ANRV397-EN55-22 ARI 10 November 2009 11:17

Integrative Taxonomy:
A Multisource Approach
ANNUAL
REVIEWS Further to Exploring Biodiversity
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including:
Birgit C. Schlick-Steiner,1 Florian M. Steiner,1
• Other articles in this volume Bernhard Seifert,2 Christian Stauffer,3
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• Our comprehensive search 1

Institute of Ecology, University of Innsbruck, 6020 Austria;
email: Birgit.Schlick-Steiner@uibk.ac.at; Florian.M.Steiner@uibk.ac.at
2
Senckenberg Museum für Naturkunde Görlitz, 02806 Görlitz, Germany;
email: Bernhard.Seifert@senckenberg.de
3
Institute of Forest Entomology, Forest Pathology and Forest Protection, BOKU,
University of Natural Resources and Applied Life Sciences, 1190 Vienna, Austria;
email: Christian.Stauffer@boku.ac.at
4
Institute of Zoology, BOKU, University of Natural Resources and Applied Life Sciences,
1180 Vienna, Austria; email: Erhard.Christian@boku.ac.at
5
School of Marine and Tropical Biology, James Cook University, Townsville,
Queensland 4811, Australia; email: Ross.Crozier@jcu.edu.au

Annu. Rev. Entomol. 2010. 55:421–38 Key Words

First published online as a Review in Advance on
September 8, 2009
The Annual Review of Entomology is online at
ento.annualreviews.org
complementarity of disciplines, species delimitation hypotheses,
resolution of disagreement, procedural protocol, catalysis of
evolutionary biology

This article’s doi: Abstract

10.1146/annurev-ento-112408-085432
Copyright  c 2010 by Annual Reviews.
All rights reserved
0066-4170/10/0107-0421$20.00
Good alpha taxonomy is central to biology. On the basis of a survey of
arthropod studies that used multiple disciplines for species delimitation,
we evaluated the performance of single disciplines. All included disci-
plines had a considerable failure rate. Rigor in species delimitation can
thus be increased when several disciplines chosen for complementarity
are used. We present a flexible procedure and stopping rule for inte-
grative taxonomy that uses the information from different disciplines
separately. Disagreement among disciplines over the number and de-
marcation of species is resolved by elucidating and invoking evolution-
ary explanations for disagreement. With the identification of further
promising study organisms and of new questions for in-depth analysis,
evolutionary biology should profit from integrative taxonomy. An im-
portant rationale is clarity in researcher bias in the decision-making pro-
cess. The success of integrative taxonomy will further increase through
methodological progress, taxonomic training of evolutionary biologists,
and balanced resource allocation.

421
 ANRV397-EN55-22 ARI 10 November 2009 11:17

INTRODUCTION Three imperatives drive integrative taxon-

omy. First, morphological methods fail in some
The Task, Relevance, and State cases, absolutely necessitating the application
Taxonomy: science of of Alpha Taxonomy
characterizing, of other approaches, and, second, even where
classifying, and Taxonomy is central to exploring and under- morphology can succeed in delimiting species,
naming taxa standing biodiversity. It is the science of char- other approaches can assist significantly and
Species category: acterizing, classifying, and naming taxa. Alpha speed the process (5, 8, 9, 12, 15, 25, 32–34,
level in taxonomic taxonomy deals with the species category, beta 38, 44, 48, 49, 51, 55–60, 63, 76). Third, the use
hierarchy, considered of several disciplines helps taxonomy go beyond
taxonomy with higher categories. To most biol-
by most to reflect
ogists, the species category is unique in the taxo- the naming of species to understanding the pro-
actual evolving groups
nomic hierarchy in that it has claims to objective cesses bringing them about. This is especially
Species delimitation:
apparent in cases of disagreement among disci-
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building explicit reality (1, 10, 57). Delimiting species—using

hypotheses as to which empirical data to build explicit hypotheses as to plines, in that such cases are resolved by drawing
on evolutionary biology (15, 18, 19, 44, 48, 49,
Annu. Rev. Entomol. 2010.55:421-438. Downloaded from www.annualreviews.org

specimens constitute which specimens belong to particular species

particular species taxa taxa (57)—is a practical application of such a
Species concept: view. Any species delimitation depends on a the-
theoretical definition oretical idea of what species are, a species con-
of the entity species;
cept. Whichever of the more than 20 species
over 20 concepts
concepts (23) is chosen, a delimitation criterion
available
appropriate to that concept is required, and the
Delimitation
concept used will influence the choice, analysis,
criterion: empirical
method for translating and interpretation of data (2, 32).
a species concept into Alpha taxonomy is central to biology:
the logic of data Species are the basic units of many fields
analysis and
(2, 49, 57) and the species name provides
interpretation
the link to the knowledge about an organ-
Hypothesis-driven
ism. The need for good alpha taxonomy is
approach: test of
further increased by the biodiversity crisis
prior hypotheses with
data (37, 64, 65), both for assisting conservation
programs and documenting diversity before
Discovery approach:
data analysis without it is lost. However, taxonomy’s resources—
prior hypotheses; including manpower—have been declining
hypotheses follow steadily, both in absolute numbers and in pro-
from data
portion to the rest of biology, and this decline
has strongly affected the field’s vitality and ac-
centuated the taxonomic impediment (3, 6, 54,
61, 74).
Integrative Taxonomy
A multisource approach that takes advantage of
complementarity among disciplines, i.e., fields
of study, has been called combined (38), mul-
tidisciplinary (55), multidimensional (76), col-
laborative (18), or integrative (12, 15, 51, 62,
73) taxonomy. We use the term integrative tax-
onomy and focus on species.
51, 55–59).
Integrative taxonomy does not replace tra-
ditional taxonomy. Rather, it compresses the
traditional but slow taxonomic routine of vis-
iting a taxonomic problem repeatedly (1, 3,
24, 65, 66) into one procedure by coordinat-
ing the findings of different disciplines under
the procedure. By doing so, integrative taxon-
omy improves rigor. More rigorous delimita-
tion by integrative taxonomy has yielded a bet-
ter biodiversity inventory, by both increasing
and decreasing species numbers. Increases have
been due especially to the discovery of cryp-
tic species, with prominent examples including
understudied marine (5, 33) and tropical ter-
restrial taxa (5, 7, 9, 38, 48, 76) but extending
to well-studied biomes (49, 55, 56, 60). Species
numbers have decreased through demonstra-
tion of conspecificity of nominal species, thus
often ending longstanding taxonomic disputes
(34, 45, 58).
WORKING TERMINOLOGY
A delimitation hypothesis is one about the num-
ber and demarcation of the species in the set
of specimens. We recognize two approaches
to species delimitation and adapt terms from
systems biology (29) to term these the dis-
covery and hypothesis-driven approaches. In
the discovery approach, specimens are an-
alyzed without prior hypotheses about the
species present—including their number—and

