Ecological Entomology (2012), 37, 342–349
DOI: 10.1111/j.1365-2311.2012.01370.x
The dominant exploiters of the fig/pollinator mutualism
vary across continents, but their costs fall consistently
on the male reproductive function of figs
S I M O N T . S E G A R 1 and J A M E S M . C O O K 1,2
of Reading, Reading, U.K. and
2
1
School of Biological Sciences, University
Hawkesbury Institute for the Environment, University of Western Sydney, Sydney, Australia
Abstract. 1. Fig trees (Moraceae: Ficus) are keystone species, whose ecosystem
function relies on an obligate mutualism with wasps (Chalcidoidea: Agaonidae) that
enter fig syconia to pollinate. Each female flower produces one seed (fig female
reproductive function), unless it also receives a wasp egg, in which case it supports
a wasp. Fig male reproductive function requires both male flowers and pollinator
offspring, which are the only vectors of fig pollen.
2. The mutualism is exploited by other wasps that lay eggs but provide no pollination
service. Most of these non-pollinating fig wasps (NPFWs) do not enter syconia, but
lay eggs through the wall with long ovipositors. Some are gall-makers, while others
are parasitoids or lethal inquilines of other wasps.
3. Ficus is pan-tropical and contains >750 fig species. However, NPFW
communities vary across fig lineages and continents and their effects on the mutualism
may also vary. This provides a series of natural experiments to investigate how the
costs to a keystone mutualism vary geographically.
4. We made the first detailed study of the costs of NPFWs in a fig (Ficus obliqua
G. Forst) from the endemic Australasian section Malvanthera. In contrast to the
communities associated with section Americana in the New World, wasps from the
subfamily Sycoryctinae (Chalcidoidea: Pteromalidae) dominated this community.
5. These sycoryctine wasps have a negative impact on pollinator offspring numbers,
but not on seed production. Consequently, while the NPFW fauna varies greatly at high
taxonomic levels across continents, we show that the consistent main effect of locally
dominant exploiters of the mutualism is to reduce fig male reproductive function.
Key words. Conflict, costs, Ficus, mutualism, pollination, stability, wasps.
Introduction
Mutualisms are partnerships between members of different
species, often from highly divergent taxa, that exchange
resources or services (Foster & Wenseleers, 2006; Leigh,
2010). These associations underpin various ecosystem functions, such as nitrogen fixation and pollination, and are key
components of global biodiversity (Wardle et al., 2004; Sachs
& Simms, 2006). Mutualisms obviously involve co-operation,
but also have inherent conflicts, because the fitness of partners is never perfectly aligned (Herre et al., 1999; Yu, 2001;
Foster & Wenseleers, 2006). The associations often involve a
Correspondence: James M. Cook, School of Biological Sciences, University of Reading, Reading, RG6 6AS, UK. E-mail:
james.cook@reading.ac.uk
342
large host species and several smaller symbiont species, some
of which are beneficial (i.e. mutualists) and others that are not.
The non-mutualist species have been variously termed ‘parasites’, ‘cheaters’, or ‘interlopers’ (Bronstein, 2001; Yu, 2001).
For simplicity, we refer to them here as exploiters to avoid
potential confusion between a generalised use of the term parasite and the more precise ecological role of parasitoid.
It is common for such exploiters to be ecologically and
taxonomically similar to the mutualistic symbiont species
(e.g. Althoff et al., 2001). The exploiters of mutualisms are
generally viewed as detrimental to one or both mutualism
partners (Bronstein, 1994), but their effects have rarely
been quantified. Intriguingly, such exploiters might destabilise
mutualisms (e.g. Lach, 2008), or alternatively help stabilise
them (Dunn et al., 2008), depending on circumstances, so their
roles and costs clearly require targeted study.
