Are insect pollinators more generalist
than insect herbivores?
Colin Fontaine1,*, Elisa The ´bault1and Isabelle Dajoz2
1NERC Centre for Population Biology, Division of Biology, Imperial College London,
Silwood Park Campus, Ascot, Berkshire SL5 7PY, UK
2Bioge ´ochimie et Ecologie des Milieux Continentaux, UMR 7618, Universite ´ Paris 7,
46 rue d’Ulm F-75230, Paris Cedex 05, France
Recent community-level studies have acknowledged that generalist species are more widespread than
previously thought and highlighted their preponderant impact on community functioning and evolution.
It is suggested that the type of interaction, trophic versus mutualistic, should affect species generalization
level; however, no direct comparison has been made yet. Here, we performed such a comparison using 44
plant–insect networks describing either pollination or herbivory communities. Our analysis shows that
the type of interaction does indeed have an impact on various aspects of species generalism, from the
distribution of generalism in the community to the phylogenetic diversity of the plants with which a
given insect species interacts. However, the amplitude of the observed differences depends on the
aspect of species generalism studied. While the non-quantitative and quantitative measures of generalism
suggest that pollinators interact with more plant species and more evenly than herbivores, phylogenetic
measures clearly show that herbivores interact with plant species far more closely related to each other
than pollinators. This comparative approach offers a promising perspective to better understand the
functioning and evolution of multispecies assemblages by pointing out some fundamental singularities
of communities depending on the type of interaction considered.
Keywords: generalism; herbivory; interaction web; mutualistic; pollination; trophic
Interactions among species are one of the most important
drivers of the ecology and evolution of species. Although
historically studies in terrestrial plant–animal interactions
have focused on direct pairwise interactions, it is now
acknowledged that generalization in interactions among
species is more widespread than previously thought. This
relatively high prevalence of generalist species has been
highlighted in both mutualistic (Waser et al. 1996) and
trophic (Novotny & Basset 2005) interaction networks.
Species generalism has some important consequences on
the functioning and evolution of ecological systems, and
the way we study them. Indeed, from an evolutionary per-
spective, the long-standing interest in coevolution between
pairs of species is now challenged by the concept of diffuse
coevolution, where selection pressures caused by one
species change in the presence of other species (Janzen
1980; Fox 1988; Inouye & Stinchcombe 2001; Strauss &
Irwin 2004). In the same way, from an ecological per-
spective, studies on the ecological dynamics of simple
prey–predator systems are now replaced by multispecies
systems and network approaches in which indirect effects
among species via shared interacting partners can be as
strong as the direct effects between interacting species (Lau &
Strauss 2005; van Veen et al. 2006). Thus, generalism is
clearly an important species property from both functional
and evolutionary perspectives. But interestingly, the views
on species generalization are different between the two
research areas concerned, respectively, with mutualistic
plant–pollinator systems and trophic plant–phytophagous
In plant–pollinator studies, network approaches have
been used to identify general patterns in community
organization. It has been proposed that the distribution
of species generalism follows power law family distri-
butions (Jordano et al. 2003); but see Okuyama (2008).
This implies that there is a higher proportion of specialist
species and some higher generalist species than expected
from a random distribution. These findings generate great
interest in the internal structure of pollination webs with
much emphasis on the importance of highly generalist
species in the functioning and resistance to perturbations
of pollination webs (Memmott et al. 2004; Fortuna &
vore studies, the interest mainly focused on the proportion
of extreme specialist species in a community. This is
directly related to the controversy surrounding global
estimates of arthropod species richness (Erwin 1982;
Novotny et al. 2002) that range from 2 to 80 million
species according to the percentage of specialist species
(Thompson 1994). Whereas recent studies have shown
that insect herbivores consume more species than
previously thought (Novotny & Basset 2005), it has been
proposed that these herbivores are often genus specialists,
i.e. thatthe hostplant rangemainlylieswithin plantgenera
rather than within plant species or family (Novotny et al.
2002; Novotny & Basset 2005).
These different current views on insect generalism
may simply arise for historical reasons. The scientific
* Author for correspondence (email@example.com).
Electronic supplementary material is available at http://dx.doi.org/10.
