Four ways towards tropical herbivore megadiversity

R E V I E W A N DS Y N T H E S I S Four ways towards tropical herbivore megadiversity

Thomas M. Lewinsohn1* and

Tomas Roslin2

1Laboratorio Interacoes Insetos-

Plantas, Depto. Zoologia, IB,

UNICAMP, Campinas 13083-970,

Sao Paulo, Brazil2Metapopulation Research

Group, Department of

Biological and Environmental

Sciences, FI-00014 University of

Helsinki, Helsinki, Finland

*Correspondence: E-mail

[email protected]

Abstract

Most multicellular species alive are tropical arthropods associated with plants. Hence, the

host-specificity of these species, and their diversity at different scales, are keys to

understanding the assembly structure of global biodiversity. We present a comprehensive

scheme in which tropical herbivore megadiversity can be partitioned into the following

components: (A) more host plant species per se, (B) more arthropod species per plant

species, (C) higher host specificity of herbivores, or (D) higher species turnover (beta

diversity) in the tropics than in the temperate zone. We scrutinize recent studies

addressing each component and identify methodological differences among them. We

find substantial support for the importance of component A, more tropical host species.

A meta-analysis of published results reveals intermediate to high correlations between

plant and herbivore diversity, accounting for up to 60% of the variation in insect species

richness. Support for other factors is mixed, with studies too scarce and approaches too

uneven to allow for quantitative summaries. More research on individual components is

unlikely to resolve their relative contribution to overall herbivore diversity. Instead, we

call for the adoption of more coherent methods that avoid pitfalls for larger-scale

comparisons, for studies assessing different components together rather than singly, and

for studies that investigate herbivore beta-diversity (component D) in a more

comprehensive perspective.

Keywords

Beta-diversity, diversity structure, herbivory, host specialization, plant–animal interac-

tions, rarity, species richness, tropics.

Ecology Letters (2008) 11: 398–416

A S P E C I A L F O N D N E S S F O R T R O P I C A L B E E T L E S –

A N D O T H E R P L A N T - E A T I N G B U G S

Recent decades have seen a vigorous debate regarding the

probable number of extant species on Earth. In 1982, Terry

Erwin stirred this up by suggesting that terrestrial species

richness may surpass presently known species by a factor of

15, largely because of undescribed tropical arthropods.

Erwin�s estimate escaped from academia into public

awareness. A major Non-Governmental Organization dis-

tributed a bumper sticker stating �Save Tropical Forests –

30 million insects ca not all be wrong�. Nonetheless, this

figure is still controversial. As pointed out by Stuart Pimm

(2001), our best approximations of the number of species

on Earth are far less precise than current estimates of the

size of the universe.

We do know that most multicellular species alive are

tropical arthropods associated with plants (Price 2002), and

that the regional diversity of most such taxa is highest in the

tropics (with aphids and sawflies as notable exceptions;

Dixon et al. 1987; Gaston & Williams 1996). Hence the

diversity of herbivorous arthropods at different scales is

central to understanding how global biodiversity is put

together. Furthermore, herbivorous arthropods maintain

many important ecosystem processes (Didham et al. 1996)

and form sizeable parts of terrestrial food webs (Lewis et al.

2002; Morris et al. 2004). Given the likely contribution of a

large proportion of species to different ecosystem functions

(Kinzig et al. 2002; Hector & Bagchi 2007), and the

manifold links between species diversity, overall biomass,

resource utilization and the stability of important ecosystem

services (Balvanera et al. 2006; Cardinale et al. 2006), the

dynamics of terrestrial ecosystems seem critically linked to

arthropod diversity.

A central element in Erwin�s (1982) estimate was the

number of insect species unique to each tree species and, by

extension, the expected overlap among the faunas associated

with different hosts in tropical forests. Reevaluation of

Ecology Letters, (2008) 11: 398–416 doi: 10.1111/j.1461-0248.2008.01155.x

� 2008 Blackwell Publishing Ltd/CNRS

overlap coefficients in light of other studies has produced

total figures much below the original 30 million, of the

order of 6–8 million species (Thomas 1990; Ødegaard

2000a and references therein). Hence, the dissimilarity of

faunas associated with different plant species remains of

special interest to current ecology (Ødegaard 2000a;

Novotny et al. 2006; Dyer et al. 2007). It is an effective

quantity, as it can be directly related to ecological processes

and verified by experiments. For a group as poorly

described as arthropods, this measure may also be more

amenable to extrapolations than, for instance, taxonomic

discovery rates (Bebber et al. 2007).

In this appraisal, we scrutinize current ideas about

patterns underlying the higher diversity of herbivores in

the tropics than in the temperate zone. We propose that

recent notions can be represented within a general

conceptual framework, allowing us to apportion variation

in herbivore diversity into four primary components and

their combinations. We identify the relevant components,

scrutinize the most recent assessments of the role of each,

point out important differences among influential studies

and assess our present understanding of patterns and

explanations of tropical insect biodiversity.

F O U R T I E R S O F D I V E R S I T Y

The general idea of dissecting species diversity into

individual components was conceived in studies of

vegetational change over habitat gradients (Whittaker

1967). We will partition the diversity of herbivorous

arthropods into structural elements of herbivore-plant

associations. In this context, we will not discuss the

ultimate ecological or evolutionary processes generating

high tropical biodiversity, as they have been reviewed

repeatedly (Rosenzweig 1995; Gaston 2000; Hill & Hill

2001; Ricklefs 2004; Mittelbach et al. 2007). Instead, we

propose to focus on the resulting, measurable and specific

building blocks of insect–plant interactions. To this effect,

we put forward that current hypotheses for the higher

diversity of herbivores in the tropics than in the temperate

zone can be usefully grouped into four basic components:

(A) more host plant species per se, (B) more arthropod

species per plant species, (C) higher host specialization, or

(D) higher herbivore beta-diversity (Fig. 1). Clearly, these

components are not mutually exclusive: they may combine

in different ways to produce observed differences in total

diversity. Thus, they offer a comprehensive framework

where general differences in diversity can be partitioned

into individual components A–D, and their relative

contribution thereby conveniently compared. We will first

characterize the components individually, then evaluate the

empirical evidence regarding the magnitude of each one in

turn.

More host plant species per se

If the herbivore assemblages of two different regions have

similar patterns of host association, regional differences in

Figure 1 Four seminal components of tropical arthropod megadiversity. Herbivore diversity is depicted schematically as small circles linked

to their host plants by lines. Each symbol represents a different species. Herbivore species may have multiple hosts as indicated by crossing

lines. For each component, the reference assemblage is shown on the left, the more diverse assemblage on the right. Relevant differences are

highlighted by darkened symbols. Components contributing to increased herbivore diversity from the temperate to the tropical zone are: (A)

more host plant species per se; (B) more herbivore species per plant species; (C) less overlap or similarity of herbivores among hosts,

equivalent to higher host specialization; (D) higher turnover of herbivore species on the same hosts among localities.

Review and Synthesis Diversity of herbivore communities 399


floristic diversity will also produce differences in herbivore

diversity (Fig. 1A). The basic component of herbivore

diversity is therefore directly derived from host plant

diversity. Tropical forests are clearly characterized by

outstanding floristic diversity as compared to their temper-

ate counterparts (Gentry 1988; Richards 1996), a pattern

variously ascribed to a number of factors ranging from

current solar energy to Pleistocene history (Brown &

Lomolino 1998; Hill & Hill 2001). In fact, Erwin�s (1982)

estimate of extant insects was derived from the number of

species per host plant species examined, multiplied by the

number of plant species available (Ødegaard 2000a).

Arguably, a linear relation between plant and herbivore

diversity may be regarded as an ecological null pattern

(Gotelli & Graves 1996), so that relevant studies should

focus on deviations from this pattern. Such deviations may

then fruitfully be partitioned into those attributable to B, C

and ⁄or D (Fig. 1).

More herbivore species per plant species

A second way of increasing diversity involves the packing

of more herbivore species on each host species (Fig. 1B).

The general notion of herbivores being more tightly

packed on each tropical plant species can be traced to

several lines of thought which presume that tropical

conditions favour fundamental processes driving species

evolution. This view was formed by early naturalists like

Darwin (1845) and Wallace (1878) who, faced with the lack

of strong winters and the assumed lack of ice ages in the

tropics, believed that this stability would offer time to

build up both more and more highly specialized species

here than in the temperate zone (but for a critique, see

Vazquez & Stevens 2004). Evolution may indeed proceed

at a higher pace in the tropics, given higher temperatures

and faster generation times (Wright et al. 2006; Mittelbach

et al. 2007). As a corollary, Klopfer & MacArthur (1961)

suggested that the main difference between the tropics and

the temperate zone may reside not in the number of

niches available, but in an increase in the similarity of

coexisting species, as shown by reduced character dis-

placement (but see Hubbell & Foster 1986; Terborgh

1992). The extent to which these causal explanations apply

is beyond the scope of the present review. However,

empirical data tend to suggest that communities of

herbivorous insects on plants may not be saturated. Rather

than converging on a set number of insect species per

plant species, local communities tend to vary in proportion

to their regional species pool (Cornell 1985; Cornell &

Lawton 1992; Caley & Schluter 1997; Gaston 2000).

Hence, even without latitudinal differences in basic niche

width, local pools of herbivore species might vary in size

due to factors affecting species richness at larger spatial

scales, including geological and climatic dynamics (Gaston

2000; Hill & Hill 2001).

Another factor which may increase the number of

herbivore species per host species is the higher structural

complexity in tropical habitats. On average, tropical

vegetation in general and tropical forests in particular will

contain more microhabitats per unit ground area than their

temperate counterparts (MacArthur 1972; Proctor 1986).

Hence, each tropical plant species may offer more complex

resources for herbivore species to share or partition.

Thus, several distinct processes may drive Component B.

As the focus of this review is not on evaluating causes but

on their outcomes, our chief interest is whether they

produce a joint, measurable imprint of Component B.

Higher host specialization

Increased diversity in the tropics may also be due to a

smaller overlap of herbivore species among individual host

plant species (Fig. 1C). Like component B, component C

derives from the general notion that in the tropics

organisms are more specialized, with narrower and more

tightly packed niches (Dobzhansky 1950; Levins 1968;

MacArthur 1972). The key distinction is that component C

assumes that the herbivores divide the available set of plant

species more finely amongst themselves, whereas compo-

nent B derives from more herbivore species sharing any

given host. Nevertheless, separating the diversity compo-

nent attributable to host specialization from that of total

host plant diversity (component A, above) is not straight-

forward, as a flora richer in species will also tend to be richer

in genera and families (though not so among continents,

Prance 1994). Hence a comparison of the similarity of

herbivore faunas of two plant species in different families in

one area against that of two congeneric plant species in

another area is difficult to interpret. Some sort of

phylogenetic control will therefore be desirable (Irschick

et al. 2005; Ødegaard et al. 2005) and, whenever possible,

this should be extended to evaluate the phylogenetic �spread�of potential hosts in a local community (Weiblen et al. 2006).