2012 The Authors
Ecological Entomology 2012 The Royal Entomological Society
Segar and Cook exploiters decrease fig male function
Ecosystem functions, such as nitrogen fixation and pollination, occur globally and those underpinned by mutualisms
often involve the same lineages (higher taxa) on different continents. However, the exact species involved usually
differ across continents and their little-studied exploiter assemblages are also likely to differ (Thompson, 2005). An important pantropical mutualism involves fig trees (genus Ficus)
and fig-pollinating wasps (family Agaonidae). This evolved
some 75 MYA (Cruaud et al., 2012) and has radiated into
over 750 species pairs (Berg & Corner, 2005). Fig trees are
an important constituent of tropical and subtropical forests
on all continents (Harrison, 2005), as well as occurring in
more open savannah habitats. They can play a key role in
sustaining vertebrate frugivore populations because of their
unusual phenology, which leads to year-round fruit production in most tropical species at the population level. This, in
turn, is linked to their intimate symbiosis with fig wasps,
in which the wasps provide pollination services to fig trees
in exchange for nourishment for their larvae (Cook & Rasplus,
2003).
Female wasps enter fig syconia (inflorescences or ‘figs’)
during a brief period of receptivity. Once inside, they pollinate the female flowers, but also lay eggs into some of them.
Each fig flower can support the development of either one
seed or one pollinator offspring. When the pollinator offspring
are mature, they hatch and mate in the syconium before the
pollen-bearing females disperse to find receptive syconia on
other trees. About half of all Ficus species are monoecious and
the other half functionally dioecious (Berg & Corner, 2005).
The dioecious species have male trees that produce pollen and
wasps, and female trees that produce only seeds. In monoecious fig species, there is just one type of tree and male and
female function occur together in the same syconia (Berg &
Corner, 2005). While many aspects of the fig/pollinator interaction are similar on all tropical continents, each has one or
more endemic radiations of figs from the subgenus Urostigma.
These are Malvanthera in Australasia, Galoglychia in Africa,
Conosycea and Urostigma in Asia, and Americana in America. Some of these Ficus sections co-occur locally, but each
has been evolving independently for at least 30 million years
(Rønsted et al., 2005).
Fig syconia host specialist exploiters – several lineages
of non-pollinating fig wasps (NPFWs) that belong to the
superfamily Chalcidoidea (Hymenoptera) and develop only
in Ficus syconia (see Table 1). Most NPFW species are
known from only one host fig species, just like the pollinating
wasps (Cook & Segar, 2010). Some NPFW lineages have
been associated with Ficus for tens of millions of years
and have radiated across many Ficus sections and continents
[e.g. subfamily Sycophaginae (Cruaud et al., 2011a)], while
others are likely to be more recent colonisers with lower
diversity and geographic range (e.g. family Ormyridae).
Importantly, NPFW communities can differ greatly across
continents. For example, most fig wasp communities from
Africa and Asia include species from several subfamilies
(Table 1) (Compton et al., 1994; Chen et al., 1999; Kerdelhué
et al., 2000), while those associated with the highly speciose
New World section Americana figs (Bronstein & McKey,
343
Table 1. The families and subfamilies of chalcid wasps associated
with Ficus. Taxa in bold are only known to occur on fig plants.
(Sub)family
Region
Trophic role(s)
Sycophaginae
Epichrysomallinae
Otitesellinae
Sycoryctinae
Sycoecinae
Eurytomidae
Torymidae
Ormyridae
Pantropical
Old world
Pantropical
Pantropical
Old world
Pantropical
Pantropical
Old world
Galling wasps and inquilines
Large galling wasps
Galling wasps and inquilines
Parasitoids/inquilines
Galling wasps and inquilines
Large parasitoids/inquilines
Large parasitoids/inquilines
Large galling wasps and
inquilines
1989; West et al., 1996) are dominated by NPFWs from
one subfamily (Sycophaginae). Consequently, the impacts of
exploiters on fig/pollinator mutualisms may vary considerably
across continents.