1098/rspb.2009.0635 or via http://rsbl.royalsocietypublishing.org.
Proc. R. Soc. B (2009) 276, 3027–3033
Published online 10 June 2009
Received 15 April 2009
Accepted 13 May 2009
This journal is q 2009 The Royal Society
communities that focused on mutualism or herbivory
were interested in different questions, resulting in appar-
ent differences in insect generalization between these two
types of communities. However, this might also reflect
some real differences in insect generalization depending
on whether insects establish mutualistic or trophic inter-
actions with their plant partners. Indeed, it has been
suggested that the type of interaction could have an
effect on the way interactions are distributed among
species within a community (Rezende et al. 2007;
Bascompte et al. 2003). A few recent studies have
network types (Lewinsohn et al. 2006; Guimaraes et al.
2007a; Thebault & Fontaine 2008; Van Veen et al.
2008). However, although having important evolutionary
and ecological implications, the generalization of mutua-
listic and trophic interaction web has not been compared
yet. In this study, we aim to carry out this comparison,
asking the following questions: first, does the nature of
the interaction affect the level of non-quantified species
generalization (measured as the number of species with
which a focal species interacts) within a community?
Second, are patterns different when considering quanti-
fied generalization indexes that take into account the
relative frequency of interaction? Third, is there a
relationship between non-quantified generalism and
phylogenetic generalism measured as the phylogenetic
range of the species with which a given species interacts?
And if this is the case, is it affected by the nature of the
interaction considered? We performed the comparisons
using community-level plant–insect interaction web data-
sets with resolution at the species level. We focused on
insect generalization because plant–herbivore webs are
mostly focused on one or a few insect groups, whereas
pollination webs aim to consider all pollinators in the
community. Thus, the estimation of plant vulnerability
(i.e. total number of insects that feed on this plant) is
We used 43 datasets from published community-wide studies
of plant–pollinator (n=24) and plant–phytophagous insect
(n=20) interactions (complete references are given in the
electronic supplementary material, appendix 1). Each dataset
had a species resolution level except for a few cases where a
few species were lumped into groups owing to identification
failure. Each dataset consisted of a list of insects associated
with the plant species with which they interact.
(b) Measurement of non-quantified insect
Distributions of non-quantified insect generalism within a
community usually belong to the power family (Jordano
et al. 2003). In order to detect differences among different
parts of the distributions, such as the proportion of extreme
specialist or generalist species, we partitioned them into
octaves. Octaves are intervals that contain a constant increase
with respect to the previous interval and for which divisions
between the classes are equally spaced on a logarithmic
scale (Williams 1964). We choose to use a log3scale that
partitions insect species into six classes of generalism: 1,
2–4, 5–13, 14–41, 42–123 and 124–367. The interest of
this scale is that it allows an extreme specialist to be kept in
a single octave. For each web, we calculated the proportion
of insect species that belongs to the different octaves.
(c) Measurement of quantified insect generalism
in quantified datasets
For 10 of the pollination webs and nine of the herbivory
webs, data on the frequency of each interaction were avail-
able. For these datasets, we calculated the quantified
generalism of each insect k using the metric nk¼ 2Hkdefined
by Bersier et al. (2002), where Hk¼ ?Ps
events of the insect k on plant i and b.krepresents the total
number of feeding events recorded for the insect k.
log2ðbik=b:k;bikÞ represents the number of recorded feeding
(d) Measurement of phylogenetical insect
In order to quantify the degree of phylogenetic generalism
(i.e. the trend for insects to interact with a broad phyloge-
netic range of plant species), we calculated the mean of
the time to the nearest common ancestor of all possible
pairs of plants with which a given insect interacts, using
PHYLOCOM software (Webb et al. 2008). A few plant species
belonging to fern groups were excluded from the analysis
since the available super tree only includes the plant family
belonging to the Euphyllophyte clade. Similarly, the species
name of a few plant species were not available in the original
publication and were also removed from the analysis.