Higher beta-diversity

The number of species in any region will be a function of

how many species we find locally (alpha-diversity) and the

differences we find in species composition among sites

(beta-diversity). Therefore, as a fourth and last alternative,

high diversity can also be due to higher turnover of species

among sites. Note that, for host-associated insects, some

authors also use beta-diversity to designate the turnover of

herbivores among host species (Novotny et al. 2007a;

Murakami et al. 2008). In our scheme, such among-host

turnover comes under component C, so that here

400 T. M. Lewinsohn and T. Roslin Review and Synthesis


beta-diversity is restricted to the spatial turnover of

herbivores on a given host (Fig. 1D).

Latitudinal patterns of beta-diversity were first sought in

plants. Here, initial work suggested low beta-diversity in

neotropical rainforests, despite high total diversity (Pitman

et al. 1999, 2001; Condit et al. 2002). For herbivores, two

ecological patterns may lead us to expect high species

turnover at low latitudes: first, the latitudinal increase in

species richness seems to accelerate towards the equator

(Rosenzweig 1995; but see Gaston et al. 2007) and second,

the species� latitudinal span allegedly decreases (Rapoport�srule; Stevens 1989). In combination, these two effects

should result in higher rates of species spatial turnover at

lower latitudes. Yet the generality of Rapoport�s rule is still

open to debate (Gaston et al. 1998; Kerr 1999; Arita et al.

2005). As an alternative, Novotny & Weiblen (2005) predict

low turnover rates at low latitudes, for two other reasons

combined: many herbivores are specialized on plant genera

and families rather than species (see below; Novotny et al.

2002), and many species-rich plant genera are widely

distributed across large areas of tropical forests (Gentry

1990; Pitman et al. 1999; Condit et al. 2002). Finally, some

recent studies (e.g. Weiser et al. 2007) argue against any

simple and large-scale relation between range size, species

richness and latitude. Thus, as for other components, there

are several theoretical reasons to examine the extent of

Component D, but conflicting predictions on what to

expect.

To end this overview, we note that the four components

are to be interpreted sensu lato. They therefore encompass

several factors which have sometimes been offered as

alternatives to a simple plant-based scheme. For example,

higher herbivore diversity in tropical forests has been

variously ascribed to greater overall plant biomass or to

higher net primary production (Wright 1983). Where such

explanations will fit in our proposed conceptual framework

will depend on their key feature: thus, if it is the individual

size of plants that allows accommodating more herbivore

species per plant, this comes explicitly under component B.

If �higher biomass� implies �more plant species per unit area�,the pattern falls into component A. Such implications are

further examined in the next section, where we turn to

empirical evidence for components A–D.

T H E E V I D E N C E

Most studies so far have addressed components of diversity

one at a time, and even a quick glimpse through the

literature reveals that different components have attracted

very different levels of interest so far (Fig. 2; see also

Appendix S1 in Supplementary Material). Few studies have

examined several components at the same time, or at least

controlled for others while assessing one. This limits the

direct comparison of the relative contribution of each

component, as well as the interpretation of empirical results.

To illustrate the wide array of study systems and approaches

that have been used to date, we have compiled a set of

representative studies in Table 1, including the sampling

design adopted and the main conclusions that concern

individual components.

More host plants

The general increase in diversity from the poles towards the

equator has been established for a very wide range of taxa,

including plants and insects (Hillebrand 2004). As Gaston

(1992) points out, there are no herbivorous insects where

there are no plants – and plenty of both in the tropics.

Therefore, on a crude scale, a general positive relationship

between numbers of arthropod species and numbers of

plant species is obligatory. Nevertheless, for component A

to be regarded as an important contributor to herbivore

diversity, this large-scale association between the diversity of

plants and the diversity of herbivorous arthropods should

clearly be observable across multiple spatial scales as well as

for multiple taxa. Moreover, as different studies have

examined the general relation between insect and plant

diversity by very different techniques, we should also

examine how methodological choices affect the results. To

these ends, we performed a meta-analysis (Cooper &

Hedges 1994) of effect sizes reported in studies addressing

component A. For other components, approaches and data

are too disparate to allow an equivalent exercise.

To examine whether the diversity of herbivorous insect

species will typically increase with the diversity of plants (the

core of component A), we compiled 31 published studies

reporting 80 correlations between the species richness of

herbivorous insects and plants. Search procedures, exact

criteria for inclusion and details on methodology are given

in Appendix S2 (in Supplementary Material), along with the

list of included studies. For each study, we extracted two

descriptors of the study system and four variables delimiting

how the authors dealt with methodological aspects

(Table 2). As our analysis dealt with correlations, we chose

Fisher�s z-transform as measure of effect size (Cooper &

Hedges 1994). To facilitate interpretation, correlation

coefficients were back-transformed [r = tanh(z)] with their

95% CL.

Our meta-analysis of the literature suggests that compo-

nent A makes a key contribution to high diversity of insect

herbivores in areas with high plant diversity. The overall

average correlation coefficient was high (r = 0.56) and

significantly different from 0 (95% CL: 0.519–0.597) across

a broad range of scales and taxonomic resolution. Contrary

to Wolters et al. (2006), we found no difference in the

average correlation effect size among studies conducted in



the tropical and temperate zones (P = 0.16), nor among

effect sizes from different arthropod taxa (P = 0.28), which

suggests a general pattern. Nevertheless, high heterogeneity

among individual values (Q = 408.8, d.f. = 79;

P < 0.00001) indicates that the pattern detected is strongly

affected by how the study was conducted. In particular,

sampling effects seemed a pervasive factor. The correlation

effect size was lower for studies focusing on smaller areas

(P = 0.006; Fig. 3a), and studies inferring local species

richness from limited sample size (P = 0.001; Fig. 3b).

Studies building on many records generated over long time

periods (literature compilations) consistently reported the

highest correlations (P = 0.002; Fig. 3c, see also Fig. 3b).

Furthermore, perhaps not surprisingly, studies where the

herbivores were actually observed on the vegetation

revealed a clearer link between herbivore and plant species

richness than studies where the insects were trapped off the

plant (P = 0.001; Fig. 3d).

Figure 2 Numbers of studies addressing

each individual Component A–D, as broken

down by their study region (abcissas:

Temperate [TEMP], Tropical [TROP] or

Comparative [COMP; i.e. studies spanning

both climatic regions]), and also by: (a)

spatial extent of study (local, regional or

continental); (b) habitats explored (forest,

open habitats or a mixture of both), and (c)

principal feeding mode of herbivores

(endophages, ectophages or both). The

studies included in each category are listed

in Appendix S1. Probability shown above

columns are exact values from the Fisher–

Freeman–Halton exact test (two-tailed) for

the Temperate-Tropical comparison (as

these are exact values, no d.f. apply).

Approximate limits for spatial categories are:

local (< 100 km2); regional (< 100 000 km2);

continental (> 500 000 km2). Open habitats

include savannahs, meadows, agricultural

and cleared areas. Endophages are borers,

miners and gallers whose larvae develop

inside tissues of living plants; ectophages are

especially leaf-chewers and sap-suckers.



Tab

le1

Rep

rese

nta

tive

stu

die

sth

atev

alu

ate

ind

ivid

ual

com

po

nen

tsco

ntr

ibu

tin

gto

the

tota

ld

iver

sity

of

her

biv

oro

us

inse

cts

(Fig

.1).

Co

lum

n�M

eth

od�i

nd

icat

esth

eap

pro

ach

use

d

toco

llect

sam

ple

san

des

tab

lish

the

ho

stp

lan

tar

ray

per

her

biv

ore

spec

ies.

In�M

ain

con

clu

sio

n�l

ette

rsA

–D

ind

icat

ere

sult

sre

levan

tfo

rd

isti

nct

div

ersi

tyco

mp

on

ents

:A

,m

ore

ho

st

pla

nts

;B

,m

ore

her

biv

ore

spec

ies

per

ho

st;

C,

hig

her

spec

ializ

atio

n;

D,

hig

her

bet

a-d

iver

sity

;()

)in

dic

ates

con

trar

yev

iden

ce.

Ind

ivid

ual

stu

die

sar

eso

rted

acco

rdin

gto

the

com

po

nen

t(s)

that

they

pri

mar

ilyre

late

to.

Ref

eren

ceL

oca

tio

n,

hab

itat

Sp

atia

lex

ten

t

of

stu

dy

Tem

po

ral

exte

nt

of

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dy

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nts

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get

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ore

sM

eth

od

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ncl

usi

on

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rdo

ch

etal

.(1

972)

US

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fiel

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ma.

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om

clea

red

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refo

rest

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in(1

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ama,

LT

FL

oca

l,19

tree

s,

500

ha

1-t

ime

fogg

ing

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e(1

sp.)

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l.(6

82

sup

po

sed

her

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ore

s)

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ggin

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ializ

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n

assu

med

B:

hig

hn

um

ber

of

her

biv

ore

so

na

tro

pic

al

tree

Jan

zen

(1988)

Co

sta

Ric

a,d

ry

tro

pic

alfo

rest

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ion

al,

11000

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10

year

s,

con

tin

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(725

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ivo

re

rich

nes

sp

erh

ost

C:

hig

hh

ost

spec

ifici

ty

War

d&

Sp

ald

ing

(1993)

Bri

tain

,al

lh

abit

ats

Co

nti

nen

tal

>50

year

sA

llvas

cula

r

pla

nts

(127

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ilies

)

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her

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oro

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inse

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mp

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s

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on

larg

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op

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ializ

ed(a

th

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)th

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ecto

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edth

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.(2

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tral

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(48–

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in20-k

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per

ate

zon

e

C()

):tr

op

ical

her

biv

ore

s

no

mo

reh

ost

spec

ific

than

tem

per

ate

on

es



Tab

le1

(Con

tinu

ed)

Ref

eren

ceL

oca

tio

n,

hab

itat

Sp

atia

lex

ten

t

of

stu

dy

Tem

po

ral

exte

nt

of

stu

dy

Tar

get

pla

nts

Tar

get

her

biv

ore

sM

eth

od

Mai

nco

ncl

usi

on

Co

rnel

l

(1985)

US

A,

Cal

ifo

rnia

,

var

iou

sh

abit

ats

Reg

ion

al,

c.