422 Schlick-Steiner et al.

 ANRV397-EN55-22 ARI 10 November 2009 11:17

hypotheses about the species present follow SURVEY OF ARTHROPOD

from the data (specimens). An example would LITERATURE
be to subject population genetics data to clus-
We used the ISI Web of KnowledgeSM to sur-
ter analysis (16). In the hypothesis-driven ap-
vey published studies from 48 journals, from
proach, the set of specimens is used to test prior
1977 to 2008 (for the journals and search terms
hypotheses about the existence of species, as
used in the ISI search, and for the complete
when a species delimitation hypothesized from Supplemental Material
list of studies selected, see the Supplemen-
morphology is tested using population genetics
tal Material (follow the Supplemental Mate-
data.
rial link from the Annual Reviews home page
By discipline we understand a field of study,
at http://www.annualreviews). One hundred
such as the study of nuclear DNA, ecology, or
eighty-four studies were selected that reported
morphology; frequently, we refer to a discipline
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arthropod diversity at the species level using

in a short form, e.g., nuclear DNA. A disci-
more than one discipline, and we analyzed the
pline is termed conclusive for a particular set
Annu. Rev. Entomol. 2010.55:421-438. Downloaded from www.annualreviews.org

data from the various disciplines separately; if

of specimens when its delimitation hypothesis
a taxonomic problem was treated in more than
is significant, and when more than one data set
one study, only the latest study was used if it
from the discipline has been analyzed (such as
reanalyzed the same data presented earlier.
morphological data for males and females), the
The arthropod classes covered were Insecta
same hypothesis is significant for all of them.
(n = 141 studies), Arachnida (n = 20), Mala-
The delimitation hypothesis is significant when
costraca (n = 13), Maxillopoda (n = 5), Bran-
more than 95% of the specimens fit it (a prag-
chiopoda (n = 4), Chilopoda (n = 1), and
matic level suggested; 72), in accord with the
Ostracoda (n = 1). The genera most ana-
significance cut-off specified for the data analy-
lyzed were Drosophila (n = 7 studies), Anopheles
sis method. A discipline is inconclusive for a set
(n = 6), Encarsia (n = 5), Chrysoperla (n = 4),
of specimens when its delimitation hypothesis is
and Heliconius (n = 3). About 3010 species were
not significant or when different data sets from
analyzed, the uncertainty stemming from unre-
the same discipline significantly support differ-
solved delimitation; we then adopted the con-
ent hypotheses.
servative view according to the latest author.
More than one discipline can be applied to
In Table 1, we classified the methods ap-
the same taxonomic problem, in which case
plied into 11 disciplines in order of frequency
agreement, partial agreement, or total disagree-
of use: morphology (qualitative or quantitative
ment over the number and demarcation of
analyses), mitochondrial DNA (sequencing,
species will emerge among disciplines. In case of
fingerprinting), nuclear DNA (sequencing of
agreement, all specimens are placed into species
one or more loci, fingerprinting, genotyping),
in the same way by the disciplines applied. With
ecology (habitat; ecological niche; pathogen,
partial agreement, disciplines agree for some of
symbiont, host, or foodplant association),
the hypothesized species, but not for others.
enzymes, behavior (mating-related, social, or
With total disagreement, disciplines disagree
interspecific behavior), reproductive compat-
for all hypothesized species. Disagreement can
ibility, life history (spatiotemporal, physio-
be of different types: Disciplines can either dis-
logical, reproduction-related, or social traits),
agree over the number of species, or agree over
cytogenetics (karyology, DNA content), chem-
the number of species but disagree over the
istry (cuticular hydrocarbons, sex pheromones,
placement of specimens into species. Arriving
venoms), and whole genome scans (amplified
at a final delimitation hypothesis then involves
fragment length polymorphism, random
deciding which of the hypotheses supported by
amplification of polymorphic DNA). The
conclusive disciplines are plausible and which
number of disciplines ranged from two to eight
are implausible.
per study. Discovery (hypothesis building)

www.annualreviews.org • Integrative Taxonomy 423

 ANRV397-EN55-22 ARI 10 November 2009 11:17

Table 1 Performance of disciplines in the survey of arthropod literature

Species delimitation hypotheses
Delimitation Failure Performance
Disciplines Totala definitiveb ratec superior tod
Morphology 359 302 0.23 Ecology
Mitochondrial DNA 284 235 0.33 Ecology
Nuclear DNA 142 119 0.28 Ecology
Ecology 72 65 0.60
Enzymes 46 39 0.21 Ecology
Behavior 27 24 0.08 Ecology
Reproductive compatibility 25 22 0.23 –
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Life history 24 21 0.52 –

Cytogenetics 25 20 0.20 –
Annu. Rev. Entomol. 2010.55:421-438. Downloaded from www.annualreviews.org

Chemistry 11 9 0.22 –
Whole genome scans 9 8 0.38 –

a
Total number of delimitation hypotheses.
b
Number of delimitation hypotheses for sets of specimens for which delimitation was thought definitive.
c
Portion of failure scores among delimitation hypotheses for sets of specimens for which delimitation was thought
definitive; e.g., 68 of delimitation hypotheses by morphology for the 302 sets of specimens for which delimitation was
thought definitive failed.
d
Failure rate significantly lower than that of compared discipline (Fisher’s exact test, α = 0.05, Bonferroni-Holm adjusted).

and hypothesis-driven approaches (hypothesis each contributing discipline as either success or

testing) were taken, either alone or in various
combinations. In the case of iterative analyses in
a study, we considered the results from the pri-
mary and final analyses. For considering clades
in phylogenetic reconstructions as significantly
supported, we applied a cut-off value for node
support of >70 to bootstrapping results (26)
and >0.95 to posterior probabilities (28).
We extracted one delimitation hypothesis
per discipline for every set of specimens. The
number of sets of specimens per study was de-
termined by pairwise comparison of the results
of all disciplines. One set of specimens com-
prised all those hypothesized species over which
disciplines either agreed, or over which dis-
agreement of one particular type emerged for a
pairwise combination of disciplines. The num-
ber of delimitation hypotheses per study ranged
from 2 to 24. In total, 1024 delimitation hy-
potheses were extracted for 353 sets of speci-
mens (Table 1).
When an author considered delimitation as
definitive for a set of specimens (n = 296 sets
of specimens), we evaluated the performance of
failure. A discipline’s performance was scored
as a success when the delimitation hypothesis
it supported was identical to the definitive de-
limitation reached at the end of the study. A
discipline’s performance was scored as a failure
when it was inconclusive or when the delimita-
tion hypothesis supported by it differed signif-
icantly from the definitive delimitation, either
initially or on reanalysis.
PRINCIPAL OUTCOMES OF
USING MULTIPLE DISCIPLINES
Agreement among Disciplines
When multiple disciplines are used for analyz-
ing a taxonomic problem, the clearest result
is agreement among disciplines. In the survey,
such overall agreements emerged for 147 of
353 sets of specimens. Study authors considered
agreement as reason to regard a delimitation
hypothesis as plausible. Authors also explic-
itly or implicitly considered agreement among
disciplines as a stronger indication that the