(e) Statistical analyses
All statistical analyses were performed using R statistical
software (v. 2.6). To test for different distributions of
non-quantified insect generalism between pollination and
herbivory webs, we performed a multivariate analysis of
variance (MANOVA). The dependent variables were the per-
centage of insects belonging to the different octaves that were
arcsin(square-root) transformed. The explanatory variables
were the interaction type, the total number of plants per
web and the interaction term. We incorporated this covariate
in the analyses because estimates of species generalism
should indeed be considered with regard to the number of
potentially available alternative plants (Novotny & Basset
2005). To test which part of the distribution differed, we
then analysed each octave separately using linear models
(gls function of nlme package) with the same model structure.
We used a variance function (varIdent of nlme library) that
allows different variances for each level of a stratification vari-
able (here, the type of interaction) in order to accommodate
for heteroscedasticity when necessary. Analyses were not
performed on the two largest octaves as insect never reached
such a generalism level in the herbivory networks present in
our dataset. Finally, since the three herbivory datasets that
involved grasshoppers strongly differed from all other data-
sets in their insect generalism distribution (almost no
extreme specialists; figure 1), we performed this analysis
with and without these three networks.
The quantified generalism of insects was analysed with a
mixed linear model (lme function of nlme package) that
included the type of interaction; the non-quantified insect
generalism (number of plant species) and the interaction
term as fixed effects. The random variable or grouping
factor was the web and this affected the intercept estimates.
We used a variance function (varPower of nlme library) that
3028 C. Fontaine et al. Generalism and interaction type
Proc. R. Soc. B (2009)
allows proportional variance to a covariate (here insect gener-
alism) in order to accommodate for heteroscedasticity. To
insure linearity, both the quantified and non-quantified
insect generalism were log-transformed.
Phylogenetic generalism was analysed with a mixed linear
model (lme function of nlme package) that included the type
of interaction; the non-quantified insect generalism and the
interaction term as fixed effects. The random variable or
grouping factor was the web and this affected both the inter-
cept and the slope estimates. Many pollinator species, mainly
those belonging to Robertson’s dataset, had a higher non-
quantified generalism than the maximum of phytophagous
insects. Therefore, we restricted the dataset to insect species
that had a non-quantified generalism higher than 1 and lower
than 40. The latter value roughly corresponds to the maximal
species generalism observed in phytophagous webs (note that
the results were similar to the complete dataset). Finally, we
used a variance function (varPower of nlme library) that allows
proportional variance to a covariate for each level of a strati-
fication variable (here, the type of interaction), in order to
accommodate for heteroscedasticity.
(a) Non-quantified insect generalism
When analysing the complete dataset, the result of
the MANOVA indicated that the distribution of non-
quantified insect generalism significantly differed between
pollination and herbivory networks (table 1). When ana-
lysing each octave separately, the model integrating
unequal variance between network types always fitted
the data better, indicating a higher variance in herbivory
webs (2.5 times higher on average). We did not find any
effect on the proportion of insect species belonging to
the first octave (mean+s.e. 0.49+0.03; table 2 and
figure 2). For the second octave, we found a significant
effect of the type of interaction with a higher proportion
of such insects in pollination webs (mean+s.e. 0.38+
0.02 and 0.24+0.03 for pollination and herbivory
webs, respectively; table 2 and figure 2). Moreover, the
interaction between the interaction type and the number
of plants in the networks was significant, indicating that
the proportion of such insects decreases with increasing
plant number in pollination webs, whereas it remains con-
stant in herbivory webs (slopes: 20.05, p =0.002 and
0.03, p =0.41, respectively, table 2). We did not find
any significant effect on the proportion of insect species
belonging to the third octave (mean+s.e. 0.16+0.03;
table 2 and figure 2). For the fourth octave, we did not
find any effect of the interaction type (mean+s.e.
0.04+0.01; table 2 and figure 2), but we found a signifi-
cant positive effect of the number of plants present in the
webs (slope estimate: 0.1). Finally, for the two largest
octaves grouping insect species interacting with 42–123
and with 124–367 plant species, none of the hebivory
webs contains such highly generalist insect species.