900-k

m

span

2ye

ars,

sum

mer

cen

suse

s

Que

rcus

(9sp

p.)

Hym

.ga

ll-m

aker

s

(max

39

spp

.p

er

ho

st,

tota

ln

ot

given

)

Vis

ual

cen

sus

of

galls

B:

no

evid

ence

of

loca

l

satu

rati

on

;

D:

con

stan

tra

tio

of

loca

l

tore

gio

nal

rich

nes

s

An

dre

w

&H

ugh

es

(2004,

2005)

Au

stra

lia,

Eco

ast,

26�–

35�S

;o

pen

low

lan

deu

caly

pt

fore

st

Reg

ion

al,

1150-k

msp

an

2ye

ars,

8

sam

ple

s

Aca

cia

(1fo

cal

+

8co

occ

urr

ing

spp

.)

Co

l.,H

em(1

94

spp

.)

Sh

ort

-dis

tan

cefo

ggin

gB

()):

Hem

rich

nes

s

dec

reas

esw

ith

lati

tud

e;

Co

l.n

och

ange

.

D(±

):b

eta

div

ersi

ty

dec

reas

esw

ith

lati

tud

e

(lo

cal

rich

nes

sco

nst

ant,

regi

on

alri

chn

ess

dec

reas

es);

bu

tsi

mila

rity

hig

her

atlo

wer

lati

tud

es

Zw

olf

er

(1987)

vs.

Lew

inso

hn

(1991)

Eu

rop

ean

dN

Tu

rkey

(41–

51�N

),

mo

stly

op

en

hab

itat

s;vs.

SE

Bra

zil

(17–

24�S

),co

asta

l

du

nes

tom

on

tan

e

mea

do

ws

Co

nti

nen

tal,

77

area

s,2700-k

m

span

vs.

regi

on

al,

11

loca

tio

ns,

720-k

msp

an

>10

year

s,

NS

Svs.

2ye

ars,

3sa

mp

les

in

dif

fere

nt

seas

on

s

Ast

erac

eae,

her

bs

tosh

rub

s

(37

spp

.)vs.

her

bs

totr

eele

ts

(70

spp

.)

Dip

t.,

Lep

.,C

ol.,

flo

wer

hea

d

end

op

hag

es(7

7vs.

86

spp

.)

Han

dco

llect

ing;

on

ly

rear

ing

reco

rds

use

d

B:

mo

resp

ecie

so

fin

sect

s

per

pla

nt

inB

razi

lth

an

Eu

rop

e

D:

hig

hb

eta-

div

ersi

tyin

bo

thre

gio

ns

Bas

set

&

No

vo

tny

(1999)

Pap

ua

New

Gu

inea

,

LT

Fan

d

coas

tal

site

s

17

·31

km

span

,p

lus

nea

rsh

ore

isla

nd

s

1–

2ye

ars,

var

iab

le

Fic

us(1

5sp

p.)

Co

l.,L

ep.,

Ort

h.

foliv

ore

san

d

Ho

m.

sap

-su

cker

s

(779

spp

.)

Han

dp

ickin

g;fe

edin

g

tria

lsan

dre

arin

g

B:

ver

yh

igh

rich

nes

sp

er

ho

stp

lan

t

D:

few

erin

sect

spp

.o

n

coas

tal

ho

sts

Maw

dsl

ey

&S

tork

(1997)

Bru

nei

,L

TF

loca

l,1-k

msp

an1-t

ime

fogg

ing

tree

s(5

spp

.)C

ol.

adu

lts

(859

spp

.,in

clu

din

g

oth

erfe

edin

g

mo

des

)

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ggin

g;h

ost

asso

ciat

ion

infe

rred

fro

mco

n-

vs.

het

ero

spec

ific

inci

den

ce

C()

):h

ost

spec

ifici

tylo

w:

10%

of

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l.sp

ecie

sin

can

op

yes

tim

ated

as

ho

st-s

pec

ific

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egaa

rd

(2000b

)

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ama.

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op

y

of

dry

LT

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Lo

cal,

on

e

site

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ha

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ar,

mo

nth

ly

(day

⁄nig

ht)

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nas

(50

spp

.)

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l.ad

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s,le

af

chew

ers

(286

spp

.)

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tin

g,h

and

pic

kin

gfr

om

cran

e;h

ost

asso

ciat

ion

fro

mo

bse

rvat

ion

s,tr

ials

C:

ho

stsp

ecifi

city

hig

h

No

vo

tny

etal

.

(2002)

Pap

ua

New

Gu

inea

,

LT

F

Lo

cal,

4si

tes,

17

·31

km

span

6ye

ars,

atle

ast

mo

nth

ly

Tre

esan

dsh

rub

s

(51

spp

.)

Co

l.,L

ep.,

Ort

h.,

foliv

ore

s(9

35

spp

.)

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dp

ickin

g;fe

edin

gtr

ials

and

rear

ing

C()

):lo

wfe

edin

g

spec

ializ

atio

n

Dye

ret

al.

(2007)

Can

ada

toB

razi

l,8

area

s(5

3�N

–16�S

).

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rest

s,ce

rrad

o

and

oth

erh

abit

ats.

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cal

to

con

tin

enta

l,

1600–

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000

000

ha*

5–

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S*

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s);

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.)*

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.,m

ost

ly

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tter

flie

s(1

4–

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spp

.)*

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d-p

ickin

g,b

eati

ng

and

oth

erre

cord

s;re

arin

g

reco

rds

on

ly

C:tr

op

ical

her

biv

ore

sm

ore

ho

stsp

ecifi

cth

an

tem

per

ate

on

es



Heterogeneity remained high within groups even after

subdividing studies by methodology (Fig. 3), preventing the

estimation of a single, joint effect size (Cooper & Hedges

1994). Nevertheless, we believe that the most dependable

values derive from studies building on long-term samples

from relatively large areas. For such studies, the correlation

values typically range around 0.8 (Fig. 3a,c), which closely

matches the overall figure reported by Wolters et al. (2006)

for correlations between auto- and heterotroph species

richness. This suggests that c. 60% of variation in the species

richness of herbivorous insects is explained by variation in

the number of plant species.

We conclude that studies that sample herbivorous insects

with appropriate methods and sample sizes typically find an

intermediate to high correspondence between the species

diversity of plants and insects. Therefore, there is consid-

erable support for component A as a prime contributor to

the megadiversity of insects in the diverse flora of the

tropics. Nevertheless, the observed pattern leaves sub-

stantial scope for contribution by other components. This

impression is reinforced by the fact that significant

heterogeneity remains within almost every group formed

in our meta-analysis (Fig. 3), highlighting the unexplained

variation in herbivore diversity due to factors beyond total

plant diversity.

More herbivore species per plant species

Most of what we know about numbers of insects that

actually feed on individual plant species come from studies

which combine in situ feeding observations, experimental

feeding tests, and ⁄or rearing of immature stages (Zwolfer

1987; Marquis 1991; Basset et al. 2003). To date, these

studies offer little direct support for any significant

difference between tropical and temperate regions in terms

of the general number of herbivore species feeding on any

single plant species (Janzen 1988; Basset & Novotny 1999).

Nevertheless, compared to the fair number of assessments

of herbivore richness on plant species in a given locality or

region (Fig. 2), few studies have actually attempted a direct

comparison of herbivore richness among plants in tropical

and temperate sites. Of those that do, almost every one has

adopted a different approach. Four studies exemplify the

range of approaches taken (Table 1).

Andrew & Hughes (2004, 2005) compared insect

assemblages on a single plant species over a 10� latitudinal

range on Australia; they found a slight decrease in

hemipteran richness, but none in beetles (Table 1).

At a much larger spatial scale, Lawton et al. (1993)

examined another species, the bracken fern (Pteridium

aquilinum complex; Thomson 2005). This plant offers a

unique opportunity to compare what is virtually the same

host species among different continents on which it isTab

le1

(Con

tinu

ed)

Ref

eren

ceL

oca

tio

n,

hab

itat

Sp

atia

lex

ten

t

of

stu

dy

Tem

po

ral

exte

nt

of

stu

dy

Tar

get

pla

nts

Tar

get

her

biv

ore

sM

eth

od

Mai

nco

ncl

usi

on

Flo

ren

&

Lin

sen

mai

r

(1998)

Bo

rneo

,L

TF

Lo

cal,

1lo

calit

y,

scal

e?

2ye

ars,

var

iab

le

sch

edu

les

Lo

wer

-str

atu

m

tree

s(3

spp

.)

Co

l.ad

ult

s

(688

spp

.)

Fo

ggin

g,h

ost

asso

ciat

ion

assu

med

D:

hig

hh

erb

ivo

re

bet

a-d

iver

sity

amo

ng

bo

th

con

-an

dh

eter

osp

ecifi

c

tree

ind

ivid

ual

s

Ød

egaa

rd

(2006)

Pan

ama.

Can

op

y

of

mo

ist

and

dry

LT

F

Lo

cal,

2si

tes

c.80

km

apar

t,

0.8

–0.9

ha

each

1ye

ar,

mo

nth

ly

(day

⁄nig

ht)

Tre

esan

dlia

nas

(102

spp

.)

Co

l.,fo

livo

res

(520

spp

.)

As

inØ

deg

aard

2000b

D:

hig

hh

erb

ivo

re

bet

a-d

iver

sity

amo

ng

two

site

s(c

limat

e?)

No

vo

tny

etal

.(2

007a)

Pap

ua

New

Gu

inea

,

LT

F

Reg

ion

al,

8si

tes

in500-k

m

span

5ye

ars,

3m

on

ths

per

site

Tre

es(2

6sp

p.

in

4ge

ner

a)fo

r

Lep

.

Lep

.fo

livo

res

(370

spp

.),

Co

l.w

oo

d-b

ore

rs

(86

spp

.),

Dip

t.

(46

spp

.)

Lep

.h

and

-pic

ked

on

folia

ge,

rear

ed;

Co

l.

ind

ead

wo

od

bai

t;D

ipt.

insc

ent

trap

s(h

ost

sfr

om

oth

erst

ud

y)

D()

):lo

wh

erb

ivo

re

bet

a-d

iver

sity

in

ho

mo

gen

eou

sh

abit

at

Hab

itat

:L

TF

–lo

wla

nd

tro

pic

alfo

rest

.T

emp

ora

lex

ten

to

fsa

mp

ling:

NS

S–

no

sam

plin

gsc

hed

ule

.T

arge

th

erb

ivo

res:

Co

l.–

Co

leo

pte

ra,

Ort

h.