424 Schlick-Steiner et al.

 ANRV397-EN55-22 ARI 10 November 2009 11:17
Table 2 Decision-making process in choosing three disciplines for primary exploration
Targeted contributionsa
Phenotypic information; link to Linnean nomenclature
Nuclear genetic information
Complementary information
a
One discipline per targeted contribution is chosen.
b
See section Primary Exploration.
Abbreviations: Mo, morphology; Nu, nuclear DNA, either sequencing or genotyping; Wh, whole genome scans;
En, enzymes; Be, behavior; Cy, cytogenetics; Ch, chemistry, either cuticular hydrocarbons or pheromones;
Mt, mitochondrial DNA; Re, reproductive compatibility; Ec, ecology; Li, life history.
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evolutionary pattern had indeed been discov-
ered than if data from only a single discipline
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had been analyzed (25).
The plausibility of a delimitation hypothesis
rises with the independence of the information
of the disciplines contributing to the finding.
Complete independence of different informa-
tion that relates to one and the same organism
is unachievable, considering that any given or-
ganism has a single history (25), but our un-
derstanding of the degree of independence is
incomplete. Integrative taxonomy has to oper-
ate with this uncertainty and assumptions from
general biology are useful (Table 2).
Of course, disciplines may agree but
nonetheless be incorrect about the species in
nature. For example, two disciplines may sup-
port the same two-species hypothesis, whereas
in fact only one species in nature is involved.
This problem holds for any taxonomy and re-
minds us that any species taxon, i.e., a taxo-
nomic construct assigned to the species cate-
gory, is a hypothesis and should not be seen
as true even if well-supported (47). This risk
cannot be avoided, but it is arguably lowered
the more the information from multiple disci-
plines is independent. In practical terms, agree-
ment means the link between a species taxon
and the evolving group, i.e., the species in na-
ture, is the closest that can be made from cur-
rent knowledge.
Disagreement among Disciplines
The application of multiple disciplines be-
comes more complicated when there is
Suggested order of considering disciplines
through answering Questions 1 to 4b
Mo
Nu → Wh → En
Be → Cy → Ch → Mt → Re → Ec → Li
disagreement among them. In the literature
survey, disagreements occurred for 206 of 353
sets of specimens. Given disagreement, one of
the delimitation hypotheses should be plausible
and the other(s) implausible. To identify the
plausible hypothesis is challenging, requiring
an evolutionary explanation for disagreement
(Table 3) (44, 51, 57, 71). Once an explanation
has been found, the conflicting delimitation
hypotheses can be qualified as plausible or
implausible (Table 3). We have noted that
when disciplines agree about the species
present, this conclusion can still be wrong. It
is also true that when there is disagreement
none of the disciplines may have inferred the
correct situation; thus, one might lead to the
conclusion of one species, another that there
are two, but in fact there are three in nature.
Disagreement can lead to new evolutionary
insights. It raises the number of promising
study organisms, without which evolutionary
biology will stagnate (75), and facilitates access
to a range of questions for in-depth analysis
(Table 3) that thus potentially lead to “in-
triguing insights” (19). Integrative taxonomy
profits through a reverse-flow effect: The
evolutionary explanations at hand for resolving
disagreements become more complete and
better founded. The large proportion of
disagreements in our literature survey sug-
gests that irregular evolutionary patterns and
processes that shape species might be more
common than we appreciate and may require Species taxon:
several disciplines to uncover.
taxonomic construct
assigned to species
In practical terms, the resolution of dis- category
agreement marks situations in which use of a
www.annualreviews.org • Integrative Taxonomy 425
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Table 3 Evolutionary explanations for disagreements among disciplines, detailed questions potentially resolvable, and operational priority of disciplines,
exemplified by morphology, nuclear DNA, and mitochondrial DNAa
ANRV397-EN55-22

Operational priority of disciplines, depending on the particular disagreement

ARI

Evolutionary Detailed questions potentially resolvable

explanation through the integrated data Mo Nub Mt Mo Nu Mt Mo Nu Mt
d

426
Recent speciation Allopatric? Parapatric? Peripatric? Sympatric? c    
Ecological? Allochronic? Mediated by
endosymbionts? Sexual selection?
Hybridization Recent? Ancient? Hybrid speciation?     
Reinforcement? Lack of selection against
10 November 2009

hybridization? Selection for hybridization?

Disruptive selection? Sexual selection?

Schlick-Steiner et al.
11:17

Mediated by endosymbionts? Paternal

leakage? Genome organization?
Intraspecific Sympatric? Geographic? Ecological?     
morphological Alternative reproduction strategies?
variation Phenotypic plasticity? Selection for
accelerated morphological evolution?
Disruptive selection?
Cryptic species, Morphological stasis? Convergent evolution? 
speciation not Parallel evolution? Sexual selection?
recent Stabilizing selection? Mimicry?
Substitution Genome organization?  
saturation
Incomplete lineage Recent vicariance? Balancing selection?    
sorting Peripatric speciation? Population sizes?
Selective sweep Genome organization? Mediated by  
endosymbionts? Population sizes?
Mt substitutions Population sizes? 
accelerated by
endosymbionts
Pseudogenes Genome organization?  