To date, most studies that have directly addressed the cost
of exploiters in monoecious figs have involved figs from the
section Americana (e.g. Bronstein, 1991; West & Herre, 1994;
West et al., 1996; Pereira & Prado, 2005). Costs of exploitation
can be difficult to detect, due to unmeasured variation between
syconia in resource availability and pollination intensity, and
the fact that NPFW numbers are often low (Bronstein, 1988,
1992; West & Herre, 1994; Bronstein & Hossaert-McKey,
1996; Cook & Power, 1996). However, where a significant
cost has been found in neotropical figs, it has always been to
fig male function, through reduction in numbers of pollinator
offspring. In figs from other continents, some wasps from
the chalcid subfamily Sycoryctinae may reduce pollinator
numbers in a few Asian species (Weiblen et al., 2001; Tzeng
et al., 2008). There is more equivocal evidence for costs
using survey data from African fig species (Kerdelhué et al.,
2000), but again any costs seem to be to fig male function,
and there is further evidence for this from a manipulative
study in which ant exclusion led to increased attack by
Apocrypta wasps and reduced pollinator production (Compton
& Robertson, 1988).
Here, we provide the first detailed description of a NPFW
community of an Australian fig (Ficus obliqua) from the
endemic section Malvanthera and contrast this with the
better studied American and African communities. We then
explore the effects of the dominant NPFW subfamily on
fig male and female function. Our study species, F. obliqua,
is particularly suitable for identifying such costs, because
two major confounding factors – pollination intensity (related
to pollinator foundress number; West & Herre, 1994) and
resource availability (related to fig size; Cook & Power,
1996) – show little variation within and between fruit crops.
Specifically, most fruits receive just one foundress and the
small fruits show little size variation compared to closely
related species such as F. rubiginosa Desf. Ex Vent. (Cook
& Power, 1996).
Within our overall aim to assess the effects of exploiters
on the mutualism, is a subsidiary aim to clarify the ecological
roles and effects of certain key NPFW taxa. This community is
dominated by sycoryctine wasps, the most species-rich lineage
2012 The Authors
Ecological Entomology 2012 The Royal Entomological Society, Ecological Entomology, 37, 342–349
344
Simon T. Segar and James M. Cook
of parasites in figs globally (Segar et al., 2012), but one
whose impacts on the mutualism remain controversial (Dunn
et al., 2008; Herre et al., 2008). The costs of sycoryctines,
absent from the Americana figs, are amenable to study in
F. obliqua, where they prove to be the dominant exploiters
of the mutualism.
Methods
The study system
Ficus section Malvanthera belongs to the subgenus Urostigma and comprises 23 species (Rønsted et al., 2008). It
is endemic to Australasia and has two distinct geographical
radiations, with nine species restricted to Papua New Guinea
(PNG) and the surrounding islands, and the remaining 14 to
Australia (Rønsted et al., 2008). Most species grow as hemiepiphytic stranglers in rainforests, but some grow on rocks in
dry habitats. The Malvanthera probably evolved in Australian
rainforests about 45 Ma (Rønsted et al., 2005).
Ficus obliqua is found along most of the eastern seaboard
of Australia, from Cape York to the south coast of New
South Wales (Dixon et al., 2001), which is a distance of about
2000 km, and in a few south Pacific islands (Berg & Corner,
2005). It grows on rocks in arid areas and as a freestanding
tree or a hemi-epiphyte in rainforests and is pollinated by two
sister species of wasps from the agaonid genus Pleistodontes
(Lopez-Vaamonde et al., 2002).
Dissection of syconia
Wasp communities were sampled by removing, counting, and
identifying all the wasps in large numbers of near-ripe, but
intact, syconia. In total 149 syconia from 11 different sites in
Northern Queensland were collected from 1996 to 2005 and
preserved in 70–95% ethanol. Fruit crops contained from 1
to 19 syconia and most syconia were measured to the nearest
0.1 mm (diameter and length) using vernier callipers before
dissection. Syconia were dissected under a 10–60× dissecting
microscope and each fig ovule was removed from the syconium wall and its contents recorded. Any wasps loose in the
syconium cavity were also counted. Ovules were classified as
seeds, exited galls, galls containing wasps or empty. Empty
ovules, referred to as bladders by some authors (Corlett et al.,
1990; Anstett et al., 1996), were probably undeveloped seeds
or wasps.