–O

rth

op

tera

+P

has

mat

od

ea,

Dip

t.–

Dip

tera

,H

om

.–

Ho

mo

pte

ra,

Hym

.–

Hym

eno

pte

ra,

Lep

.–

Lep

ido

pte

ra.

*Det

ails

on

ind

ivid

ual

dat

ase

tsar

egi

ven

inD

yer

etal

.(2

007,

Tab

le1

and

Su

pp

lem

enta

ryO

nlin

eM

ater

ial)

.



native. Here, the herbivore assemblage on bracken seems to

reflect idiosyncratic features of each regional biota, and no

latitudinal trend in diversity is detectable (Lawton et al.

1993).

Within an entire host family, Lewinsohn (1991) con-

fronted his own data with those of Zwolfer (1987) to

compare local species richness of flowerhead-feeders on

Asteraceae in the neotropics with that in Europe (Table 1).

Here, species diversity in non-forest ecosystems seems

higher in the neotropics, after adjusting for differences in

sampling effort. However, this comparison is complicated

by the fact that the commonest Asteraceae tribes are

different between the continents, and there is no way to

control for this.

Finally, Dixon et al. (1987); reanalysed by Gaston 1992)

used yet another approach, and focused on the level of the

full flora. With data for 23 countries, they showed that the

ratio of aphid to plant species declines with the number of

plant species per unit area, whereas the ratio of butterfly to

plant species is unrelated to plant diversity. Hence, for

butterflies, species diversity increases in direct proportion to

plant diversity, without any change in species numbers per

plant species. This demonstrates a significant contribution

of Component A (above) but not of Component B.

However, for aphids, tree species at lower latitudes will

actually sustain fewer insect species, an inverse effect of

component B. This may result from a dilution effect: in a

more diverse vegetation, individual host species will be

Table 2 Study descriptors extracted for the meta-analysis of Component A. For each study, we scored two descriptors of the study system

(Climate and Arthropod group) and four variables delimiting how the authors dealt with methodological aspects (Sampling method, Study

scale, Temporal extent and handling of rarity)1. The table defines each variable and classes formed within them.

Variable Classes

Climate – climatic belt where study conducted Temperate ⁄ tropical

Arthropod group – insect order or (where taxonomic

affliation not offered) feeding mode

Coleoptera ⁄Diptera ⁄Heteroptera ⁄Homoptera ⁄Hymenoptera ⁄Lepidoptera ⁄Orthoptera ⁄Thysanoptera ⁄Gallers ⁄Herbivores2 ⁄All3

Sampling method – technique used to generate the insect

material; separates between cases where insects caught or

observed on the plants and methods that build on insect

activity off the plant

Attraction4 ⁄Passive5 ⁄In situ6 ⁄Feeding7 ⁄Compilation8 ⁄Several9

Study scale – scale of individual plots within which plant and

arthropod diversity was measured.10

< 0.001 km2 ⁄0.001–0.099 km2 ⁄0.1–9.9 km2 ⁄10–999 km2 ⁄> 1000 km2

Temporal extent – time span over which the plots were

sampled

Visit11 ⁄Compilation12

Handling of rarity – whether and how author(s) dealt with

rarity and potential sampling problems in the insect material

None13 ⁄Rarefaction ⁄Exclusion14 ⁄Compilation15 ⁄Accumulation16

1Variables are not completely independent, because �compilation� enters as a separate class in three variables. This is justified because

literature compilations differ both from other collection methods (they usually combine data collected by several methods) and from short-

term sampling (they usually sum records obtained over long time periods), and avoid some sampling effects associated with short-term

sampling (they usually build on huge numbers of individual records).2A subset of insects singled out as herbivores by the author(s).3Groups together studies including all insects in the region, regardless of diet, but likely including a non-trivial fraction of herbivores among

them. Studies including at least three different herbivorous insect orders were also attributed to class All.4Trapping methods based on actively attracting the insect to light or baits.5Trapping methods where actively moving individuals are caught off the plant (e.g. pitfall and window traps).6Methods where the insects are observed in, on or near the vegetation (incl. sweep netting, drop traps and line transects).7Methods where the insects are actually observed directly feeding on the plant, e.g. visual observation of gallers.8Studies extracting their data from published catalogues of herbivorous insects and plants.9Studies including several of the methods defined above.10Where sizes varied, the study was classified on the basis of the average size of plots.11Plots sampled by the authors during one or a few field seasons.12Data reflect long-term compilations of the fauna and flora of the study areas.13Author used raw species counts.14Rare species excluded.15Data reflect long-term compilations of the fauna and flora of the study areas.16Species accumulation curve explicitly examined, deemed by author(s) to reach an asymptote.



present at a lower density. Given limited herbivore dispersal,

many host species may then be present at densities too low

for herbivore metapopulations to persist (Dixon et al. 1987).

These few examples attest the shortage of studies that

directly tackle differences in the species diversity of

arthropods per plant species at different latitudes. However,

another line of evidence comes from studies of resource

partitioning in the tropics compared to the temperate zone.

Here, there are more indications for a difference between

tropical and temperate herbivorous faunas. As finer

resource-partitioning can be seen as a mechanism support-

ing more species on a single host plant species (Four tiers

of diversity, above), such studies add indirect support for an

important role for Component B. For example, the fauna on

saplings in the understorey differs from that of the higher

canopy layers of their conspecific trees (Basset 1999, 2001;

Basset et al. 2003). Such differences seem much less

pronounced in temperate forests (Fowler 1985; Lowman

et al. 1993; Le Corff & Marquis 1999) – but not always so

(Murakami et al. 2005).

Figure 3 Results from the meta-analysis of

Component A. Shown are means and 95%

CL for correlations between insect and plant

species richness as broken down by study

methodology: (a) study scale (km2); (b)

handling of rarity and sampling effects; (c)

temporal extent of the study; (d) sampling

method (for Passive traps, the lower confi-

dence limit extended to less than )0.99 and

was truncated). N-values given above sym-

bols refer to the number of correlations in

each group; H indicates that studies within a

category are heterogeneous. For detailed

definitions of variables and class limits, see

Table 2.



To conclude, at present the studies directly comparing

species numbers on tropical and temperate plant species are

relatively few, and their results too varied to support any

generalization. A larger and quicker-growing literature does

reveal differences in the level to which tropical resources are

partitioned among species, suggesting that after all, more

species may be able to share the same tropical plant species

by slicing it in more ways.

Higher host specialization

Arguably, there is more theory and data regarding the host

plant spectra used by herbivore species than on other

aspects of insect-plant associations (Lewinsohn et al. 2005;

Ødegaard 2006). Nevertheless, initial empirical approaches

suffered from methodological problems (see below, It ain�tnecessarily so). More recently, the knowledge of herbivore host

specificity has gradually been improving with studies based

on feeding observations or trials and on rearing records

(Table 1; Janzen 1988; Marquis 1991; Basset & Novotny

1999; Novotny & Basset 2005; Novotny et al. 2004). Here,

high specialization, where strict monophages represent a

large share of the species, has been found in some guilds

(e.g. seed predators, Janzen 1980). In other cases, genera (or

genus groups within families), appear to be the commonest

host span of herbivores (Barone 1998; Novotny et al. 2002),

even those belonging to more specialized guilds (Lewinsohn

1991).

Given this variation in host specificity among taxa, the

evidence for general differences between the tropics and the

temperate zone is ambiguous at best. Overall, the original

expectation of higher specialization in tropical organisms

has been challenged by empirical comparisons of various

organisms (Price 1991); for example, tropical wood-boring

beetles were said to be less, not more, specialized than their

temperate counterparts (Beaver 1979). But as for compo-

nent B, studies actually combining primary data from

different latitudes have been few (Fig. 2). Among the few

that do, Benson (1978) showed that the effective host span

of heliconiine butterflies increases with latitude; in this case,

component C does contribute to an increase in tropical

diversity.

Two other, more recent studies take opposite approaches

to investigate host specialization and its consequences for

herbivore diversity structure. Dyer et al. (2007) examined

specialization patterns over a large geographical range by

aggregating an extensive set of different insect-host studies

(Table 1). By contrast, Novotny et al. (2006) based their

study on a direct comparison of host specificity among

insects on phylogenetically matched sets of hosts in tropical

and temperate local communities (Table 1). Interestingly,

these two studies arrive at completely opposite conclusions.

Whereas Novotny et al. (2002, 2006) assert that tropical

arthropods are no more host-specific than temperate ones,

Dyer et al. (2007) conclude that host specificity is demon-

strably higher in the tropics. Hence, the few comparative

assessments of host specialization in different regions are

Figure 4 Fraction of studies addressing diversity components B

and C by different approaches in different climatic regions

(abcissas: Temperate [TEMP], Tropical [TROP] or Comparative

[COMP; i.e. studies spanning both climatic regions]). (a) Source of

data on feeding association. Here, publication refers to compilation

of published data; mass to data collected by mass sampling such as

fogging, trapping and similar methods; and field to field observa-

tions of actual feeding and ⁄or feeding tests and rearing performed

in the laboratory (b) Growth forms of focal plant taxa. Here,

herb ⁄ shrub refer to studies of herbs, shrubs and vines; tree to studies

focusing on trees including woody shrubs above 3-m height; and all

to studies including many growth forms in the vegetation.

Probabilities shown above columns are exact values from the

Fisher–Freeman–Halton Exact test (two-tailed) for comparisons

among all three climatic regions (as these are exact values, no d.f.

apply). For further details see Appendix S1.



fairly evenly balanced in favour and against its contribution

to herbivore diversity in the tropics. Nevertheless, apparent

discrepancies in results may at least partly reflect discrepant

approaches – an issue to which we return below (It ain�tnecessarily so).

Higher beta-diversity

Patterns of species turnover are hard to address both under

temperate and tropical conditions, as they require extensive

– or at least similar – sampling at repeated sites. In the

tropics, the task is often complicated by challenging

logistical conditions. Yet, several studies have addressed

patterns of beta-diversity within each region (Fig. 2), but by

very different approaches. Two contrasting patterns seem

to emerge: the majority of studies have examined sites

differing in their physical conditions, for instance along an

altitudinal gradient (Novotny et al. 2005a) or sites differing

in disturbance or climate (Beck et al. 2002; Brehm et al.

2003; Ødegaard 2006). Studies in this category tend to

show considerable species turnover. This pattern contrasts

with more mixed findings from the very few studies

comparing sites lacking major physical differences. For

such sites in the tropics, the local species pool can typically

represent a large proportion of the regional species pool,

restricting the margin for species turnover among sites.

Such a pattern has been observed among both fruit flies

and butterflies (Orr & Hauser 1996; Novotny et al. 2005b).