a
Based on the arthropod literature survey. Each row illustrates up to three scenarios based on morphology (Mo), nuclear (Nu) genes, and mitochondrial (Mt) genes. For each scenario
consideration of the evolutionary processes listed leads to rejection of the hypotheses for the disciplines with open boxes; checked boxes indicate disciplines whose hypotheses remain plausible.
b
Any nuclear gene which resolves at species level but has a lower substitution rate than mitochondrial DNA.
c
After invoking the evolutionary explanation for disagreement, the hypothesis supported by the discipline is qualified as implausible.
d
After invoking an evolutionary explanation for disagreement, the hypothesis supported by the discipline is qualified as plausible and the discipline is given priority operationally over disciplines
supporting an implausible hypothesis(es).
 ANRV397-EN55-22 ARI 10 November 2009 11:17
single discipline would potentially have failed,
by yielding an implausible hypothesis. The next
practical question is whether there is any silver-
bullet discipline for taxonomy, i.e., one that
rarely results in implausible hypotheses, the ap-
plication of which would render application of
other disciplines redundant.
EVALUATION OF THE
PERFORMANCE OF
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SINGLE DISCIPLINES
The failure rates of the 11 disciplines in the
Annu. Rev. Entomol. 2010.55:421-438. Downloaded from www.annualreviews.org
literature surveyed ranged from 0.08 to 0.60;
5 disciplines have statistically significantly
better performance when compared with
ecology (Table 1). Conclusions from these
failure rates should take account of additional
considerations. First, improved data genera-
tion and analysis methods might decrease a
discipline’s failure rate, such as for ecological
niche modeling in ecology (48, 49, 60) or
geometric morphometrics in morphology (42).
Second, more rigor in applying a consistent
approach might decrease a discipline’s failure
rate. Third, the failure rate may not perfectly
reflect the performance of a discipline because
it was not consistent across studies, whether
or not reanalysis of data from a discipline that
had been inconclusive or that had resulted in
an implausible delimitation hypothesis was
attempted. Careful reanalysis can be successful,
as shown for morphology (21, 41, 42, 56).
Fourth, if a discipline is sufficiently decisive,
its hypothesis might be plausible even if it
disagreed with one supported by many other
disciplines, a possibility requiring a comparison
of statistical support across disciplines, imprac-
tical at present. Fifth, if a discipline is generally
deployed for particularly difficult problems,
its failure rate may be inflated. Sixth, the true
failure rate may be higher, as when disciplines
agree on an incorrect solution. The first and
second considerations indicate that the picture
could change in the future, but the observed
failure rates reflect current practice. The other
considerations all indicate the superiority of
using several disciplines for a problem because
only then can incongruence be detected.
In particular, two sources of information
have been much contrasted: morphology and
genetics. Indeed, genetic methods have dra-
matically improved taxonomic insight (5, 25).
However, as Hillis (25) noted, “collaborations
between morphological and molecular system-
atists often produce analyses that transcend the
usefulness of separate studies.” The failure rates
of morphology and the various genetic disci-
plines in our literature survey (Table 1) confirm
that neither should be used as a single informa-
tion source. This conclusion agrees with recent
assertions that genetics may distort taxonomy
when other data are neglected (15, 36, 40, 44,
65, 67). We conclude that there is no single
silver-bullet discipline and that integrated use
of several disciplines is needed to guard against
single-discipline failure.
A PROTOCOL FOR
INTEGRATIVE TAXONOMY
Taxonomy is a decision-making process, and
more decisions are necessary when more than
one discipline is used. Our survey of the arthro-
pod literature found inconsistencies in how de-
cisions were made, and the justification for
how decisions were made was often vague, as
noted elsewhere (8, 70). We used conclusive el-
ements of the studies surveyed and present a
general protocol for integrative taxonomy. Nar-
row guidelines may not be universally applica-
ble (57, 62), and hence the protocol does not in-
clude rules other than taking decision-making
steps in a particular order. Figure 1 as well
as the Worked Examples (follow the Supple- Supplemental Material
mental Material link from the Annual Reviews
home page at http://www.annualreviews.org)
illustrate how the protocol is used. The exam-
ples are hypothetical in that in each of them a
range of situations from multiple separate stud-
ies is projected onto imaginary species, but they
are realistic with regard to the general natural
history of the insects used.
The overarching idea of the protocol is that
information from different sources should first
www.annualreviews.org • Integrative Taxonomy 427
 ANRV397-EN55-22 ARI 10 November 2009 11:17

Researcher bias in decision making

Choice of study system
No researcher bias in decision making

Choice of: three disciplines including Choice of: one additional discipline
data generation methods including data generation method
+ species concept + species concept for all disciplines
+ delimitation criteria + delimitation criteria for all disciplines

Sequential exploration
Primary exploration

+ data analysis methods + data analysis methods

Further samples available?**

Further samples available?**

Data generation, Data generation,
Data generation, three disciplines
additional discipline all disciplines
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Discipline by discipline data analysis Discipline by discipline data analysis

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+ delimitation hypotheses elaboration + delimitation hypotheses elaboration

No Yes
No Yes

Inconclusive Conclusive Conclusive Inconclusive

discipline(s) discipline(s) discipline(s) discipline(s)

** Applicable only if inconclusiveness is due to

More than one One or none lack of significance of delimitation hypothesis

Further discipline(s) available?

Agreement Partial agreement; Disagreement; potential
conclusive disciplines

= plausible hypothesis set-of-specimens splitting set-of-specimens splitting

Comparison of

No Yes
No evolutionary
Evolutionary explanation Evolutionary explanation
explanation

Priority of discipline(s) with plausible

hypothesis over discipline(s) with
implausible hypothesis/es

Choice of data analysis method(s)

for hypothesis-driven approach
characterization
Integrated

Reanalysis of data from inconclusive

discipline(s) and/or discipline(s)
supporting implausible hypotheses

Characterization by disciplines supporting plausible

hypothesis either initially or on reanalysis
If applicable

Nomenclatural consequence(s) No delimitation

Figure 1
Protocol for integrative taxonomy.

