Plant Phenology and Absence of Sex-Biased Gall Attack
on Three Species of Baccharis
Mário M. Espı́rito-Santo1, Frederico S. Neves1,2, G. Wilson Fernandes2, Jhonathan O. Silva3*
1 Departamento de Biologia Geral, Centro de Ciências Biológicas e da Saúde, Universidade Estadual de Montes Claros, Montes Claros, Minas Gerais, Brazil, 2 Ecologia
Evolutiva & Biodiversidade/DBG. ICB/Universidade Federal de Minas Gerais, Belo Horizonte, Minas Gerais, Brazil, 3 Departamento de Ecologia, Instituto de Ciências
Biológicas, Universidade de Brası́lia, Brası́lia, Distrito Federal, Brazil
Abstract
Background: Dioecy represents a source of variation in plant quality to herbivores due to sexual differences in intensity and
timing of resource allocation to growth, defense and reproduction. Male plants have higher growth rates and should be
more susceptible to herbivores than females, due to a lower investment in defense and reproduction.
Methodology/Principal Findings: We compared resource investment to growth and reproduction and its consequences to
herbivore attack on three Baccharis species along one year (B. dracunculifolia, B. ramosissima, and B. concinna). Phenological
patterns presented by the three species of Baccharis were quite different over time, but the number of fourth-level shoots
and plant growth rate did not differ between sexes in any studied species. Intersexual difference in reproductive investment
was only observed for B. concinna, with female individuals supporting higher inflorescence density than male individuals
throughout the year. Gall abundance on the three Baccharis species was not influenced by plant sex. However, all plant
traits evaluated here positively influenced the gall abundance on B. concinna, whereas only the number of fourth-level
shoots positively influenced gall abundance on B. ramosissima and B. dracunculifolia.
Conclusions/Significance: The absence of differential reproductive allocation may have contributed to similar growth and
shoot production between the sexes, with bottom-up effects resulting in gender similarities in gall abundance patterns. The
number of fourth-level shoots, an indicator of meristem availability to herbivores, was the most important driver of the
abundance of the galling insects regardless of host plant gender or species. Albeit the absence of intersexual variation in
insect gall abundance is uncommon in the literature, the detailed study of the exceptions may bring more light to
understand the mechanisms and processes behind such trend.
Citation: Espı́rito-Santo MM, Neves FS, Fernandes GW, Silva JO (2012) Plant Phenology and Absence of Sex-Biased Gall Attack on Three Species of Baccharis. PLoS
ONE 7(10): e46896. doi:10.1371/journal.pone.0046896
Editor: Minna-Maarit Kytöviita, Jyväskylä University, Finland
Received March 13, 2012; Accepted September 10, 2012; Published October 4, 2012
Copyright: ß 2012 Espı́rito-Santo et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits
unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Funding: This study was supported by Fundação de Amparo à Pesquisa de Minas Gerais (Fapemig) and the Postgraduate Program in Ecologia, Conservação e
Manejo da Vida Silvestre of the Universidade Federal de Minas Gerais (UFMG). The funders had no role in study design, data collection and analysis, decision to
publish, or preparation of the manuscript.
Competing Interests: The authors have declared that no competing interests exist.
* E-mail: jhonathanos@gmail.com
to intersexual differences in resource allocation, male plants are
more susceptible to herbivore attack than females (the sex-biased
herbivory hypothesis) [7–11]. Several studies conducted mainly in
temperate regions have detected higher herbivory levels on male
plants. However, a male-biased herbivore attack has not been
corroborated in some recent studies in tropical systems involving
Baccharis shrubs [9,12,13]. Baccharis (Asteraceae) is a genus with
over 500 species distributed from United States to Argentina. All
species are perennial and dioecious shrubs, except for Baccharis
monoica [14]. Baccharis likely supports the richest galling-inducing
insects fauna studied so far in the Neotropics, with 121 galls species
on 40 host plant species [15]. With such a rich community in
which the gall-inducing insects belong to several different taxa, the
system comprised of Baccharis species and their gall-inducing
insects provides an ideal scenario to test for plant sexual differences
on intensity and timing of resource allocation and herbivory
attack.