In contrast, one neotropical study (Lewinsohn 1991) found

substantial turnover among similar montane sites in the

species composition of flower-head feeding insects

(Table 1). Yet, a more recent study sampling replicate sites

within a 500-km span reports little turnover across a large

expanse of lowland rainforest (Novotny et al. 2007a). The

authors suggest that from an insect perspective, rainforests

may typically consist of relatively large tracts of homoge-

neous habitat, where beta-diversity will contribute little to

overall arthropod diversity. However, the larger-scale

floristic uniformity of tropical rainforests is not supported

by other studies (Tuomisto et al. 1995; Schulman et al.

2007), and hence the results of Novotny et al. (2007a) will

require replication in other regions before their generality

can be asserted.

To conclude our overview of the evidence for Compo-

nents A–D, the bulk of current evidence indicates that

component A makes a major contribution to tropical

megadiversity, whereas evidence regarding the relative

contribution of B–D seems less easy to generalize. For B,

there is emerging consensus that tropical herbivores

partition their resources more finely than temperate ones,

and ⁄or that there are more and more diverse resources to

share. For components C and D, authors disagree on the

magnitude of individual components, and the data collected

to date do not allow major generalizations. Why do studies

diverge to this extent, and how can current obstacles be

overcome?

I T A I N ’ T N E C E S S A R I L Y S O

Unifying current ideas about factors underlying herbivore

diversity in a general framework not only serves to bring

together disparate patterns into a theoretical whole, but also

pinpoints biases in the evidence collected so far. Our review

of the literature shows that such biases represent critical

impediments for the development of the field. While studies

published to date offer substantial insights into how diverse

herbivore assemblages are put together, they do not allow

any fair comparison of the relative contribution of

components A–D. Most importantly, straightforward con-

trasts are compromised by issues related to sampling

methods, sampling effects, taxonomic biases and spatio-

temporal coverage. As illustrated by Table 1 and Figs 2–4,

different studies have approached them in very different

ways, with likely consequences for the results reported.

Sampling method

Some of the most extensive data on the species richness of

tropical arthropods on individual hosts (Table 1, Fig. 4a)

were obtained by mass-sampling the forest canopy by

insecticide fogging (reviewed in Stork et al. 1997). Yet this

approach is really unsuitable for dissecting insect-host

associations. Insects encountered on a given host do not

necessarily feed on it, and the fraction actually doing so is

hard to establish.

The earlier dependence on fogging data may have

influenced our view on the host specificity of tropical

insects (Fig. 4a; Ødegaard 2000a; Basset et al. 2003). Such

data are rife with pitfalls which also beset other mass-

collecting methods, such as vacuuming or net-sweeping. In

particular, much of the data suggesting high turnover of

insect species among host tree species originally lacked

proof of feeding association (Table 1). Two approaches

have been used to address this problem: first, compare

species turnover rates among heterospecific and conspecific

trees (Mawdsley & Stork 1997); second, estimate non-

sampled associations by fitting observations to a binomial

model (Ødegaard 2000a). Both approaches converged on

c. 10% as an estimate of the fraction of herbivore species

that are effectively restricted to an average host. The extent

to which this figure differs between areas with different

herbivore diversity, or among host plant assemblages that

differ in diversity, growth forms and taxonomic or

phylogenetic breadth, remain open questions.

Nevertheless, to fog or not may not be the only

methodological decision with bearings on likely results. As



shown by the preceding meta-analysis of the literature on

Component A, different sampling techniques tend to show

very different levels of association between species numbers

for herbivores and hosts. The tightest associations are

detected when insects are actually sampled on the vegetation

(or sampled by several techniques combined), whereas

methods that depend on the insects actively moving into

sampling devices report more diffuse associations (Fig. 3d).

As naturalists have known for hundreds of years, how you

seek largely determines what you get.

Rarity and sampling effects

Rarity is the worst nightmare of most diversity studies, and

decisions on how to deal with it often have profound effects

on the results that are obtained. Here, our major concern is

that rarity may affect tropical and temperate studies

differently, and thereby compromise comparisons across

regions.

In the vast majority of biotic communities, most species

are relatively rare, and especially so in species-rich tropical

communities (Price et al. 1995; Basset & Novotny 1999;

Novotny & Basset 2000). Rare species are statistically

elusive, hence researchers face tough choices: sample the

community exhaustively (which may be logistically impos-

sible), truncate data and concentrate on commoner species

(which may bias results), or extra- or intrapolate the data to

estimate real patterns (which again will depend on the

validity of necessary assumptions).

Regarding plant rarity, many authors have simply focused

on common trees (Table 1, Fig. 4b; Erwin 1982; Basset &

Novotny 1999; Barone 2000). For instance, Novotny et al.

(2006); Table 1) chose to sample a fixed number of more

abundant tree species for a phylogenetically controlled

comparison of herbivore richness and host specialization

among tropical and temperate sites. This option may entail a

pitfall: given that more plant species were left out of the

tropical than the temperate survey, and that most of those

are rare hosts, the results of Novotny et al. will only hold for

their entire communities if insect richness and specialization

are not affected by host abundance (Norton & Didham

2007; Novotny et al. 2007b).

Rarefaction techniques, commonly used to make differ-

ent-sized samples comparable (Gotelli & Colwell 2001) do

not fully solve the sampling problem of rare species. In the

meta-analysis of Component A, effect sizes of plant vs.

herbivore species richness were typically even lower for

rarefied samples than for uncorrected values, whereas long-

term data compilations ranked the highest (Fig. 3b).

Likewise, the estimated effect size was higher for long-term

studies than for single samples, likely due to the incom-

pleteness of any short-term sample (Fig. 3c). As each

methodological option comes with a potential bias, the

choice of study organisms and the frequency with which

methods are employed can also affect our general percep-

tion of the literature (Figs 2 and 4a). But do the rare species

most susceptible to sampling effects actually influence the

general structure of insect-plant associations? Recent

research suggests that they do.

Whereas a large fraction of the rare species may be

�tourists� that occur only incidentally on the plant, feeding

trials and rearings show that many rare species are indeed

associated with the studied hosts (Novotny & Basset

2000). Hence, infrequent interactions form a substantial

part of plant-herbivore assemblages (Price et al. 1995;

Novotny & Basset 2000). The simplest alternative in

dealing with such samples is to truncate data and only

consider herbivore species that are represented above an

arbitrary abundance or frequency threshold (Frenzel &

Brandl 1998; Novotny et al. 2007a), but again, in tropical

communities there is a much higher penalty for excluding

species that are statistically inconvenient because of their

rarity. Also, quite worryingly, the consequences of incom-

plete sampling may differ among generalist and specialist

insects (Frenzel & Brandl 1998), so that exclusion of rarer

species will produce biases in comparisons of host

specificity and beta-diversity among data sets and regions.

For beta-diversity, which is fundamentally a reflection of

the range size and local incidence of individual species, the

results are typically established by the commonest species.

Any relation between local abundance and regional

distribution (Hanski et al. 1993) will then threaten the

scope for generalizations.

To sum up, the rarity of a major proportion of both

herbivore and plant species offer one of the chief challenges

to studies of diverse herbivore-plant assemblages. New

procedures may help to overcome at least the statistical

obstacles (Cunningham & Lindenmayer 2005 and compan-

ion papers). For establishing feeding association, we see no

viable alternatives to experimental feeding trials and ⁄or

direct feeding and rearing records.

Taxonomic biases

Data collected from temperate and tropical locations are

often incommensurable. Studies which reach seemingly

different conclusions have often centred on ecologically

distinct taxa (Table 1). In herbivores, what you choose is

partly what you get, as different feeding guilds are known to

exhibit different levels of host specificity. Endophages tend

to be more specialized than ectophages (Gaston et al. 1992;

Ward & Spalding 1993). Thus, of the studies in Table 1,

those focusing on endophages tend to show higher host-

specificity than studies on ectophages, regardless of biome.

Overall, studies to date are biased towards folivores and

other ectophages (Table 1; Fig. 2c) which likely colours our



perception of host specificity in general, and its role for

tropical diversity.

The choice of host plant species to study may also

influence results. So far, much of the work conducted in the

tropics is focused on forest trees (Table 1, Figs 2b and 4b;

for exceptions, see Lewinsohn 1991; Marquis 1991),

whereas temperate studies address either herbs (Brassica-

ceae, Frenzel & Brandl 1998; Asteraceae, Zwolfer 1987;

Table 1), shrubs and trees (oaks, Cornell 1985; Moran &

Southwood 1982; Table 1) or a range of growth forms

(Rosaceae, Leather 1986). Yet we now know that distribu-

tional patterns may differ among trees and other growth

forms. Compared to what appears to be low beta-diversity

in trees (Pitman et al. 1999, 2001; Condit et al. 2002),

pteridophytes and Melastomataceae show substantial turn-

over with both distance and habitat heterogeneity (Tuom-

isto et al. 1995, 2003). While some of these differences may

be attributable to sampling effects (Ruokolainen et al. 2002;

Tuomisto et al. 2003), others are likely true. If the insects

track their hosts, we may then expect different patterns

among insects associated with different kinds of hosts.

From the perspective of insects, there may be more to

plant growth form than potential differences in the hosts�distributional patterns: growth form is intimately linked to

structural complexity, which has been shown to influence the

size and composition of insect assemblages associated with

different hosts (Lawton 1983). Nonetheless, interest in

different growth forms has been highly uneven so far,

especially for studies on herbivore specialization (Fig. 4b).

Of the few extant studies, some do suggest differences in

host specificity among taxa associated with different growth

forms. For example, high numbers of beetles feeding on

lianas tend to show relatively high host specificity (Ødegaard

2000a). Hence, several considerations indicate that surveying

multiple components of the vegetation is another key priority

for future work on arthropods (Ødegaard 2000b, 2006).

Finally, differential focus on distinct growth forms may

entail yet another sampling issue. Given that there are more

studies of smaller-sized plants (e.g. herbs and shrubs) in

temperate than in tropical regions (Fig. 4b), tropical samples

may actually comprise more biomass or larger surfaces of

foliage. While some studies have standardized the area of

foliage examined (Barone 2000; Novotny et al. 2006) or

inspection time (Basset & Novotny 1999), most have not.

Though comparisons of host species with similar growth

forms are most desirable, robust comparisons will at least

require adjustment to equal weight or surface.