428 Schlick-Steiner et al.

 ANRV397-EN55-22 ARI 10 November 2009 11:17
be used separately and then integrated. Thus,
we did not consider the total evidence ap-
proach that submits data from different disci-
plines to combined analysis (31), although it
is sometimes used in species delimitation (68).
However, the approach either does not explore
whether data from different sources agree or
disagree, or does so but nevertheless uses dis-
agreeing data for elaborating one hypothesis.
Choice of Study System
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Using several disciplines rather than just one
costs more; hence problems for integrative tax-
Annu. Rev. Entomol. 2010.55:421-438. Downloaded from www.annualreviews.org
onomy should be carefully chosen. Examples
include (a) longstanding taxonomic disputes,
(b) ambiguous delimitation in morphology-
based revisionary work, (c) pronounced life-
history variability of or broad geographic or
ecological space occupied by nominal species,
(d ) biodiversity hotspots, and (e) outstanding
importance of organisms to progress in other
fields.
Primary Exploration
The primary exploration consists of several
steps that are run through in turn.
Choice of disciplines. We recommend
choosing three disciplines because, given
the mean failure rate of single disciplines of
Table 1, 0.30, the combination of two disci-
plines should result in an average error rate of
0.09, and the combination of three disciplines
in an average error rate of 0.027. These average
error rates represent those instances when
disciplines agree but nonetheless are incorrect
about the species in nature. On the one hand,
the estimates are overly pessimistic in that they
consider the case of all disciplines settling on
the same wrong result out of the many possible
ones; on the other hand, the estimates are
overly optimistic in that they do not account
for those instances when disciplines disagree
and none of them is correct about the species
in nature; neither inaccuracy can be quantified.
We suggest that the approximate error rate of
0.027 represents an acceptable compromise
between practical constraints and power of
resolution.
The above consideration rests on indepen-
dence of the disciplines chosen, and the actual
but unknown error rate will be higher when
they are not independent. Thus, we suggest
choosing one discipline each for targeting phe-
notypic, nuclear genetic, and complementary
information (Table 2). Our suggestion to al-
ways choose morphology for obtaining pheno-
typic information flows from the ease of obtain-
ing morphological information, compatibility
with past taxonomic practice, the need to assess
morphology as a discriminator in any case and,
for at least some years to come, better access for
most people to the biological knowledge tied to
names. Both genetics and morphology should
be included in the first set of disciplines because,
on the one hand, species are genetic and not
morphological entities, and on the other hand,
morphological identification is generally much
easier if it is possible at all.
The decision-making process we suggest for
choosing the other two disciplines allows for
the flexibility needed across taxa. On the basis
of the results in Table 1 and general method-
ological considerations (4, 19, 21, 35, 39, 40, 42,
48–52, 57, 60), we suggest a particular order of
considering disciplines within targeted contri-
butions (Table 2). For a discipline to be chosen,
four questions need to be answered positively;
if the list of disciplines for any of the three tar-
geted contributions becomes exhausted without
positive answers, the problem cannot be solved
under the protocol. Question 1: Is the disci-
pline actually or potentially established for the
organism? Question 2: Has the discipline suc-
cessfully resolved species-level problems in re-
lated organisms? Question 3: Are the existing
samples adequate (type of preservation, living
organisms if necessary) or, if not, can new sam-
ples be collected? Question 4: Are the necessary
resources available?
The choice of disciplines then entails choos-
ing the best mode of generating data for
each. Characters should be sought that delimit
species unambiguously. Discrete characters
www.annualreviews.org • Integrative Taxonomy 429
 ANRV397-EN55-22
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ARI 10 November 2009 11:17
have better ease of use but therefore are likely
to have already been studied, so that new quan-
titative characters will often be needed for per-
sistent taxonomic problems, as noted for mor-
phology (56, 69, 72). Reasonably high numbers
of characters varying in state between speci-
mens should be sought so that a subset can be
selected if reanalysis is needed.
Choice of species concept. The species con-
cept must be applicable to data from the three
disciplines chosen. Different species concepts
focus on different aspects of species. No species
concept is perfect when applied to nature, i.e.,
every concept will in some instances lead to am-
biguities in species delimitation (23, 24), but to
increase the comparability of species taxa (66),
it would be desirable that all taxonomists agree
on one concept. Agreement on one concept is
unrealistic, though, given the contentions about
species concepts (10, 23). A less strict version of
standardization may arise from the notion that
all species concepts have a common core (23).
Thus, delimitation hypotheses can be built un-
der one primary, unified species concept lacking
defined properties (13) with the justification of
the delimitation based on any of the properties
of species that other species concepts consider.
Choice of delimitation criteria. Delimita-
tion criteria are empirical methods (57) used
for translating species concepts into the logic
of data analysis and interpretation and can dif-
fer among disciplines; for example, a criterion
under the genotypic cluster concept is the oc-
currence of a lack of heterozygotes in sym-
patric populations (13). A delimitation crite-
rion thus needs to be compatible with at least
one of the disciplines and the species concept
chosen. Intuitive criteria are often used in the
sense of verbal postanalysis arguments without
explicit tests (8, our survey), but explicit crite-
ria are needed for reproducibility and rigor (8,
57). Sites & Marshall (57) reviewed 12 delimi-
tation methods, and other formal criteria have
been presented since, for example, for genetic
(14, 46) and ecological data (48, 49, 60). Under
many species concepts there are no delimitation
430 Schlick-Steiner et al.
criteria for various disciplines. However, the
unified species concept (13) is sufficiently ro-
bust to accommodate any delimitation crite-
rion; thus, using a phenotypic distinctness cri-
terion, this concept readily handles discrete as
well as continuous characters (43, 56).
Some criteria can be applied only in a
hypothesis-driven approach (hypothesis test-
ing), meaning that the choice of taking a discov-
ery (hypothesis building) or a hypothesis-driven
approach restricts the criteria applicable. There
is no alternative to the discovery approach when
there is no adequate prior hypothesis, but this
approach is also appropriate if the existing hy-
potheses are inadequate. Given that it may not
be knowable whether any hypotheses are cor-
rect under the hypothesis-driven approach, the
discovery approach may be more appropriate in
general because it has the potential to use the in-
formation available when inferring the number
and demarcation of species present more fully
than does the hypothesis-driven approach (43,
63). An erroneous prior hypothesis might ap-
pear to be corroborated under the hypothesis-
driven approach (because this approach chooses
between hypotheses), even if the discipline used
for hypothesis testing would delimit the actual
species in nature when analyzed in a discovery
approach. We thus doubt the wisdom of sug-
gestions to use one discipline for building a hy-
pothesis (e.g., morphology, 12; DNA, 63) and
the others for testing it, and, instead, suggest
applying the discovery approach whenever fea-
sible for a discipline.
Choice of data analysis methods. A data
analysis method needs to be compatible with
a delimitation criterion chosen. We focus on
discovery (hypothesis building) methods. Such
methods are standard procedure for some dis-
ciplines, such as in DNA-based phylogenetic
reconstruction (17), and are also available for
population genetics analysis (16). For all other
disciplines, classical statistics offers a range of
ordination methods (53) as does machine learn-
ing (20), albeit the latter has as yet rarely been
used in species delimitation (59).
 ANRV397-EN55-22 ARI 10 November 2009 11:17
Data generation. The set of specimens for the
disciplines used should be the same; that is, the
same specimens should be used throughout as
far as possible. Otherwise, disagreements may
be apparent rather than real or discrepancies
may not be discovered.
Hypothesis elaboration. Using the delimita-
tion criteria and the data analysis methods cho-
sen, delimitation hypotheses are built (discov-
ery approach) or tested (hypothesis-driven ap-
proach) for all three disciplines separately.
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Assessment of conclusiveness of disciplines.
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To reduce the error rate of the procedure, it is
desirable to minimize the number of inconclu-
sive disciplines. A discipline that is inconclusive
owing to nonsignificance of a delimitation
hypothesis may become conclusive if further
specimens are sampled; these specimens
then should also be examined for the other
disciplines (Worked Example 2). A discipline
that stays inconclusive is considered again in
the integrated characterization. If two or all
disciplines stay inconclusive, the procedure
continues with sequential exploration.
Comparison of Conclusive Disciplines
The delimitation hypotheses from all con-
clusive disciplines are compared. In case of
agreement (Worked Example 1), the delimi-
tation hypothesis is considered plausible, with
the number of conclusive disciplines determin-
ing the error rate. Disciplines that resulted in
the plausible hypothesis are considered again
in the integrated characterization.
With partial agreement, the part of the set of
specimens for which all disciplines agree is split
operationally from the part with disagreement
(Worked Example 3). For the part with agree-
ment the procedure continues as above. The
following pertains to the disagreement part of
partial agreements and to total disagreement:
No splitting of the set of specimens is neces-