When removing the three grasshopper datasets that
exhibit really different distributions of insect generalism
from the analysis (figure 1), the differences in generalism
distribution between pollination and herbivory networks
were more pronounced (table 1). When analysing each
octave separately, higher variance in the herbivory web
was still found for octaves 1 and 2 (1.7 times higher on
average) but no longer for octaves 3 and 4. We found a
significantly lower proportion of insects belonging to the
first octave in pollination webs (mean+s.e. 0.46+0.004
and 0.61+0.01 for pollination and herbivory webs,
respectively; table 2 and figure 2), and a higher proportion
of insects belonging to the second and third octaves in
pollination webs (mean+s.e. for pollination and herbivory
webs, respectively, 0.38+0.017 and 0.26+0.028 for the
second octave and 0.14+0.002 and 0.09+0.003 for
the third octave; table 2 and figure 2).
(b) Quantified insect generalism
The model incorporating proportional variance to the
non-quantified generalism fitted the data best, indicating
an increase in quantified generalism variance with
05 10 15202530 35
non-quantified insect generalism (number of plant species)
05 1015 2025
05 10 1520 25
Figure 1. Distribution of insect generalism. Histograms representing the insect generalism distribution (in number of plant
species) from the studies of (a) Arroyo (1982), (b) Prado (2004) and (c) Joern (1979). Pollination networks are in black
and herbivory ones are in grey. Joern’s dataset illustrates the singularity of grasshopper webs compared with other the
datasets used in this analysis.
Table 1. MANOVA of the distribution of insect generalism.
Upper values correspond to the analysis on the complete
dataset. Lower values correspond to the analysis without
number of plant species6,35
of plant species
Generalism and interaction type
C. Fontaine et al.
Proc. R. Soc. B (2009)
non-quantified generalism (figure 3). We found a
significant interaction between the type of interaction
and non-quantified generalism (table 2), indicating that
quantified generalism increased with non-quantified
generalism faster in pollination webs than in herbivory
webs (slope estimates: 0.76 and 0.66, respectively).
(c) Phylogenetic insect generalism
The models that integrated proportional variance to the
non-quantified generalism for each type of interaction
fitted the data best, indicating a higher decrease of
variance with increasing non-quantified generalism in
pollination data compared with trophic data. The mean
time to the common ancestor of the plants with which
an insect interacts was significantly higher in pollination
than in phytophagousnetworks
estimates+s.e. 108 MY+5.1 and 52 MY+5.6, respect-
ively), indicating a much higher phylogenetic generalism
for pollinators. Moreover, the significant interaction
between non-quantified generalism and the type of inter-
action indicates that phylogenetic generalism was not
related to non-quantified generalism in pollination net-
in herbivory networks (slopes: 0.36, p=0.31 and 2.17,
p , 0.0001, respectively, for pollination and herbivory
networks; table 4 and figure 4).
a positive relationship
This study integrates the growing body of recent literature
aiming to understand how different interaction types
influence community structure, dynamics and evolution
(Bascompte et al. 2003; Lewinsohn et al. 2006; Vazquez
et al. 2007; The ´bault & Fontaine 2008). Our analysis
suggests that the type of interaction, i.e. mutualistic
versus trophic, has an impact on various aspects of
species’ generalism, from the distribution of non-quanti-
fied generalism in the community to the phylogenetic
diversity of the plants with which a given species interacts.
However, the amplitude of the observed differences
depends on the aspect of species generalism studied.
While the quantitative measure of generalism helped to
support our results on non-quantified generalism, the
strongest differences were obtained for the phylogenetic
generalism. Hereafter, we will first discuss our results in
the light of the current literature. Second, we will present
different hypotheses involving either ecological mechan-
isms or evolutionary mechanisms, which could be made
to explain the differences in generalization between
pollination and herbivory communities.
When comparing species generalism measured as the
number of interacting partners, the most striking result
was the higher variance observed for herbivory webs.