Spatiotemporal coverage

Studies of herbivore-plant associations have a very different

history in the tropics than in the temperate zone. As a result,

the very type of host plant records available to ecologists

will often differ between latitudes: whereas many temperate

studies analyse host records gathered over large areas and

long time periods (Strong et al. 1984), tropical data will often

come from the vicinity of biological stations or from

intensive efforts focused on relatively small sites (Janzen

1988; Novotny et al. 2002; Table 1, Fig. 2a). Comparisons

among regions are often based on catalogue data collected

over large areas and many years (Fig. 2a). Yet, the choice of

regional extent will likely affect the patterns observed. This

was illustrated by the meta-analysis of data pertinent to

Component A (Fig. 3b), but also by two studies addressing

Component C. As summarized above (see The evidence), Dyer

et al. (2007) and Novotny et al. (2006) take opposite

approaches to examine Component C – and arrive at

opposite conclusions. By aggregating diverse studies of

insect-host associations at local and regional scales, Dyer

et al. (2007) achieve one of the largest data sets ever on

numbers of hosts per insect. Inevitably, they then pay the

price of using heterogeneous data collected over different

time and space scales, and with different aims and sampling

procedures (Table 1). This constrains their conclusions,

because effects of latitude and scale cannot be easily

untangled. By adopting standardized samples and consistent

criteria for analysis, Novotny et al. (2006) are less exposed to

such methodological noise, but their strict approach limits

the number of observations that can be achieved. Their

temperate-tropical comparison relate to two pairs of local

surveys – which also constrains the generality of their

findings.

The contradiction of the results of these two major

studies highlights that current results are contingent on

methodological choices, and that the stalemate of opposing

conclusions will only be overcome by a number of studies

that comprise sets of sufficiently comparable local surveys

replicated in several regions. Only such data will allow us to

assess the relative contributions of Components A–D to

large-scale patterns in herbivore diversity. Such data are also

required to analyse the interaction structure of plants and

herbivores at different scales and its variation across space

and among habitats. This provides a unique link between

the diversity components of our conceptual scheme, and the

structural and functional attributes of interactive plant-

animal assemblages (Lewinsohn et al. 2006).

T O W A R D S I M P R O V E D B R O A D S C A L E

C O M P A R I S O N S

Modern ecologists have worked hard to disclose the factors

underlying tropical megadiversity of herbivores: over the

last decade or so, the density and quality of evidence has

made a quantum leap. This progress is epitomized by the

latest study by Novotny et al. (2007a), based on over 30

person-years spent under remote field conditions. Such



efforts also incorporate novel methods to investigate

challenging tropical systems. Compilation of the huge data

sets recently published would never haven been possible

without the engagement of local parataxonomists (Basset

et al. 2004; Janzen 2004) and the creative use of recently

produced phylogenies (Novotny et al. 2002, 2006; Weiblen

et al. 2006). Even so, recent progress is still insufficient to

settle disputes on the contribution of various components

to large-scale patterns of insect herbivore diversity. Very

significantly, our review reveals that while new information

is being steadily added both in the tropics and in the

temperate zone, much of it is incommensurable due to

both methodological disparities (different target taxa,

different spatial scales, different ways to handle rarity,

etc.) and to an overall diversity of approaches (especially by

investigating factors singly without controlling for others).

The bottom line of this review is hence that more evidence

of previous kinds will do little to resolve remaining

questions.

Further advances in this field will require new initiatives.

Considering the methodological biases highlighted in this

paper, it is clear that as long as we keep confronting

temperate acorns with tropical breadfruit, we will be

stumped by the same problems of incomparability over and

over again. Given the limitations and challenges that

tropical studies face, researchers were forced to devise ways

of overcoming these obstacles, and it may now be more

profitable to adopt similar protocols in temperate regions

for broad-scale collaborations (Lewinsohn et al. 2005).

What we really need to implement are common and strict

suites of methods across both tropical and temperate sites

(Novotny et al. 2006). But in addition to attempting to

implement the same procedures at several sites across the

globe, it is also important to recognize that some factors

are truly hard to control for. Breadfruit is breadfruit and

acorns are acorns, and whole forests cannot be trans-

planted in a reciprocal approach. As tropical and temperate

forests differ in terms of several factors at once (such as

climate, structural complexity, taxonomic and phylogenetic

diversity of plants), significant effort should be put not

only into detailed dissections of individual associations, but

also into valuable descriptive studies that document

differences between tropical and temperate forests, and

their implications for the assembly of arthropod-plant

communities (for such an ambitious initiative, see Basset

et al. 2007).

Our survey of the literature also highlights that some

components of diversity have received much less attention

than others (Fig. 2). In particular, we argue that stronger and

more comprehensive approaches to quantify patterns of

beta-diversity are needed. The remarkably low species

turnover among distant sites within uniform forest (Nov-

otny et al. 2007a) is related to a very particular definition of

beta-diversity: to species turnover among aggregate samples

from similar sampling localities. The observed pattern

reflects the wide distributional range of some common

species, but it reveals little about local species incidence on

individual host trees, i.e. about patterns that derive from

processes at the population level. More generally, although

the wide distributional range of common species (Hanski

et al. 1993) may inform us of dispersal over evolutionary

time (as reflected in the range sizes of different species), it

reveals little about dispersal in ecological time (with respect

to the contemporary flow of individuals among extant

populations). Novotny et al. (2006, 2007b; see also Novotny

& Weiblen 2005) argue that low beta-diversity in homoge-

neous environments implies that dispersal limitation is not a

key constraint for herbivorous insects. However, only direct

studies of insect dispersal may resolve this issue (Roslin &

Kotze 2005), but these are critically lacking for tropical

regions.

Patterns of low beta-diversity now observed for the first

time in arthropods seem akin to those previously reported

for tropical trees (Pitman et al. 1999, 2001; Condit et al.

2002). Here, a first paradigm of low beta-diversity was later

challenged by results from other taxa and growth forms, and

from the comprehension of species turnover among sites

differing in edaphic conditions (Tuomisto et al. 1995, 2003).

We therefore suggest that additional work on smaller-scale

patterns, on taxa that include other growth forms as well as

trees, may greatly enrich the emerging view on beta-diversity

in tropical as well as temperate arthropods.

Finally, we advocate studies that strive to address

different components of herbivore diversity together rather

than singly. This overview of current knowledge showed

that most studies to date have focused on one component in

a single locality or region. It is high time to collaborate on

more comprehensive study designs, replicated over and

across larger and different regions.

A C K N O W L E D G E M E N T S

We thank Lee Dyer, Angela Moles, Vojtech Novotny, Kalle

Ruokolainen, Hanna Tuomisto and two anonymous referees

for insightful comments on earlier drafts of the manuscript,

and for providing advance copies of papers in press. We

also wish to acknowledge the contribution of many

colleagues, with whom we have discussed these ideas over

the years. Yves Basset and Mar Cabeza-Jaimejuan are

thanked in particular for contributing valuable pointers to

additional literature. Umberto Kubota helped prepare

Figures 1, 2 and 4. Financial support by the Academy of

Finland (grant numbers 111704 and 213457), Fapesp (the

Sao Paulo Research Foundation, grant 04 ⁄15482-1) and

CNPq (the National Research Council of Brazil, grant

306049 ⁄2004) is gratefully acknowledged.



R E F E R E N C E S

Andrew, N.R. & Hughes, L. (2004). Species diversity and structure

of phytophagous beetle assemblages along a latitudinal gradient:

predicting the potential impacts of climate change. Ecol. Ento-

mol., 29, 527–542.

Andrew, N.R. & Hughes, L. (2005). Diversity and assemblage

structure of phytophagous Hemiptera along a latitudinal gradi-

ent: predicting the potential impacts of climate change. Global

Ecol. Biogeogr., 14, 249–262.

Arita, H.T., Rodriguez, P. & Vazquez-Dominguez, E. (2005).

Continental and regional ranges of North American mammals:

Rapoport�s rule in real and null worlds. J. Biogeogr., 32, 961–971.

Axmacher, J.C., Tunte, H., Schrumpf, M., Muller-Hohenstein, K.,

Lyaruu, H.V.M. & Fiedler, K. (2004). Diverging diversity pat-

terns of vascular plants and geometrid moths during forest

regeneration on Mt Kilimanjaro, Tanzania. J. Biogeogr., 31, 895–

904.

Balvanera, P., Pfisterer, A.B., Buchmann, N., He, J.S., Nakashizuka,

T., Raffaelli, D. et al. (2006). Quantifying the evidence for bio-

diversity effects on ecosystem functioning and services. Ecol.

Lett., 9, 1146–1156.

Barone, J.A. (1998). Host-specificity of folivorous insects in a

moist tropical forest. J. Anim. Ecol., 67, 400–409.

Barone, J.A. (2000). Comparison of herbivores and herbivory in

the canopy and understory for two tropical tree species. Biotro-

pica, 32, 307–317.

Basset, Y. (1999). Diversity and abundance of insect herbivores

foraging on seedlings in a rainforest in Guyana. Ecol. Entomol.,

24, 245–259.

Basset, Y. (2001). Communities of insect herbivores foraging on

saplings versus mature trees of Pourouma bicolor (Cecropiaceae) in

Panama. Oecologia, 129, 253–260.

Basset, Y. & Novotny, V. (1999). Species richness of insect her-

bivore communities on Ficus in Papua New Guinea. Biol. J. Linn.

Soc., 67, 477–499.

Basset, Y., Novotny, V., Miller, S.E. & Kitching, R.L. (eds) (2003).

Arthropods of Tropical Forests: Spatio-Temporal Dynamics and Resource

Use in the Canopy. Cambridge University Press, Cambridge, UK.

Basset, Y., Novotny, V., Miller, S.E., Weiblen, G.D., Missa, O. &

Stewart, A.J.A. (2004). Conservation and biological monitoring

of tropical forests: the role of parataxonomists. J. Appl. Ecol., 41,

163–174.

Basset, Y., Corbara, B., Barrios, H., Cuenoud, P., Leponce, M.,

Aberlenc, H.-P. et al. (2007). IBISCA-Panama, a large-scale study

of arthropod beta-diversity and vertical stratification in a low-

land rainforest: rationale, study sites and field methodology. Bull.

Inst. R. Sci. Nat. Belg. Entomol., 77, 39–70.

Beaver, R.A. (1979). Host specificity of temperate and tropical

animals. Nature, 281, 139–141.

Bebber, D.P., Marriott, F.H.C., Gaston, K.J., Harris, S.A. &

Scotland, R.W. (2007). Predicting unknown species numbers

using discovery curves. Proc. R. Soc. London B. Biol. Sci., 274,

1651–1658.

Beck, J., Schulze, C.H., Linsenmair, K.E. & Fiedler, K. (2002).

From forest to farmland: diversity of geometrid moths along

two habitat gradients on Borneo. J. Trop. Ecol., 18, 33–51.