sary (Worked Example 2) if, for the whole set
of specimens from the perspective of one of
any two disciplines compared, there is only one
of the following: (a) lower number of species,
(b) higher number of species, (c) same number
of species but different placement of specimens
into species, or (d ) agreement (disagreement
between two disciplines can be accompanied by
a further discipline agreeing with one of them,
Worked Examples 2–4). Splitting is necessary
(Worked Example 4) if, from the perspective
of one of any two disciplines compared, any
combination of a through c occurs for differ-
ent parts of the set of specimens. Splitting then
aims at sets of specimens with only one type of
disagreement, and for each of them the proto-
col continues separately.
For sets of specimens with disagreement, a
resolution is sought. Resolution cannot be ob-
tained by a simple tally of how many disciplines
support each delimitation hypothesis. Rather,
the evolutionary processes known for each
discipline are examined to see if any of these
processes could explain why the delimitation
hypothesis from a discipline disagrees with that
from another discipline (see Table 3 for exam-
ples). A few quantitative methods are available
for this step, including one to test convergence
in morphology (71) and one to distinguish
between hybridization and incomplete lineage
sorting in sequence data for large numbers of
loci (27). If an evolutionary explanation can be
found, hypotheses are qualified as plausible or
implausible. Disciplines that support the plau-
sible delimitation hypothesis are given priority
operationally over disciplines that support im-
plausible ones. If no evolutionary explanation
Supplemental Material
can be found, the procedure continues with
sequential exploration (Worked Example 3).
Sequential Exploration
Once sequential exploration has become nec-
essary, the procedure follows the rationale of
sequential analysis in statistics (22), where the
final number of observations is not fixed in ad-
vance but where observations are added until
a predefined stopping rule applies. Here, the
stopping rule is resolution of disagreement or
exhaustion of the number of disciplines appli-
cable or affordable, whichever applies first.
www.annualreviews.org • Integrative Taxonomy 431
 ANRV397-EN55-22 ARI 10 November 2009 11:17
One additional discipline is chosen, as inde-
pendent from the other disciplines in the infor-
mation revealed as possible. Species concept,
Nomenclature:
system of scientific delimitation criteria, and data analysis meth-
names for taxa and the ods are chosen. Data are generated by the addi-
provisions for the tional discipline, aiming at sample congruence
formation, treatment, across all disciplines. Discipline by discipline,
and use of those names
data analysis follows for hypothesis elabora-
tion. Conclusiveness of disciplines is assessed.
In case of inconclusiveness due to nonsignifi-
cance of a delimitation hypothesis, additional
samples are analyzed, if available, by all dis-
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ciplines. Disciplines that stay inconclusive are
considered again in the integrated characteri-
Annu. Rev. Entomol. 2010.55:421-438. Downloaded from www.annualreviews.org
zation. If there is more than one conclusive dis-
cipline, their hypotheses are compared. If no
evolutionary explanation for the disagreement
can be found, or if only one or no disciplines
Supplemental Material are conclusive, the sequential exploration starts
over again (Worked Example 3).
Integrated Characterization
When the three disciplines of the primary ex-
ploration are conclusive and their hypotheses
plausible, the information from all disciplines
is presented in such a way that it best character-
izes the species. When disciplines from primary
and/or sequential exploration do not support
the plausible delimitation hypothesis (inconclu-
sive or implausible hypotheses), data analysis
methods are chosen for hypothesis-driven re-
analysis. Reanalysis is performed to see if the
plausible hypothesis accords with the data of
those disciplines (at least as well as the implau-
sible hypothesis if a discipline did not fail be-
cause of inconclusiveness). Reanalysis can thus
reveal that all or some of the data from a disci-
pline which failed in the first place can never-
theless be used for the integrated characteriza-
tion (Worked Examples 2–4).
Methods used here include classification
methods, for example from classical statistics
or machine learning (20, 53), ecological niche
modeling (48, 49, 60), and methods to search for
characters that mediate information in accord
with the plausible delimitation hypothesis, such
as techniques to estimate and test association
432 Schlick-Steiner et al.
of characters (53). Classification methods can
be used for the latter purpose as well, by ex-
ploratory omission of some of the characters,
as through an exhaustive process using combi-
nation procedures to identify the optimal com-
bination of characters for discrimination (41).
In morphology, correction for allometry is pos-
sible at this stage (21, 56), in combination with
any of the methods described above.
If any characters from an inconclusive dis-
cipline, or even one that led to an implausi-
ble hypothesis, support the ultimate plausible
hypothesis, then they are available for charac-
terizing species. If no characters of a discipline
support the plausible hypothesis, the discipline
is not used further (Worked Examples 3–4).
Nomenclatural Consequences
In taxonomy, any species delimitation and
characterization is available, and thus open to
further scrutiny, only if it is associated with a
formal name published in accord with nomen-
clature (30), such publications having “eternal
life” (6). Thus, if the analyses we propose reveal
the need for nomenclatural changes, these must
be published. This activity is straightforward
if current nomenclature is oversplit, i.e., when
a nominal species needs to be sunk into syn-
onymy; however, if nomenclature is undersplit,
analysis of type specimens is necessary. In any
case, adherence to standard nomenclatural
rules (30) is essential. The findings could reveal
that an available junior synonym can be rescued
from synonymy or that the species delimited
needs to be described as a new species. When it
is possible to include morphology in the inte-
grated characterization, there is a morphologi-
cal system at hand for type analysis; otherwise,
in many cases, but certainly not all, molecular
information can be obtained from types (11).
No Delimitation
Cases may remain where the supply of dis-
ciplines is exhausted without delimitation, al-
though we are not aware of any. This would
not be a negative result in the sense of failing
 ANRV397-EN55-22 ARI 10 November 2009 11:17
to contribute to science. Rather, these would be
cases where the nature of the evolving groups
is poorly understood and would demarcate the
limits of present integrative taxonomy. Such
cases should be documented carefully. In-depth
analysis by evolutionary biology could reveal a
hitherto unrecognized evolutionary pattern or
process which would then become available as
an evolutionary explanation for disagreements
in general.
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EXAMPLE
For an illustration of how the protocol is used,
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consider the following hypothetical situation
(see Worked Example 2).
 Choice of study system: Criterion (a).
There is a longstanding dispute whether
the ant species Novomyrmex secundus is in-
deed a species separate from N. primus.
 Primary exploration: Morphology, nu-
clear DNA, and chemistry are chosen
as disciplines, with traditional morpho-
metrics (10 continuous characters), mi-
crosatellite genotyping (10 loci), and
analysis of cuticular hydrocarbons by gas
chromatography coupled with mass spec-
trometry as modes of generating data.
The unified species concept (13) is cho-
sen, and the delimitation criteria to be
applied are phenotypic distinctness for
morphology and chemistry, and repro-
ductive isolation for nuclear DNA. Dis-
covery (hypothesis building) data analysis
methods are selected for the three dis-
ciplines. The same 50 worker ants are
analyzed under all disciplines, and de-
limitation hypotheses are built for the
disciplines separately. Nuclear DNA and
chemistry are conclusive, but morphol-
ogy is inconclusive, in that the statisti-
cal significance level is not met. There-
fore, 50 further workers are sampled for
all three disciplines, resulting in conclu-
siveness of all of them.
 Comparison of conclusive disciplines:
Total disagreement of one particular
type emerges: morphology supports a
two-species hypothesis, but nuclear DNA
and chemistry support a one-species hy-
pothesis. Because there is total disagree-
ment of one particular type, the set of
specimens does not need to be split and
the procedure continues with seeking
an evolutionary explanation for the dis-
agreement. Intraspecific dimorphism of
workers is invoked as the evolutionary
explanation for the disagreement. The
morphology-based hypothesis is con-
sidered implausible, and nuclear DNA
and chemistry are given priority over
morphology. Evolutionary biology prof-
its from the resolution of disagreement,
in that Novomyrmex ants had not been Supplemental Material
known to show intraspecific dimorphism;
in-depth analysis of whether the worker
dimorphism is coupled with alternative
reproductive strategies by small and large
queens can now follow.
 Integrated characterization: The
hypothesis-driven approach (hypothesis
testing) is taken to test whether, despite
lack of support for the plausible hypothe-
sis in the discovery approach (hypothesis
building), the morphometric data at
hand can be used to characterize the
species as one entity. With an association
test, those morphometric characters
that contributed most strongly to the
grouping of specimens as two entities
are singled out and omitted from the
data set. In a reanalysis of the remaining
characters by the discovery data analysis
method used in the primary exploration,
all 100 workers plot as one group. The
remaining characters are thus used for
the morphological characterization of
the species, and the ones omitted are
labeled as indicative of the dimorphism.
The complete microsatellite and cu-
ticular hydrocarbon data sets are used
for the nuclear genetic and chemical
characterization, respectively.
 Nomenclatural consequences: Novo-
myrmex secundus is synonymized under
N. primus.
www.annualreviews.org • Integrative Taxonomy 433
 ANRV397-EN55-22 ARI 10 November 2009 11:17