This could be owing to the higher diversity of tropic
guilds or feeding groups (Simberloff & Dayan 1991)
Table 2. Analysis of the proportion of insect species belonging to different generalism octaves. Upper values correspond to
the analysis of the complete dataset. Lower values correspond to the analysis without grasshopper webs.
octave 1 (generalism
octave 2 (generalism
octave 3 (generalism
octave 4 (generalism
non-quantified insect generalism
5−13 14−41 42−123 124−367
mean proportion of insects
non-quantified insect generalism
5−13 14−41 42−123 124−367
Figure 2. Distribution of insect generalism transformed in to octaves. Bars represent the mean proportion of insects interacting
with a number of partners included in the different octave ranges, in black for pollinators and grey for herbivores. (a) Histogram
representing the complete dataset. (b) Histogram with grasshopper webs removed. Asterisk indicates significant differences
between pollination and herbivory networks (see table 2).
3030 C. Fontaine et al.Generalism and interaction type
Proc. R. Soc. B (2009)
included in the herbivory networks (see electronic sup-
plementary material, appendix 1). However, most of the
variance observed was due to the three grasshopper net-
works that exhibit a singular distribution of generalism
(figure 1) and was not related to classical feeding group
partitioning since they belong to the leaf-chewing guild
that was represented by five other webs in our dataset.
When excluding these three networks from the analysis,
extreme specialization appeared more common in herbiv-
ory networks, and in contrast, generalization was more
widespread in pollination ones. The slightly higher preva-
lence of generalization in pollination communities was
further confirmed by the results on the quantified gener-
alism. Overall, despite some non-negligible variability and
exception, our results are in accordance with the idea that
mutualistic networks tend to be more generalist than
antagonist ones. This idea is commonly held in the litera-
ture dealing with community-level interaction networks
but has not been properly tested yet. Indeed, the nested
structure of mutualistic networks (Bascompte et al.
2003; Guimaraes et al. 2007b; Ollerton et al. 2007)
implies the presence of numerous generalist species, inter-
acting with each other and forming a core to which
specialized species bind. Although less studied, the struc-
ture of antagonistic bipartite networks tends to be
described as compartmentalized (Prado & Lewinsohn
2004; Lewinsohn et al. 2006), i.e. characterized by cohe-
sive groups of interacting species (compartments) with
relatively few interactions among groups. Such a structure
implies a lower prevalence of generalist species. In
addition, herbivores appeared to interact with plant
species far more closely related to each other than pollina-
tors. These results strengthen previous findings showing
that the host plant range of herbivores is often restricted
within a genus (Novotny et al. 2002; Novotny & Basset
2005) and furthermore highlight the comparatively
weaker restriction in the phylogenetic host range for
pollinators (but see Rezende et al. 2007).
These differences in the various aspects of insect gen-
eralization suggest that the ecological and evolutionary
processes generating these interaction webs might differ
between pollination and herbivory communities. Several
ecological factors might affect herbivore and pollinator
generalism. In the plant–herbivore literature, it has been
proposed that the predation pressure imposed by natural
enemies could drive herbivores to specialize (Bernays &
Graham 1988). As most predators of herbivores have
searching patterns related to plant species identity, the
specialization on a plant species not visited by predators
will provide an enemy-free space (Jeffries & Lawton
non-quantified insect generalism
quantified insect generalism
Figure 3. Relation between quantified and non-quantified
insect generalism. Each point represents an insect species.
Black points are pollinator species and grey points are phyto-
phagous species. Lines represent significant regressions
between non-quantified species generalism and associated
Table 3. Analysis of the quantified insect generalism index.
non-quantified insect generalism
phylogenetical insect generalism
mean time to nearest plant common ancestor (MY)
Figure 4. Relation between insect generalism (in number of
plant species) and phylogenetic insect generalism. Each
point represents an insect species: black points for pollinator
species and grey points for phytophagous species. Lines rep-
resent significant regressions between species generalism and
associated phylogenetic generalism index.
Table 4. Analysis of the phylogenetic generalism of insect
Generalism and interaction type
C. Fontaine et al.
Proc. R. Soc. B (2009)
1984). Such an ecological pressure towards specialization
might be less strong for pollinators since the actual flower
handling time by a pollinator is short compared with that
of herbivores that live on a plant for part of their develop-
ment (but see Reader et al. 2006). Although more work is
needed to directly assess such difference in predation
pressure intensity, this ecological process could be
responsible for part of the difference observed.