Benson, W.W. (1978). Resource partitioning in passion vine but-

terflies. Evolution, 32, 493–518.

Brehm, G., Homeier, J. & Fiedler, K. (2003). Beta diversity of

geometrid moths (Lepidoptera: Geometridae) in an Andean

montane rainforest. Divers. Distrib., 9, 351–366.

Brown, J. & Lomolino, M. (1998). Biogeography, 2nd edn. Sinauer,

Sunderland, MA.

Caley, M.J. & Schluter, D. (1997). The relationship between local

and regional diversity. Ecology, 78, 70–80.

Cardinale, B.J., Srivastava, D.S., Emmett Duffy, J., Wright, J.P.,

Downing, A.L., Sankaran, M. et al. (2006). Effects of biodiversity

on the functioning of trophic groups and ecosystems. Nature,

443, 989–992.

Condit, R., Pitman, N., Leigh, E.G., Chave, J., Terborgh, J., Foster,

R.B. et al. (2002). Beta-diversity in tropical forest trees. Science,

295, 666–669.

Cooper, H. & Hedges, L.V. (eds) (1994). The Handbook of Research

Synthesis. Russell Sage Foundation, New York.

Cornell, H.V. (1985). Local and regional species richness of cyni-

pine gall wasps on California oaks. Ecology, 66, 1247–1260.

Cornell, H.V. & Lawton, J.H. (1992). Species interactions, local

and regional processes, and limits to the richness of ecological

communities – a theoretical perspective. J. Anim. Ecol., 61,

1–12.

Cunningham, R.B. & Lindenmayer, D.B. (2005). Modeling count

data of rare species: some statistical issues. Ecology, 86, 1135–

1142.

Darwin, C. (1845). The Voyage of the Beagle. Wordsworth, Ware,

Herts.

Didham, R.K., Ghazoul, J., Stork, N.E. & Davis, A.J. (1996).

Insects in fragmented forests: a functional approach. Trends Ecol.

Evol., 11, 255–260.

Dixon, A.F.G., Kindlmann, P., Leps, J. & Holman, J. (1987). Why

there are so few species of aphids, especially in the tropics. Am.

Nat., 129, 580–592.

Dobzhansky, T. (1950). Evolution in the tropics. Amer. Sci., 38,

209–221.

Dyer, L.A., Singer, M.S., Lill, J.T., Stireman, J.O., Gentry, G.L.,

Marquis, R.J. et al. (2007). Host specificity of Lepidoptera in

tropical and temperate forests. Nature, 448, 696–699.

Erwin, T.L. (1982). Tropical forests: their richness in Coleoptera

and other arthropod species. Coleopt. Bull., 36, 74–75.

Floren, A. & Linsenmair, K.E. (1998). Non-equilibrium commu-

nities of Coleoptera in trees in a lowland rain forest of Borneo.

Ecotropica, 4, 55–67.

Fowler, S.V. (1985). Differences in insect species richness and

faunal composition of birch seedlings, saplings and trees: the

importance of plant architecture. Ecol. Entomol., 10, 159–169.

Frenzel, M. & Brandl, R. (1998). Diversity and composition of

phytophagous insect guilds on Brassicaceae. Oecologia, 113, 391–

399.

Frenzel, M. & Brandl, R. (2003). Diversity and abundance patterns

of phytophagous insect communities on alien and native host

plants in the Brassicaceae. Ecography, 26, 723–730.

Gaston, K.J. (1992). Regional number of insects and plant species.

Funct. Ecol., 6, 243–247.

Gaston, K.J. (2000). Global patterns in biodiversity. Nature, 405,

220–227.

Gaston, K.J. & Williams, P.H. (1996). Spatial patterns in taxonomic

diversity. In: Biodiversity: A Biology of Numbers and Difference

(ed Gaston, K.J.). Blackwell Science, Oxford, pp. 202–229.



Gaston, K.J., Reavey, D. & Valladares, G.R. (1992). Intimacy and

fidelity – internal and external feeding by the British Microlep-

idoptera. Ecol. Entomol., 17, 86–88.

Gaston, K.J., Blackburn, T.M. & Spicer, J.I. (1998). Rapoport�srule: time for an epitaph? Trends Ecol. Evol., 13, 70–74.

Gaston, K.J., Davies, R.G., Orme, C.D.L., Olson, V.A., Thomas,

G.H., Ding, T.S. et al. (2007). Spatial turnover in the global

avifauna. Proc. R. Soc. London B. Biol. Sci., 274, 1567–1574.

Gentry, A.H. (1988). Changes in plant community diversity and

floristic composition on environmental and geographical gradi-

ents. Ann. Miss. Bot. Gard., 75, 1–34.

Gentry, A.H. (ed) (1990). Four Neotropical Rainforests. Yale Univer-

sity Press, New Haven.

Gotelli, N.J. & Colwell, R.K. (2001). Quantifying biodiversity:

procedures and pitfalls in the measurement and comparison of

species richness. Ecol. Lett., 4, 379–391.

Gotelli, N.J. & Graves, G.R. (1996). Null Models in Ecology.

Smithsonian Institution Press, Washington.

Hanski, I., Kouki, J. & Halkka, A. (1993). Three explanations of the

positive relationship between distribution and abundance of

species. In: Species Diversity in Ecological Communities (eds Ricklefs,

R.E. & Schluter, D.). University of Chicago Press, Chicago,

pp. 108–116.

Hector, A. & Bagchi, R. (2007). Biodiversity and ecosystem mul-

tifunctionality. Nature, 448, 188–U6.

Hill, J.L. & Hill, R.A. (2001). Why are tropical rain forests so

species rich? Classifying, reviewing and evaluating theories. Prog.

Phys. Geogr., 25, 326–354.

Hillebrand, H. (2004). On the generality of the latitudinal diversity

gradient. Am. Nat., 163, 192–211.

Hubbell, S.P. & Foster, R.B. (1986). Commonness and rarity in a

neotropical forest: implications for tropical tree conservation.

In: Conservation Biology (ed Soule, M.E.). Sinauer, Sunderland,

pp. 205–231.

Irschick, D., Dyer, L. & Sherry, T.W. (2005). Phylogenetic meth-

odologies for studying specialization. Oikos, 110, 404–408.

Janzen, D.H. (1980). Specificity of seed-attacking beetles in a Costa

Rican deciduous forest. J. Ecol., 68, 929–952.

Janzen, D.H. (1988). Ecological characterization of a Costa Rican

dry forest caterpillar fauna. Biotropica, 20, 120–135.

Janzen, D.H. (2004). Setting up tropical biodiversity for conser-

vation through non-damaging use: participation by parataxon-

omists. J. Appl. Ecol., 41, 181–187.

Kerr, J.T. (1999). Weak links: �Rapoport�s rule� and large-scale

species richness patterns. Global Ecol. Biogeogr., 8, 47–54.

Kinzig, A.P., Pacala, S.W. & Tilman, D. (eds) (2002). The Functional

Consequences of Biodiversity : Empirical Progress and Theoretical

Extensions. Princeton University Press, Princeton, NJ.

Klopfer, P.H. & MacArthur, R.H. (1961). On the causes of tropical

species diversity: niche overlap. Am. Nat., 95, 223–226.

Lawton, J.H. (1983). Plant architecture and the diversity of phy-

tophagous insects. Ann. Rev. Entomol., 28, 23–39.

Lawton, J.H., Lewinsohn, T.M. & Compton, S.G. (1993). Pat-

terns of diversity for the insect herbivores on bracken. In:

Species Diversity in Ecological Communities (eds Ricklefs, R.E. &

Schluter, D.). University of Chicago Press, Chicago, pp. 178–

184.

Le Corff, J. & Marquis, R.J. (1999). Differences between under-

storey and canopy in herbivore community composition and leaf

quality for two oak species in Missouri. Ecol. Entomol., 24, 46–58.

Leather, S.R. (1986). Insect species richness of the British Rosa-

ceae: the importance of host range, plant architecture, age of

establishment, taxonomic isolation and species-area relation-

ships. J. Anim. Ecol., 55, 841–860.

Levins, R. (1968). Evolution in Changing Environments; Some Theoretical

Explorations. Princeton University Press, Princeton, NJ.

Lewinsohn, T.M. (1991). Insects in flower heads of Asteraceae in

Southeast Brazil: a case study on tropical species richness. In:

Plant–Animal Interactions: Evolutionary Ecology in Tropical and Tem-

perate Regions (eds Price, P.W., Lewinsohn, T.M., Fernandes,

G.W. & Benson, W.W.). John Wiley, New York, pp. 525–559.

Lewinsohn, T.M., Novotny, V. & Basset, Y. (2005). Insects on

plants: diversity of herbivore assemblages revisited. Annu. Rev.

Ecol. Evol. Syst., 36, 597–620.

Lewinsohn, T.M., Prado, P.I., Jordano, P., Bascompte, J. & Olesen,

J.M. (2006). Structure in plant–animal interaction assemblages.

Oikos, 113, 174–184.

Lewis, O.T., Memmott, J., Lasalle, J., Lyal, C.H.C., Whitefoord, C.

& Godfray, H.C.J. (2002). Structure of a diverse tropical forest

insect-parasitoid community. J. Anim. Ecol., 71, 855–873.

Lowman, M.D., Taylor, P. & Block, N. (1993). Vertical stratifica-

tion of small mammals and insects in the canopy of a temperate

deciduous forest: a reversal of tropical forest distribution? Selb-

yana, 14, 25.

MacArthur, R. H. (1972). Geographical Ecology; Patterns in the Distri-

bution of Species. Harper & Row, New York.

Marquis, R.J. (1991). Herbivore fauna of Piper (Piperaceae) in a

Costa Rican wet forest: diversity, specificity and impact. In:

Plant–Animal Interactions: Evolutionary Ecology in Tropical and Tem-

perate Regions (eds Price, P.W., Lewinsohn, T.M., Fernandes,

G.W. & Benson, W.W.). John Wiley, New York, pp. 179–208.

Mawdsley, N.A. & Stork, N.E. (1997). Host-specificity and the

effective specialization of tropical canopy beetles. In: Canopy

Arthropods (eds Stork, N.E., Adis, J. & Didham, R.K.). Chapman

& Hall, London, pp. 104–130.

Mittelbach, G.G., Schemske, D.W., Cornell, H.V., Allen, A.P.,

Brown, J.M., Bush, M.B. et al. (2007). Evolution and the latitu-

dinal diversity gradient: speciation, extinction and biogeography.

Ecol. Lett., 10, 315–331.