Analysing survey data
A few NPFW taxa have been manipulated on the most
experimentally convenient fig species, such as F. racemosa
L. (Wang & Zheng, 2008). However, due to the intricacies
of fig and fig wasp natural history and problems with the
abortion of manipulated figs, the vast majority of studies utilise
survey data (e.g. Corlett et al., 1990; Bronstein, 1991; West &
Herre, 1994; Kerdelhué & Rasplus, 1996; West et al., 1996;
Kerdelhué et al., 2000; Yao et al., 2005; Lin et al., 2008; but
see Compton & Robertson, 1988 for an exception that uses
both approaches).
When investigating the cost of exploitation, variables such
as resource availability and pollination intensity should be
controlled for as far as possible (West & Herre, 1994; Cook
& Power, 1996). The fact that F. obliqua syconia vary little in
size (resource) and that most are entered by just one pollinator
foundress (pollination intensity, JMC, pers. obs.) make this an
excellent study species. However, we also need to consider
what correlations are feasible for exploiters with different
ecological roles.
Herbivorous NPFWs that gall or eat pollinated flowers
should have a negative relationship with seeds. However, they
may also compete with pollinators for flowers, so could also
show a negative relationship with pollinator offspring (West &
Herre, 1994). The observed relationship will thus depend on
when parasites lay eggs, which flowers they use (pollinators
use mostly inner flowers), and the intensity of competition
for flowers. In contrast, exploiters that usurp the galls of
pollinators, killing them directly (parasitoids) or indirectly
(lethal inquilines), should impact mostly on numbers of
pollinator offspring. Nevertheless, as each pollinator offspring
consumes one presumptive seed, parasitoids and inquilines
could also show a weaker negative relationship with seeds.
Impacts of exploiters on seed and pollinator production
The impact of exploiters on fig male and female function was
tested using the number of either seeds or pollinators as the
response variable. A square root transformation of seed number was required to satisfy the assumption of normality for all
analyses (Shapiro–Wilk tests after transformation: W = 0.99,
P = 0.384). Pollinator number was only square root transformed for the linear mixed model analyses, which excluded
syconia that lacked size measurements (Shapiro–Wilk tests
after transformation: W = 0.98, P = 0.084).
We controlled for fig crop (different trees) by including it as
a random explanatory variable. The fixed explanatory variables
were fig size (syconium diameter, a measure of resource
availability), and numbers of Sycoscapter wasps, Philotrypesis
wasps, or pooled sycoryctine wasps (i.e. all wasps in the genera
Sycoscapter + Philotrypesis + Watshamiella).
Linear mixed models were then run using the R package
‘lme4’ in R version 2.10.1 (Bates & Maechler, 2009; R Development Core Team, 2009). A maximum likelihood model was
used, rather than the default restricted maximum likelihood
model, in case some fixed-effects were removed during model
simplification (Crawley, 2007). P -values were then calculated
using the Markov Chain Monte Carlo method in the package
‘Language R’ (Bayen, 2010) using the default settings. We
also calculated Nagelkerke’s R 2 (Nagelkerke, 1991) for each
fixed variable in the maximal model. This calculates an analogue to a standard R 2 value (amount of variation explained)
by comparing the likelihood of a full model against that of one
containing only the intercept. Finally, for illustrative purposes,
we conducted simple linear regressions of the same response
variables on the number of exploiters.
2012 The Authors
Ecological Entomology 2012 The Royal Entomological Society, Ecological Entomology, 37, 342–349
Segar and Cook exploiters decrease fig male function
±
±
±
±
±
±
±
±
±
±
±
±
4.9
3.3
5.1
6.6
13.6
22.3
30.0
20.2
5.1
1.8
3.7
10.85
55.8 ± 6.0
58.3 ± 9.1
75.7 ± 7.5
112.6 ± 5.3
185.4 ± 14.2
122.4 ± 7.3
48.4 ± 9.1
95.9 ± 5.4
118.6 ± 8.1
98.3 ± 9.6
92.0 ± 13.9
100.5 1 ± 4.1
± 0.02
± 0.1
± 0.1
± 0.1
0
0
0
0.1 ± 0.07
0
0
0
0
0
0
0
0.01 ± 0.01
± 0.2
± 0.06
± 0.08
± 0.4
± 0.2
0
0.2
0
0.2
0.1
0
0
0
0.1
0
0
0.08
0.08
0.4
0.2
0.1
0.2
±
±
±
±
±
± 0.4
± 1.7
± 0.2
± 0.07
± 3.3
± 0.1
± 0.2
± 0.7
± 0.2
± 0.3
± 0.07
± 0.1
0.05
1.4
2.6
0.5
0.4
0.9
0.5
2.4
0.4
±
±
±
±
±
±
±
±
±
0
0.05
7.5
6.7
0.5
1.2
1.1
0.8
3.5
2.7
2012 The Authors
Ecological Entomology 2012 The Royal Entomological Society, Ecological Entomology, 37, 342–349
0.3
0.3
0.4
0.2
*These wasps are considerably larger than the pollinating wasps and develop in proportionately larger galls.