RATIONALES applies, for example, to morphology (57, 70).

Subjective assessments, especially of shape, are
Widely recognized general rationales apply. A
still practiced (42) and quantitative approaches
comprehensive sample in terms of intraspecific
frequently do not assess continuous character
variation including ecology- and geography-
states for persistent taxonomic problems. Well-
related variation is paramount for approach-
established methods have not been capitalized
ing congruence between recognized and actual
on: Geometric morphometrics allows capturing
species. Voucher deposition and accessibility of
shape in a refined way but has only recently been
primary data are important for follow-up stud-
applied to arthropod taxonomy (42). The de-
ies and meta-analyses. Yet there is an additional
velopment of formal species delimitation crite-
aspect that has received scant attention.
ria received negligible attention by the system-
atic biology community compared with phylo-
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Clarity in Researcher Bias

genetic reconstruction (57, 70), and a broad,
It has been deplored that “taxonomy is not an
empirical cross-validation of criteria is much
Annu. Rev. Entomol. 2010.55:421-438. Downloaded from www.annualreviews.org

exact science” (37). For alpha taxonomy, this

needed. Standardized methods for finding evo-
is true in two respects: Any attempt to catego-
lutionary explanations for disagreements would
rize the diversity of evolving life into species
reduce researcher bias as would methods for
taxa is necessarily imperfect and oversimplified
comparing statistical support across disciplines.
(24), and researcher bias is unavoidable in some
steps of the taxonomic decision-making process
(24, 57). Such researcher bias is inherent to any Taxonomic Training for
approach in taxonomy including DNA-based Evolutionary Biologists
taxonomy, in which, for example, the selection
Practicing integrative taxonomy relies on a
of genes to be sequenced involves subjectivity
strong infusion of evolutionary biological
(36). Yet, honest assessments of uncertainties of
thinking and many evolutionary biologists ad-
methods have generally been lacking (1, 24).
dress species-level problems. When the need
For integrative taxonomy, we have identi-
for nomenclatural changes is revealed, nontax-
fied steps involving researcher bias in Figure 1.
onomists, however, usually shrink from pub-
As the decisions in these steps bear on all fol-
lishing them; in our literature survey, this ap-
lowing steps, the delimitations by different tax-
plied to 75 of 123 sets of specimens. Reasons
onomists may differ. These uncertainties must
for this reluctance may include lack of exper-
be addressed by comprehensively documenting
tise and poor appreciation of the importance
how a particular decision was made. Such clar-
of nomenclature. Solutions include collabora-
ity is paramount for transparency and repro-
tion with trained taxonomists or taxonomic
ducibility of the procedure and thus for revision
training.
of species taxa and cross-validation and fine-
Collaborations between evolutionary bi-
tuning of methods. At present, there is often lit-
ologists and taxonomists are truly feasible.
tle clarity. For example, in our arthropod litera-
However, the work force of taxonomists is
ture survey, a mere 33 of 184 studies mentioned
small, between 6000 (74) and 10,000 (61)
the species concept applied, as noted elsewhere
worldwide. Thus, serious taxonomic training
(32).
for evolutionary biologists who delimit species
is important. Such training helps alleviate the
THE FUTURE OF INTEGRATIVE
taxonomist shortage and increases research out-
TAXONOMY: AGENDA
put in terms of nomenclatural consequences.
Methodological Progress Needed Also, taxonomy then becomes increasingly un-
on Many Frontiers derstood in its logic and difficulties by a broader
Data generation and analysis methods are of- community, rather than being a term to be
ten underexplored. In contrast to genetics, this avoided in grant applications or when aiming

434 Schlick-Steiner et al.

 ANRV397-EN55-22 ARI 10 November 2009 11:17

at high-ranking journals (3). Concerning the
latter we may approach a trend reversal as
shown by occasional taxonomic papers re-
sulting from multiple-discipline delimitation
appearing in high-impact journals (7).
Balanced Resource Allocation
If the profound implications for biology of in-
tegrative taxonomy are to be realized, balanced
resource allocation to both taxonomy and evo-
lutionary biology is necessary (54, 65). To facil-
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current funding policy has changed to reflect
how evolutionary biological research can po-
tentially contribute to taxonomy. This will be
an additional incentive for both communities
to coordinate their efforts.
Geopolitical balance is needed. To obtain
a comparable state of taxonomy in various
regions and thus a sensible census of the
Earth’s species, integrative taxonomy will have
to choose study systems relating to biodiversity-
rich, developing nations with higher frequency
over study systems relating to biodiversity-

itate this, taxonomists also must acknowledge poor, developed nations (64). To achieve this,
that the current taxonomy crisis is due partly international collaborations are needed, and al-
Annu. Rev. Entomol. 2010.55:421-438. Downloaded from www.annualreviews.org

to them (6). It is fair that taxonomists have though examples exist (76), they mark just the
to compete actively for funding—but only if beginning of the journey.