Moran, V.C. & Southwood, T.R.E. (1982). The guild composition

of arthropod communities in trees. J. Anim. Ecol., 51, 289–306.

Morris, R.J., Lewis, O.T. & Godfray, H.C.J. (2004). Experimental

evidence for apparent competition in a tropical forest food web.

Nature, 428, 310–313.

Murakami, M., Yoshida, K., Hara, H. & Toda, M.J. (2005). Spatio-

temporal variation in Lepidopteran larval assemblages associated

with oak, Quercus crispula: the importance of leaf quality. Ecol.

Entomol., 30, 521–531.

Murakami, M., Ichie, T. & Hirao, T. (2008). Beta-diversity of

lepidopteran larval communities in a Japanese temperate

forest: effects of phenology and tree species. Ecol. Res., 23, 179–

187.

Murdoch, W.W., Evans, F.C. & Peterson, C.H. (1972). Diversity

and pattern in plants and insects. Ecology, 53, 819–829.

Norton, D.A. & Didham, R.K. (2007). Comment on ‘‘Why are

there so many species of herbivorous insects in tropical rain-

forests?’’, Science, 315, 1666b.

Novotny, V. & Basset, Y. (2000). Rare species in communities of

tropical insect herbivores: pondering the mystery of singletons.

Oikos, 89, 564–572.



Novotny, V. & Basset, Y. (2005). Host specificity of insect her-

bivores in tropical forests. Proc. R. Soc. London B. Biol. Sci., 272,

1083–1090.

Novotny, V. & Weiblen, G.D. (2005). From communities to

continents: beta diversity of herbivorous insects. Ann. Zool.

Fenn., 42, 463–475.

Novotny, V., Basset, Y., Miller, S.E., Weiblen, G.D., Bremer, B.,

Cizek, L. et al. (2002). Low host specificity of herbivorous

insects in a tropical forest. Nature, 416, 841–844.

Novotny, V., Miller, S., Leps, J., Basset, Y., Bito, D., Janda, M. et al.

(2004). No tree an island: the plant-caterpillar food web of a

secondary rain forest in New Guinea. Ecol. Lett., 7, 1090–1100.

Novotny, V., Miller, S.E., Basset, Y., Cizek, L., Darrow, K., Kaupa,

B. et al. (2005a). An altitudinal comparison of caterpillar (Lepi-

doptera) assemblages on Ficus trees in Papua New Guinea.

J. Biogeogr., 32, 1303–1314.

Novotny, V., Clarke, A.R., Drew, R.A.I., Balagawi, S. & Clifford, B.

(2005b). Host specialization and species richness of fruit flies

(Diptera : Tephritidae) in a New Guinea rain forest. J. Trop.

Ecol., 21, 67–77.

Novotny, V., Drozd, P., Miller, S.E., Kulfan, M., Janda, M., Basset,

Y. et al. (2006). Why are there so many species of herbivorous

insects in tropical rainforests? Science, 313, 1115–1118.

Novotny, V., Miller, S.E., Hulcr, J., Drew, R.A.I., Basset, Y., Janda,

M. et al. (2007a). Low beta diversity of herbivorous insects in

tropical forests. Nature, 448, 692–695.

Novotny, V., Drozd, P., Miller, S.E., Kulfan, M., Janda, M., Basset,

Y. et al. (2007b). Response to comment on ‘‘Why are there so

many species of herbivorous insects in tropical rainforests?’’

Science, 315, 1666c-.

Ødegaard, F. (2000a). How many species of arthropods? Erwin�sestimate revised. Biol. J. Linn. Soc., 71, 583–597.

Ødegaard, F. (2000b). The relative importance of trees versus

lianas as hosts for phytophagous beetles (Coleoptera) in tropical

forests. J. Biogeogr., 27, 283–296.

Ødegaard, F. (2006). Host specificity, alpha- and beta-diversity of

phytophagous beetles in two tropical forests in Panama. Biodiv.

Conserv., 15, 83–105.

Ødegaard, F., Diserud, O.H. & Ostbye, K. (2005). The importance

of plant relatedness for host utilization among phytophagous

insects. Ecol. Lett., 8, 612–617.

Orr, A.G. & Hauser, C.L. (1996). Temporal and spatial patterns of

butterfly diversity in a lowland tropical rainforest. In: Tropical

Rainforest Research – Current Issues. Proceedings of the Conference held in

Bandar Seri Begawan, April 1993 (eds Edwards, D.S., Booth, W.E.

& Choy, S.C.). Kluwer, Dordrecht, pp. 125–138.

Pimm, S.L. (2001). The World According to Pimm : A Scientist Audits the

Earth. McGraw-Hill, New York.

Pitman, N.C.A., Terborgh, J., Silman, M.R. & Nuez, P. (1999). Tree

species distributions in an upper Amazonian forest. Ecology, 80,

2651–2661.

Pitman, N.C.A., Terborgh, J.W., Silman, M.R., Nunez, P., Neill,

D.A., Ceron, C.E. et al. (2001). Dominance and distribution of

tree species in upper Amazonian terra firme forests. Ecology, 82,

2101–2117.

Prance, G.T. (1994). A comparison of the efficacy of higher taxa

and species numbers in the assessment of biodiversity in the

Neotropics. Phil. Trans. R. Soc. London B. Biol. Sci., 345, 89–99.

Price, P.W. (1991). Patterns in communities along latitudinal gra-

dients. In: Plant–Animal Interactions: Evolutionary Ecology in Tropical

and Temperate Regions (eds Price, P.W., Lewinsohn, T.M.,

Fernandes, G.W. & Benson, W.W.). John Wiley, New York, pp.

51–69.

Price, P.W. (2002). Resource-driven terrestrial interaction webs.

Ecol. Res., 17, 241–247.

Price, P.W., Diniz, I.R., Morais, H.C. & Marques, E.S.A. (1995).

The abundance of insect herbivore species in the tropics: the

high local richness of rare species. Biotropica, 27, 468–478.

Proctor, J. (1986). Tropical rain-forest – structure and function.

Prog. Phys. Geogr., 10, 383–400.

Richards, P.W. (1996). The Tropical Rain Forest : An Ecological Study,

2nd edn. Cambridge University Press, Cambridge; New York.

Ricklefs, R.E. (2004). A comprehensive framework for global

patterns in biodiversity. Ecol. Lett., 7, 1–15.

Rosenzweig, M.L. (1995). Species Diversity in Space and Time. Cam-

bridge University Press, Cambridge.

Roslin, T. & Kotze, D.J. (2005). Insects and plants in space. Ann.

Zool. Fenn., 42, 291–294.

Ruokolainen, K., Tuomisto, H., Vormisto, J. & Pitman, N. (2002).

Two biases in estimating range sizes of Amazonian plant species.

J. Trop. Ecol., 18, 935–942.

Schulman, L., Ruokolainen, K., Junikka, L., Saaksjarvi, I.E., Salo,

M., Juvonen, S.K. et al. (2007). Amazonian biodiversity

and protected areas: do they meet? Biodiv. Conserv., 16, 3011–

3051.

Stevens, G.C. (1989). The latitudinal gradient in geographical range:

how so many species coexist in the tropics. Am. Nat., 133, 240–

256.

Stork, N.E., Adis, J. & Didham, R.K. (eds) (1997). Canopy Arthro-

pods. Chapman & Hall, London.

Strong, D.R. Jr, Lawton, J.H. & Southwood, T.R.E. (1984). Insects

on Plants: Community Patterns and Mechanisms. Blackwell, Oxford.

Terborgh, J. (1992). Maintenance of diversity in tropical forests.

Biotropica, 24, 283–292.

Thomas, C.D. (1990). Fewer species. Nature, 347, 237.

Thomson, J.A. (2005). Taxonomy and Evolutionary Relationships in

Bracken: A Worldwide Perspective on the Genus Pteridium for 2005.

International Bracken Group, Liverpool.

Tuomisto, H., Ruokolainen, K., Kalliola, R., Linna, A., Danjoy, W.

& Rodriguez, Z. (1995). Dissecting Amazonian biodiversity.

Science, 269, 63–66.

Tuomisto, H., Ruokolainen, K. & Yli-Halla, M. (2003). Dispersal,

environment, and floristic variation of western Amazonian for-

ests. Science, 299, 241–244.

Vazquez, D. & Stevens, R. (2004). The latitudinal gradient in niche

breadth: concepts and evidence. Am. Nat., 164, E1–E19.

Wallace, A.R. (1878). Tropical Nature and Other Essays. Macmillan

and Co., London,.

Ward, L.K. & Spalding, D.F. (1993). Phytophagous British insects

and mites and their food-plant families – total numbers and

polyphagy. Biol. J. Linn. Soc., 49, 257–276.

Weiblen, G.D., Webb, C.O., Novotny, V., Basset, Y. & Miller, S.E.

(2006). Phylogenetic dispersion of host use in a tropical insect

herbivore community. Ecology, 87, S62–S75.

Weiser, M.D., Enquist, B.J., Boyle, B., Killeen, T.J., Jorgensen,

P.M., Fonseca, G. et al. (2007). Latitudinal patterns of range size

and species richness of New World woody plants. Global Ecol.

Biogeogr., 16, 679–688.

Whittaker, R.H. (1967). Gradient analysis of vegetation. Biol. Rev.,

42, 207–264.



Wolters, V., Bengtsson, J. & Zaitsev, A.S. (2006). Relationship

among the species richness of different taxa. Ecology, 87, 1886–

1895.

Wright, D.H. (1983). Species-energy theory – an extension of

species-area theory. Oikos, 41, 496–506.

Wright, S., Keeling, J. & Gillman, L. (2006). The road from Santa

Rosalia: a faster tempo of evolution in tropical climates. Proc.

Natl Acad. Sci. USA, 103, 7718–7722.

Zwolfer, H. (1987). Species richness, species packing, and evolu-

tion in insect-plant systems. Ecol. Stud., 61, 301–319.

S U P P L E M E N T A R Y M A T E R I A L

The following material is available for this article:

Appendix S1 Literature included in Figures 2 and 4: search

procedure and studies selected.

Appendix S2 A meta-analysis of Component A: data sources,

studies included and calculations implemented.

This material is available as part of the online article

from: http://www.blackwell-synergy.com/doi/full/10.1111/

j.1461-0248.2008.01155.x.

Please note: Blackwell Publishing are not responsible for the

content or functionality of any supplementary materials

supplied by the authors. Any queries (other than missing

material) should be directed to the corresponding author for

the article.

Editor, Jonathan Chase

Manuscript received 24 November 2007

First decision made 15 December 2007

Manuscript accepted 21 December 2007



Four ways towards tropical herbivore megadiversity

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