Total means are derived from the full data set (n = 149).
± 0.07
± 0.3
± 0.05
0.08
0.6
0.2
0.2
0.3
0
0.08
0.6
0.2
0
0
0.2
± 0.5
± 0.2
0
0.9
0.2
0
0.07
0.3
0
0
0
0
0
0.1
± 0.5
0
0.7
0
0.1
9.8
0
0
0
2.6
0.2
0
1.4
± 0.3
± 0.5
0.5
0.7
0
0.4
0.07
0.1
0
0.2
1.0
0.2
0
0.3
6.2 ± 1.6
4.6 ± 1.5
2.2
3.2
1.9
1.2
3.6
3.5
4.1
0.7
0.9
1.4
2.0
0.7
±
±
±
±
±
±
±
±
±
±
±
±
9.4
9.4
3.3
4.9
11.0
4.1
11.7
1.3
2.4
3.7
4.2
6.4
4.7
4.4
6.6
3.7
4.2
12.2
4.7
5.6
5.3
5.5
3.9
2.2
There was a significant negative relationship between pooled
sycoryctines and pollinator numbers that explained from 8
to 14% of the variance (Tables 4 and 5). In contrast, there
was no trade-off with seed numbers, with less than 1% of
the variance in seed number being explained by sycoryctines
in mixed models or simple regressions (Tables 4 and 5 and
Fig. 1). Sycoscapter alone also displayed a negative relationship with pollinators, but the less numerous Philotrypesis did
not (Table 4). Neither Sycoscapter nor Philotrypesis showed a
significant negative relationship with seeds in the mixed models (Table 4).
0.2
0.1
0.2
0.2
The impact of sycoryctine wasps on Ficus obliqua
7.0 ±
6.2 ±
7.0 ±
7.8 ±
NA
NA
NA
NA
6.7 ±
3.4 ±
7.3 ±
6.4 ±
Nine genera and 10 species of wasps were found in 18
crops of F. obliqua syconia (Table 2). The numbers of seeds
and wasps varied considerably between syconia and crops
(Table 3), but all crops contained some NPFWs. Only 17%
of individual syconia lacked NPFWs, and only 23% did not
contain sycoryctines. Overall, the NPFW fauna was dominated
by wasps from the subfamily Sycoryctinae (1441 individuals,
84% of all NPFWs), which was represented by three species
from different genera. Sycoscapter sp. (920; 54%) was the
most abundant, followed by Philotrypesis sp. (384; 22%) and
the much rarer Watshamiella sp. wasps (49; 3%). In six figs
(5%) the sycoryctines were not identified to genus level.
Most remaining NPFWs belonged to the subfamily Sycophaginae (Table 2). Eukobelea sp. was present in only a few
crops (six of 18), but quite abundant in these. In contrast,
there were rarely more than four Pseudidarnes sp. wasps in
a syconium (Table 2). A few species of much larger wasps
that develop in large galls were also found (Table 2). These
were all rare with patchy distributions and very low numbers
(usually just one or two individuals) per syconium.
Table 3. Mean syconium contents for 11 crops (all those with n > 5 syconia) of Ficus obliqua given with 1 SE.
Wasp community composition
12
10
6
19
14
7
13
13
16
16
6
132
Results
±
±
±
±
±
±
±
±
±
±
±
±
Heredotia*
Sycophila*
There was one species in each genus apart from Pleistodontes, which
had two. Mean abundances per syconium are given with 1 SE.
