis- neither reject it as long as we assume that samples are
crimination of site diversities by this index. Beck & Chey clearly incomplete.
(2008, p. 1455) reported that in their empirical data Fish-
ers a were not closely related to sample size, whereas this
was the case for other diversity measures such as Sobs and
several species richness estimators. Such dependency could We conclude from our results that the eective number of
be indication for undersampling bias in the latter (cf. Tay- species based on bias-controlled Shannons entropy (eHbc;
lor 1978), but may, theoretically, also be a true property of Fig. 1) is the most suitable measures of diversity if undersam-
the ecosystems. pling is suspected. This is particularly true when sample
Our comparison conrmed the (well known) undersampling completeness is above 05. Estimated species richness (Sest)
bias in observed species richness and Shannons entropy (H), was also found reliable above that threshold, but it exhibited
 2010 The Authors. Journal compilation  2010 British Ecological Society, Methods in Ecology and Evolution, 1, 3844
Measuring diversity from incomplete inventories 43

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