Gall-inducing insects are highly specialized to their host and
each species attacks only a single plant organ [16–18]. Galling
Introduction
Plants have limited resources to invest in growth, reproduction
and defense against herbivores [1]. In general, resource demand
for these three processes cannot be held simultaneously, due to a
tradeoff in resource allocation among these different physiological
processes [1–3]. Differential resource allocation produces changes
in plant traits (e.g. architecture, growth, concentration of carbonbased defensive compounds), that can extend its effects on upper
trophic levels [2,4,5]. Fast-growing species or sexes (within
dioecious species; e.g., male plants) are expected to invest less in
chemical and/or structural defenses [1]. On the other hand, their
counterparts usually invest a higher amount of nutrients in
reproduction, and the consequent decrease in nitrogen levels limits
the production of new leaves. Thus, female plants or slow-growing
species are expected to protect their limited growth potential
against tissue loss via herbivory [1,4,6].
Plant sex was explored as a source of variation in quality to
herbivores in many studies with dioecious species. In general, due
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Sex-Biased Herbivory and Phenology on Baccharis
galling herbivore found on B. dracunculifolia, whereas Baccharopelma
concinnae Burckhardt dominates the galling abundance on B. concinna, the same occurring for Baccharopelma brasiliensis Burckhardt
on B. ramosissima (see [15,41] for details).
insects are able to manipulate plant chemical defenses [19,20], but
are strongly influenced by the production of new tissues
(meristems) and/or faster growth or vigorous modules of their
hosts [21–25]. Thus, attack by these insects can be synchronized to
periods in which there is an increased production of highly
nutritious young tissues or fast plant growth [26–27]. Due to their
finely-tuned interaction with the host plants, galling insects provide
excellent opportunities to evaluate the influence of bottom-up
forces on herbivores [28,29]. In a recent meta-analysis on gender
effects on plant-herbivore interactions, Cornelissen & Stiling [8]
highlighted the prevalence of galling insects as subjects of sexbiased herbivory studies, representing almost 35% of the
independent comparisons reviewed. Moreover, these authors
found that the abundances of folivores and galling insects were
more strongly influenced by plant sex than other feeding guilds,
and intersexual differences in plant morphological, phenological
and/or nutritional characteristics might be responsible for this
result.
Plant vegetative and reproductive phenology can be influenced
by several abiotic (water availability, photoperiod and wind speed,
among others) and biotic (presence of herbivores, pollinators and
seed dispersers) factors [30–32]. In dioecious species, phenology is
related to patterns of vegetative and sexual development [7–9,33–
36]. Furthermore, trade-offs in biomass allocation between
reproduction and growth can lead to temporal variations in
vegetative investment in both plant sexes, affecting resource
availability for their associated herbivores [8,36,37]. Male plants
usually present a higher investment in flower production early in
the reproductive season, whereas females divert most of their
energy to sustain fruit maturation later in the reproductive season
[33,38]. If a trade-off between growth and reproduction occurs, it
is expected that males would suffer higher galling attack later in
the reproductive season, the contrary being true for female plants.
In this way, studies regarding plant intersexual differences and
herbivory should consider resource investment across the entire
growing and reproductive seasons due to the possible contrasting
phenologies between male and female hosts (e.g., [10,33,35,39]).
This study aimed to explore the relationships between galling
insect attack and dioecy on three Baccharis species, mediated by
investment in number of shoots, relative shoot growth rate and
number of inflorescences. We assessed resource allocation to
reproduction and growth between male and female plants along
one year. The following questions were asked: i) Does resource
allocation to reproductive and vegetative functions differ between
male and female plants and, if so, does differential resource
allocation provoke differences in gall attack between sexes? ii) Are
there temporal differences in vegetative and reproductive investment between sexes and, if so, how such variations affect gall
abundance across time?
Study Sites
The populations of B. dracunculifolia and B. ramosissima were
located in the Campus of the Universidade Federal de Minas
Gerais, Belo Horizonte, Brazil (19u 309 S, 44u 009 W), at 805 m
above sea level. The average temperature of the study site varies
from 18uC to 20uC, and the average annual precipitation is
1,500 mm [12]. The vegetation is extremely heterogeneous and
disturbed, composed of native, introduced, ornamental and fruitbearing species. The adjacent native vegetation contains dry forest
and cerrado (savanna) species [42]. The plants were all located in a
3 ha area at an early successional stage, dominated by
B. dracunculifolia, B. ramosissima, grasses and herbaceous and
shrubby leguminous species [43].