Prevalence refers to the percentage of syconia in which the genus
was found.
45.6
34.3
65.3
63.6
24.2
52.3
54.8
76.9
51.6
85.8
93.8
57.5
Empty
Seeds
Megastigmus*
66
42
10
10
5
11
7
1
Pseudidarnes*
0.7
0.4
0.1
0.4
0.05
0.06
0.02
0.01
Eukobelea
Sycoscapter
6.4 ±
Philotrypesis
2.7 ±
Watshamiella
0.3 ±
Eukobelea
1.4 ±
Pseudidarnes 0.1 ±
Heredotia
0.2 ±
Sycophila
0.08 ±
Megastigmus 0.01 ±
Pollinator/
galler
Parasitoid
Parasitoid
Parasitoid
Galler
Galler
Galler
Parasitoid
Parasitoid
Watshamiella
Sycoryctinae
Sycoryctinae
Sycoryctinae
Sycophaginae
Sycophaginae
Epichrysomallinae
Eurytomidae
Torymidae
100
Philotrypesis
57.5 ± 2.2
Sycoscapter
Pleistodontes
Poll. wasps
Agaonidae
Diam. (mm)
Genus
Prevalence
(%)
Ecology
n
(Sub)family
Mean
abundance
1.6
1.5
2.0
2.1
2.2
3.2
4.5
2.0
1.4
0.7
2.1
1.0
Table 2. Wasp taxa sampled from Ficus obliqua.
345
346
Simon T. Segar and James M. Cook
Table 4. Results of linear mixed models testing for effects of
exploiters on the mutualism.
Response
Explanatory
Figs/crops
t
P
R2
Pollinators
Sycoscapter
Diameter
Philotrypesis
Diameter
Sycoryctines
Diameter
Sycoscapter
Diameter
Philotrypesis
Diameter
Sycoryctines
Diameter
93/11
−3.508
2.854
−0.146
3.056
−3.659
2.793
−1.320
2.462
0.057
2.564
0.062
2.447
<0.001
0.005
0.884
0.003
<0.001
0.006
0.190
0.016
0.955
0.012
0.951
0.016
11
4
4
6
8
4
7
4
6
5
<1
5
Pollinators
Pollinators
Seeds
Seeds
Seeds
93/11
96/12
87/11
87/11
90/12
Models contained the fixed explanatory variables exploiters
(Sycoscapter, or Philotrypesis, or pooled sycoryctines) and fig diameter, as well as the random explanatory variable fig crop. Nagelkerke’s
R 2 is given for each variable.
Table 5. Results of simple regressions of seed and pollinator numbers
on the number of exploiters.
Response
Explanatory
d.f.
t
P
% var.
Pollinators
Pollinators
Pollinators
Seeds
Seeds
Seeds
Sycoscapter
Philotrypesis
Sycoryctines
Sycoscapter
Philotrypesis
Sycoryctines
141,1
141,1
147,1
134,1
134,1
140,1
−3.887
−3.200
−5.068
−3.054
1.343
−1.344
<0.001
0.002
<0.001
0.003
0.181
0.181
9
6
14
7
1
1
Discussion
The fig/pollinator symbiosis has a pantropical distribution, but
both plant and pollinator species differ across continents. The
associated exploiter (NPFW) communities also differ (Cook
(a)
& Rasplus, 2003). We conducted the first dedicated study of
NPFW community composition for a fig from Ficus section
Malvanthera, an Australasian radiation of figs. We found that
the NPFW community differed greatly from those in studies
on other continents, but that, as on other continents, the main
impact of exploiters was to reduce fig male reproductive
function by decreasing pollinator offspring production.
Our focal species, F. obliqua, has a community dominated
by NPFWs from just a single subfamily of fig wasps, the
Sycoryctinae (see Tables 1 and 3). The situation appears
similar in F. rubiginosa, the only other malvantheran fig in
which parasites have been studied to date (Cook & Power,
1996; Dunn et al., 2008), although its parasite community
composition has yet to be described in detail (but see
Segar, 2011).