SUMMARY POINTS
1. Using multiple disciplines to solve taxonomic problems helps avoid failure inherent to
single disciplines and increases rigor in species delimitation.
2. For procedural consistency in decision making, a flexible protocol is presented based on
the use of information from every discipline separately.
3. Morphology should always be used for obtaining phenotypic information, alongside
disciplines revealing nuclear genetic and complementary information.
4. Disagreement among disciplines is resolved by seeking evolutionary explanations for
disagreement.
5. If no evolutionary explanation can be found, additional disciplines are added, one at a
time, until the disagreement has been resolved or no more disciplines can be used.
6. Explicitness in decision making is paramount to make researcher bias transparent.
7. For increased success of integrative taxonomy, methodological progress, taxonomic train-
ing, and balanced resource allocation will be vital.

DISCLOSURE STATEMENT
The authors are not aware of any affiliations, memberships, funding, or financial holdings that
might be perceived as affecting the objectivity of this review.

ACKNOWLEDGMENTS
For funding, BCS, FMS, and CS are grateful to the Austrian Science Fund (FWF), and RHC to
the Australian Research Council (DP0665890). BCS and FMS obtained Schrödinger grants (FWF
J2639-B17 and J2642-B17) for a stay in RHC’s lab in Townsville. We thank Nora J. Besansky, Joel
Cracraft, Graham W. Elmes, L. Lacey Knowles, Karl Moder, David R. Nash, and F. James Rohlf

www.annualreviews.org • Integrative Taxonomy 435

 ANRV397-EN55-22 ARI 10 November 2009 11:17

for helpful discussion, and the Editor and two anonymous reviewers for inspiring criticism. BCS
and FMS contributed equally to this review.

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Annual Review of
Entomology

Contents Volume 55, 2010

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Frontispiece
Mike W. Service p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p xiv
Annu. Rev. Entomol. 2010.55:421-438. Downloaded from www.annualreviews.org

The Making of a Medical Entomologist

Mike W. Service p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 1
Ecology of Herbivorous Arthropods in Urban Landscapes
Michael J. Raupp, Paula M. Shrewsbury, and Daniel A. Herms p p p p p p p p p p p p p p p p p p p p p p p p p p19
Causes and Consequences of Cannibalism in Noncarnivorous Insects
Matthew L. Richardson, Robert F. Mitchell, Peter F. Reagel,
and Lawrence M. Hanks p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p39
Insect Biodiversity and Conservation in Australasia
Peter S. Cranston p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p55
Ekbom Syndrome: The Challenge of “Invisible Bug” Infestations
Nancy C. Hinkle p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p77
Update on Powassan Virus: Emergence of a North American
Tick-Borne Flavivirus
Gregory D. Ebel p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p95
Beyond Drosophila: RNAi In Vivo and Functional Genomics in Insects
Xavier Bellés p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 111
Dicistroviruses
Bryony C. Bonning and W. Allen Miller p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 129
Olive Fruit Fly: Managing an Ancient Pest in Modern Times
Kent M. Daane and Marshall W. Johnson p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 151
Insect Silk: One Name, Many Materials
Tara D. Sutherland, James H. Young, Sarah Weisman, Cheryl Y. Hayashi,
and David J. Merritt p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 171
Bayesian Phylogenetics and Its Influence on Insect Systematics
Fredrik Ronquist and Andrew R. Deans p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 189
Insect Fat Body: Energy, Metabolism, and Regulation
Estela L. Arrese and Jose L. Soulages p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 207

vii
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Sex Differences in Phenotypic Plasticity Affect Variation in Sexual Size

Dimorphism in Insects: From Physiology to Evolution
R. Craig Stillwell, Wolf U. Blanckenhorn, Tiit Teder, Goggy Davidowitz,
Charles W. Fox p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 227
Facultative Symbionts in Aphids and the Horizontal Transfer of
Ecologically Important Traits
Kerry M. Oliver, Patrick H. Degnan, Gaelen R. Burke, and Nancy A. Moran p p p p p p p p p 247
Honey Bees as a Model for Vision, Perception, and Cognition
Mandyam V. Srinivasan p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 267
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Invasion Biology, Ecology, and Management of the Light Brown Apple

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Moth (Tortricidae)
D.M. Suckling and E.G. Brockerhoff p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 285
Feeding Mechanisms of Adult Lepidoptera: Structure, Function, and
Evolution of the Mouthparts
Harald W. Krenn p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 307
Integrated Management of Sugarcane Whitegrubs in Australia:
An Evolving Success
Peter G. Allsopp p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 329
The Developmental, Molecular, and Transport Biology of Malpighian
Tubules
Klaus W. Beyenbach, Helen Skaer, and Julian A.T. Dow p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 351
Biorational Approaches to Managing Stored-Product Insects
Thomas W. Phillips and James E. Throne p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 375
Parallel Olfactory Systems in Insects: Anatomy and Function
C. Giovanni Galizia and Wolfgang Rössler p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 399
Integrative Taxonomy: A Multisource Approach to Exploring
Biodiversity
Birgit C. Schlick-Steiner, Florian M. Steiner, Bernhard Seifert,
Christian Stauffer, Erhard Christian, and Ross H. Crozier p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 421
Evolution of Plant Defenses in Nonindigenous Environments
Colin M. Orians and David Ward p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 439
Landscape Epidemiology of Vector-Borne Diseases
William K. Reisen p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 461
Role of Adhesion in Arthropod Immune Recognition
Otto Schmidt, Kenneth Söderhäll, Ulrich Theopold, and Ingrid Faye p p p p p p p p p p p p p p p p p p p p 485
Physical Ecology of Fluid Flow Sensing in Arthropods
Jérôme Casas and Olivier Dangles p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 505

viii Contents
 AR397-FM ARI 12 November 2009 9:17

Managing Invasive Populations of Asian Longhorned Beetle and Citrus

Longhorned Beetle: A Worldwide Perspective
Robert A. Haack, Franck Hérard, Jianghua Sun, and Jean J. Turgeon p p p p p p p p p p p p p p p p p 521
Threats Posed to Rare or Endangered Insects by Invasions of
Nonnative Species
David L. Wagner and Roy G. Van Driesche p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 547
Malaria Management: Past, Present, and Future
A. Enayati and J. Hemingway p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 569
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Regulation of Midgut Growth, Development, and Metamorphosis

Raziel S. Hakim, Kate Baldwin, and Guy Smagghe p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 593
Annu. Rev. Entomol. 2010.55:421-438. Downloaded from www.annualreviews.org

Cellulolytic Systems in Insects

Hirofumi Watanabe and Gaku Tokuda p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 609

Indexes

Cumulative Index of Contributing Authors, Volumes 46–55 p p p p p p p p p p p p p p p p p p p p p p p p p p p 633

Cumulative Index of Chapter Titles, Volumes 46–55 p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 638

Errata

An online log of corrections to Annual Review of Entomology articles may be found at

http://ento.annualreviews.org/errata.shtml

Contents ix