Another potentially important ecological factor affect-
ing species generalization is species density. Recent
studies have linked it to species generalization through
modification of the inter- and intra-specific competition
strengths in both mutualistic and trophic systems
(Bolnick 2001; Fontaine et al. 2008). Differences in rela-
tive abundances profiles between pollinator and herbivore
communities could indeed influence their generalism
level. However, good abundance data at the community
level are very scarce, making this hypothesis difficult to
test. Although ecological processes certainly play a role
in determining species generalization, more studies are
obviously needed to assess their impacts on mutualistic
and trophic networks.
Evolutionary processes generating interaction web pat-
terns might also be influenced by the type of interaction
considered (Thompson 2005). Natural selection on
mutualisms often specifically favours the development of
multispecies networks through convergence and comple-
mentarity of traits in interacting species (Thompson
1994; Thompson 2005). Indeed, in pollination systems,
the coevolution of flower and insect morphological traits
exemplifies the convergence of disparate plant lineages
into relatively few distinct floral types, reflecting their
adaptation to different pollinator groups (Fenster et al.
2004). However, morphological adaptations (i.e. open
versus tubular flowers and long versus short insect
mouthparts) generate strongly asymmetrical constraints
since pollinators with short mouthparts are restricted to
open flower morphology, whereas insects with longer
mouthparts have access to both floral morphologies
(Fontaine et al. 2006). Such asymmetrical morphological
constraints make the evolution toward generalism poss-
ible and have been shown to strongly structure pollination
networks (Stang et al. 2006).
In contrast, for antagonistic interactions, the continu-
ous coevolution of defences and counter defences may
favour specialization (Thompson 2005). Indeed, the
range of possible interactions in plant–phytophagous
interactions is at least partially driven by the adequacy
between the composition of toxic chemical compounds
in plants and the detoxifying strategies adopted by phyto-
phagous insects (Ehrlich & Raven 1964; Schultz 1988;
Wittstock & Gershenzon 2002). Trade-off between the
ability to detoxify numerous toxic compounds and
the efficiency of the detoxifying processes might restrict
the potential benefits of being generalist. It has been
shown that generalist herbivores, on average, suffer
more from a given toxic compound than specialist
species (Cornell & Hawkins 2003).
Moreover, the specialization on a plant that herbivores
can detoxify by sequestering the toxic compounds,
providing them with protection against predators, has
been documented in various insect taxa (Duffey 1980).
The effect of such different evolutionary constraints on
insect generalism could explain our strong results
regarding the phylogenetic generalism. In pollination
communities, convergence might lead to few phylogenetic
constraints on pollinator generalism, whereas the tighter
coevolution between plants and herbivores should lead
to much stronger phylogenetic constraints on herbivore
Generalism is a species property that includes ecologi-
cal and evolutionary components. By studying these
various aspects in different types of communities, our
study highlights the type of interaction as a determinant
driver of community organization, functioning and
evolution. Although more work is clearly needed to ident-
ify and assess the strength of the different processes
involved, this comparative framework offers the promising
perspective to better understand the functioning and
evolution of multispecies assemblages.
We thank Mathilde Baude, Romain Gallet, Joaquin Hortal,
Pedro Jordano, Ge ´rard Lacroix, Nirmala Massin and
Xavier Raynaud for their help and comments on the
manuscript. We thank Owen T. Lewis, Jenella Loye, Teja
Tscharntke, Lee A. Dyer and Dan H. Janzen for providing
Arroyo, M. T. K., Primack, R. & Armesto, J. 1982 Commu-
nity studies in pollination ecology in the high temperate
Andes of central Chile. Pollination mechanisms and alti-
tudinal variation. Aus. J. Bot. 69, 82–97.
Bascompte, J., Jordano, P., Melian, C. J. & Olesen, J. M.
2003 The nested assembly of plant–animal mutualistic
networks. Proc. Natl Acad. Sci. USA 100, 9383–9387.