Overall, our well-sampled F. obliqua NPFW community
differs substantially from NPFW communities on New World
section Americana figs, which belong to the same Ficus subgenus (Urostigma). The Americana communities are dominated in terms of numbers of both species and individuals by
wasps from subfamily Sycophaginae (West et al., 1996; Pereira
et al., 2000) and have no sycoryctines. In contrast, F. obliqua
is dominated by sycoryctines and has only two species (Eukobelea sp. and Pseudidarnes sp.) of sycophagines, which make
up only 13% of all NPFW individuals. The subfamilial composition of the F. obliqua NPFW community is more similar to
communities from African and Asian Urostigma figs (Compton
et al., 1994; Chen et al., 1999; Xiao et al., 2010). However,
these communities include another subfamily, Otitesellinae,
which is absent from malvantheran figs (Bouček, 1988).
Detailed regional fig wasp surveys show that sycoryctines
also account for a significant component of NPFW species
diversity in Africa (van Noort & Compton, 1999; van Noort,
2004). In a survey of nine African fig species, van Noort and
Compton (1999) found that 37% of all fig wasp species were
sycoryctines (with 3.6 species per host fig), while the next
most common subfamily represented only 18% of all species
(b)
Fig. 1. Scatter plots of model fitted values against the number of sycoryctines per syconium for Ficus obliqua. Fitted values result from linear
mixed models with the fixed explanatory variables, sycoryctine numbers and syconium diameter, and the random explanatory variable crop. (a) The
negative association between pollinators and sycoryctines (figs: 96, crops: 12, t = −3.659, P < 0.001) remained after controlling for the fig
diameter and crop. (b) Sycoryctine number did not explain a significant amount of the variance in pollinator number (figs: 90, crops: 12, t = 0.062,
P = 0.951) after controlling for diameter and crop. See Table 4 for further details of these relationships.
2012 The Authors
Ecological Entomology 2012 The Royal Entomological Society, Ecological Entomology, 37, 342–349
Segar and Cook exploiters decrease fig male function
(1.7 species per host). Consequently, the subfamily Sycoryctinae is likely an important component of Old World fig wasp
communities in general. Indeed, many Ficus species host multiple sycoryctine species, with recent reports of an average of
2.7 species per Ficus host in Africa (McLeish et al., 2010)
and a conservative average of 1.9 in Asia and Australasia
(Segar et al., 2012). Although sycoryctine abundance can vary
dramatically both within and between crops (Cook & Power,
1996; Dunn et al., 2008), in a given crop sycoryctines can
account for up to 50% of all fig wasps reared (S. van Noort,
pers. comm). This high abundance means they are an important
source of pollinator mortality in some syconia.
Sycoryctine wasps accounted for 84% of all NPFWs sampled from F. obliqua and we explored their effects on pollinator and seed production, which represent fig tree male
and female reproductive function. These wasps, especially
Sycoscapter, have a significant negative effect on pollinator numbers, but little or no significant effect on seeds
(Table 4). The statistical effects also decrease across species
(Sycoscapter > Philotrypesis) in line with their decreasing
abundance. It is largely wasps from the genus Sycoscapter
driving the negative impact of sycoryctines on pollinators. Previous authors (e.g. Bronstein, 1991; Cook & Power, 1996)
have also noted the difficulties of detecting statistical effects
of NPFWs with low abundance, especially when there are other
uncontrolled variables.
We interpret this correlation to mean that at least Sycoscapter, and probably also Philotrypesis, wasps are parasitoids
or lethal inquilines of pollinating wasps, i.e. they usurp the
galls of pollinator larvae and kill them in the process. Nevertheless, we cannot entirely rule out alternative explanations,
such as intense competition for flowers between sycoryctines
and pollinators (see West & Herre, 1994). However, we support the widely accepted view of the larval biology of wasps
in these genera and there is direct evidence for the parasitoid
habit in one Sycoscapter species (Tzeng et al., 2008), the lethal
inquiline habit in two Philotrypesis species (Kuttamathiathu,
1959; Abdurahiman & Joseph, 1978; Bouček, 1988) and indirect evidence for the hyper-parasitoid habit in Watshamiella
(Compton et al., 2009) from other figs. Evidence from manipulation experiments further shows that the sycoryctine wasp
Apocrypta guineesis Grandi has a strong negative impact on
pollinator numbers in Ficus sur Forsk (Compton & Robertson,
1988).
There is also considerable indirect evidence supporting the
idea that most Sycoscapter and Philotrypesis species are parasitoids or inquilines in the galls of other fig wasps, rather than
making their own galls. For example, to our knowledge they
are only found in the pollinated male syconia of dioecious fig
species (Henderson, 1982; Abdurahiman, 1986; Bouček, 1988)
and not the seed-producing female syconia, which contain no
pollinator larvae. This is also consistent with our observations
that wasps of both species lay their eggs a considerable time
after the pollinators have laid their eggs, while known gallmakers tend to attack very young fig fruits before, or about
the same time, as the pollinators (Cruaud et al., 2011b).
In our study, sycoryctines and pollinators were the only
wasp occupants in over 50% of all F. obliqua syconia, but
347
sycoryctines were never found without pollinators, and appear
to use pollinator galls as their primary or only hosts. Our
new results therefore provide evidence that the sycoryctines
associated with F. obliqua are indeed likely to be inquilines
or parasitoids of the pollinators. They have limited impact on
seed production, even though far more seeds than pollinators
are accessible to sycoryctine wasps laying eggs through the
syconium wall in the closely related fig F. rubiginosa (AlBeidh et al., 2012). The weak, negative statistical association
of Sycoscapter with seeds may even be a by-product of their
preferential attack of pollinators in the outer seed layer rather
than inner ovules (Dunn et al., 2008).
Some studies on African and neotropical sycoryctines have
also detected a negative trade-off with pollinator offspring,
but not with seeds (West et al., 1996; Kerdelhué et al., 2000;
Weiblen et al., 2001), again stressing that the costs fall on
fig male function. West et al. (1996) concluded that this pattern was due to competition between pollinators and wasps
from the neotropical genus Critogaster for ovule space in figs
from the section Pharmacosycea. The authors observed Critogaster wasps ovipositing at the same time as pollinators and
therefore concluded that they were galling wasps. However,
recent phylogenetic work suggests that Critogaster may not
be a true member of the sycoryctine clade and could represent a separate colonisation of figs in South America (Segar
et al., 2012). More detailed ecological and phylogenetic studies are now required to confirm the role of Critogaster and the
evolutionary history of the subfamily Sycoryctinae.
Above, we have shown how the dominant subfamily of
exploiters impacts upon pollinators and seeds in an endemic
Australasian fig species. However, we also found wasps
from several other taxa (Table 2). Apart from Eukobelea,
sycophagine wasps occurring in low numbers, these other
wasps are all much larger than the pollinators or the common
parasite taxa. They develop in large galls emanating from
syconium wall tissue and are all relatively rare (Table 3). Even
when they do occur, there are usually only a few individuals
per syconium. Large wasps like these seem to occur as rare
members of most fig wasp communities and can sometimes
prevent abortion of unpollinated syconia or decrease seed or
pollinator production by draining resources (Compton, 1993;
West & Herre, 1994; Peng et al., 2010). However, their effects
could be more complex at the syconium level if the presence of
large galls leads to the plant directing extra resources to these
syconia. This phenomenon is known for cynipid wasp galls on
dandelions (Bagatto et al., 1995) and would be a valuable line
of future study on figs. However, these are only rare species
and, overall, we find that while the dominant exploiter taxa
differ greatly across continents, the main cost is consistently
to fig male function (pollinator offspring production).
Acknowledgements
We would like to thank Teresa Bradley, Susie Joslin, Karl
Davey, Sarah West and Laura Chamberlain for assistance with
field sampling and dissection of syconia. We are grateful
to Derek Dunn, Lizzie Jones, Simon van Noort, and an
2012 The Authors
Ecological Entomology 2012 The Royal Entomological Society, Ecological Entomology, 37, 342–349
348
Simon T. Segar and James M. Cook
anonymous referee for comments on an earlier version of this
manuscript. We thank NERC and the University of Reading
for supporting this research.
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Accepted 30 May 2012
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