Bernays, E. & Graham, M. 1988 On the evolution of host
specificity in phytophagous arthropods. Ecology 69,
Bersier, L. F., Banasek-Richter, C. & Cattin, M. F. 2002
Quantitative descriptors of food-web matrices. Ecology
Bolnick, D. I. 2001 Intraspecific competition favours niche
width expansion in Drosophila melanogaster. Nature 410,
Cornell, H. V. & Hawkins, B. A. 2003 Herbivore responses to
plant secondary compounds: a test of phytochemical co-
evolution theory. Am. Nat. 161, 507–522. (doi:10.1086/
Duffey, S. S. 1980 Sequestration of plant natural-products
by insects. Annu. Rev. Entomol. 25, 447–477. (doi:10.
Ehrlich, P. R. & Raven, P. H. 1964 Butterflies and plants: a
study in coevolution. Evolution 18, 586–608. (doi:10.
Erwin, T. L. 1982 Tropical forests: their richness in Coleop-
tera and other arthropod species. Coleopt. Bull. 36, 74–75.
Fenster, C. B., Armbruster, W. S., Wilson, P., Dudash, M. R.
& Thomson, J. D. 2004 Pollination syndromes and floral
specialization. Annu. Rev. Ecol. Evol. Syst. 35, 375–403.
Fontaine, C., Dajoz, I., Meriguet, J. & Loreau, M. 2006
Functional diversity of plant–pollinator interaction webs
enhances the persistence of plant communities. PLoS
Biol. 4, 129–135.
Fontaine, C., Collin, C. L. & Dajoz, I. 2008 Generalist fora-
ging of pollinators: diet expansion at high density. J. Ecol.
96, 1002–1010. (doi:10.1111/j.1365-2745.2008.01405.x)
Fortuna, M. A. & Bascompte, J. 2006 Habitat loss and the
structure of plant–animal mutualistic networks. Ecol. Lett.
9, 278–283. (doi:10.1111/j.1461-0248.2005.00868.x)
3032C. Fontaine et al.Generalism and interaction type
Proc. R. Soc. B (2009)
Fox, L. R. 1988 Diffuse coevolution within complex commu-
nities. Ecology 69, 906–907. (doi:10.2307/1941243)
Guimaraes, P. R., Rico-Gray, V., Oliveira, P. S., Izzo, T. J.,
dos Reis, S. F. & Thompson, J. N. 2007a Interaction
intimacy affects structure and coevolutionary dynamics
in mutualistic networks. Curr. Biol. 17, 1797–1803.
Guimaraes, P. R., Sazima, C., dos Reis, S. F. & Sazima, I.
2007b The nested structure of marine cleaning symbiosis:
is it like flowers and bees? Biol. Lett. 3, 51–54. (doi:10.
Inouye, B. & Stinchcombe, J. R. 2001 Relationships between
ecological interaction modifications and diffuse coevolu-
tion: similarities, differences, and causal links. Oikos 95,
Janzen, D. H. 1980 When is it coevolution. Evolution 34,
Jeffries, M. J. & Lawton, J. H. 1984 Enemy free space and the
structure of ecological communities. 23, 269–286.
Joern, A. 1979 Feeding patterns in grasshoppers (Orthop-
tera: Acndidae)—factors influencing diet specialization.
Oecologia 38, 325–347. (doi:10.1007/BF00345192)
Jordano, P., Bascompte, J. & Olesen, J. M. 2003 Invariant
properties in coevolutionary networks of plant–animal
interactions. Ecol. Lett. 6, 69–81. (doi:10.1046/j.1461-
Lau, J. A. & Strauss, S. Y. 2005 Insect herbivores drive
important indirect effects of exotic plants on native com-
munities. Ecology 86, 2990–2997. (doi:10.1890/04-1779)
Lewinsohn, T. M., Prado, P. I., Jordano, P., Bascompte, J. &
Olesen, J. M. 2006 Structure in plant–animal interaction
assemblages. Oikos 113, 174–184. (doi:10.1111/j.0030-
Memmott, J., Waser, N. M. & Price, M. V. 2004 Tolerance of
pollination networks to species extinctions. Proc. R. Soc.
Lond. B 271, 2605–2611. (doi:10.1098/rspb.2004.2909)
Novotny, V. & Basset, Y. 2005 Review—host specificity of
insect herbivores in tropical forests. Proc. R. Soc. B 272,
Novotny, V., Basset, Y., Miller, S. E., Weiblen, G. D.,
Bremer, B., Cizek, L. & Drozd, P. 2002 Low host speci-
ficity of herbivorous insects in a tropical forest. Nature
416, 841–844. (doi:10.1038/416841a)
Okuyama, T. 2008 Do mutualistic networks follow pourer
distributions? Ecol. Complexity 5, 59–65. (doi:10.1016/j.
Ollerton, J., McCollin, D., Fautin, D. G. & Allen, G. R. 2007
Finding NEMO: nestedness engendered by mutualistic
organization in anemonefish and their hosts. Proc. R. Soc.
B 274, 591–598. (doi:10.1098/rspb.2006.3758)
Prado, P. I. & Lewinsohn, T. M. 2004 Compartments in
insect–plant associations and their consequences for com-
munity structure. J. Anim. Ecol. 73, 1168–1178. (doi:10.
Reader, T., Higginson, A. D., Barnard, C. J. & Gilbert, F. S.
2006 The effects of predation risk from crab spiders on
bee foragingbehavior. Behav. Ecol.
Rezende, E. L., Lavabre, J. E., Guimaraes, P. R., Jordano, P. &
Bascompte, J. 2007 Non-random coextinctions in phy-
logenetically structured mutualistic networks. Nature 448,
Schultz, J. C. 1988 Many factors influence the evolution of
herbivore diets, but plant chemistry is central. Ecology
69, 896–897. (doi:10.2307/1941239)
Simberloff, D. & Dayan, T. 1991 The guild concept and the
structure of ecological communities. Annu. Rev. Ecol.
Syst. 22, 115–143. (doi:10.1146/annurev.es.22.110191.
Stang, M., Klinkhamer, P. G. L. & van der Meijden, E. 2006
Size constraints and flower abundance determine the
number of interactions in a plant–flower visitor web.
Oikos 112, 111–121. (doi:10.1111/j.0030-1299.2006.
Strauss, S. Y. & Irwin, R. E. 2004 Ecological and evolu-
interactions. Annu. Rev. Ecol. Evol. Syst. 35, 435–466.
The ´bault, E. & Fontaine, C. 2008 Does asymmetric special-
ization differ between mutualistic and trophic networks?
Oikos 117, 555–563. (doi:10.1111/j.0030-1299.2008.
Thompson, J. N. 1994 The coevolution process. Chicago, IL:
University of Chicago Press.
Thompson, J. N. 2005 The geographic mosaic of coevolution.
Chicago, IL: University of Chicago Press.
van Veen, F. J. F., Morris, R. J. & Godfray, H. C. J. 2006
Apparent competition, quantitative food webs, and the
structure of phytophagous insect communities. Ann.
Rev. Entomol. 51, 187–208. (doi:10.1146/annurev.ento.
Van Veen, F. J. F., Mueller, C. B., Pell, J. K. & Godfray,
H. C. J. 2008 Food web structure of three guilds of natu-
ral enemies: predators, parasitoids and pathogens of
aphids. J. Anim. Ecol. 77, 191–200. (doi:10.1111/j.
Vazquez, D. P., Melian, C. J., Williams, N. M., Bluthgen, N.,
Krasnov, B. R. & Poulin, R. 2007 Species abundance and
asymmetric interaction strength in ecological networks.
Oikos 116, 1120–1127. (doi:10.1111/j.0030-1299.2007.
Waser, N. M., Chittka, L., Price, M. V., Williams, N. M. &
Ollerton, J. 1996 Generalization in pollination systems,
and why it matters. Ecology 77, 1043–1060. (doi:10.
Webb, C. O., Ackerly, D. D. & Kembel, S. W. 2008
PHYLOCOM: software for the analysis of phylogenetic com-
munity structure and trait evolution. Bioinformatics 24,
Williams, C. B. 1964 Patterns in the balance of nature and
related problems in quantitative ecology. London, UK:
Wittstock, U. & Gershenzon, J. 2002 Constitutive plant
toxins and their role in defense against herbivores and
pathogens. Curr. Opin. Plant Biol. 5, 300–307. (doi:10.
Generalism and interaction type
C. Fontaine et al.
Proc. R. Soc. B (2009)