The population of B. concinna was situated at Serra do Cipó, in
the Espinhaço Mountain Chain, approximately 100 km from Belo
Horizonte. This region is characterized by quartzitic soils covered
by rupestrian fields, highly xerophytic vegetation with predominance of herbs and shrubs [44]. The study site was located at
1,250 m above the sea level (19u 179 S, 43u 359 W), inside a private
protected area (Reserva Particular Vellozia). The climate is similar
to the observed in Belo Horizonte, with average annual
precipitation of approximately 1,500 mm and average temperature between 17.4–19.8uC [45].
Samples
Thirty individuals (15 male and 15 female) of each Baccharis
species were arbitrarily marked in field. Plant sex was determined
by analysis of floral morphology (see [22] for details). We
arbitrarily selected three secondary branches on each plant, which
were tagged with thin, colored adhesive tape placed on their
terminal 15 cm, and shoot length was measured every three weeks.
Shoot relative growth rate was calculated as: [(Loge final length –
Loge initial length)/(time final-time initial)] for each measurement
date. Total number of inflorescences was counted for all marked
shoots and inflorescence density was calculated by shoot centimeter. Both shoot growth and inflorescence densities were averaged
per plant for statistical analyses. The number of fourth-level shoots
was counted for each individual at the same intervals during one
year (totaling 18 repeated measures). Fourth-level shoots are
usually young and possess many sprouting leaves, thus this variable
may be considered as an indication of the amount of active
meristems in a given individual. Higher-level shoots (e.g., fifth and
sixth level) are encountered only in few architecturally complex
individuals and it would not be helpful to indicate meristem
number for most of the plants sampled in this study [22]. In
B. dracunculifolia and B. concinna, phenological changes were
recorded from May 2001 to May 2002, while in B. ramosissima,
phenology was recorded from October 2001 to October 2002. In
each sampling date, all live galls found on plants were counted
without removal or marking. Thus, the same galls could have been
occasionally counted during successive samplings. Galls were
considered alive when exit holes from either the gall-inducer or
parasitoids were absent from external walls. The present study
considered only insect-induced galls [15].
Materials and Methods
Study System
Baccharis dracunculifolia DC is a widespread dioecious perennial
shrub ranging from 2 to 3 m in height and is found in Brazil,
Argentina, Uruguay, Paraguay and Bolivia [40]. Baccharis
ramosissima Gardner reaches from 2 to 4 m in height and occurs
predominantly in Minas Gerais state, Brazil [40]. Finally, Baccharis
concinna Barroso is usually 1–2 m tall and is endemic to Serra do
Cipó, Minas Gerais, Brazil [40]. Fernandes et al. [15] recorded 17,
15, and 11 different gall-inducing species on B. dracunculifolia,
B. concinna, and B. ramosissima, respectively. Each Baccharis species
support a monophagous species of gall-inducing Baccharopelma [41].
Baccharopelma dracunculiafoliae Burckhardt is the most common
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Analysis
To examine the intersexual differences in the number of fourthlevel shoot, relative growth rate and inflorescence density along
one year, we adjusted linear mixed-effect models (LME) for each
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Sex-Biased Herbivory and Phenology on Baccharis
Figure 1. Average number of fourth-level shoots (mean ± s.e.) in male and female individuals of (a) Baccharis dracunculifolia, (b)
B. concinna and (c) B. ramosissima. Fourth-level shoots were counted every three weeks during one year.
doi:10.1371/journal.pone.0046896.g001
interaction between sex and date were used as explanatory
variables (fixed effects), whereas the resulting groups per plant
were treated as random effects (date by plant identity).
To verify the effects of the date, sex and plant traits (number of
fourth-level shoot, relative growth rate and inflorescence density)
on gall abundance on the three Baccharis species, LMEs were also
adjusted as described for the previous models. For these models,
the response variables were log-transformed to meet normality.
Minimal adequate models were adjusted with the removal of the
non-significant terms. All model and analyses were conducted
of these response variables for each Baccharis species [46]. These
analyses were employed because the data were obtained repeatedly in the same plants during subsequent intervals, and the
temporal autocorrelation generated by consecutive counting
violates the assumption of sampling independence. Assuming
independence when it is not true would inflate the error degrees of
freedom and could lead to spurious significance (Type I error)
[46]. To overcome this problem, the data were grouped by plant
and the error variances were calculated for each different group.
In this case, the response is not the individual measure, but the
sequence of measures in an individual [46]. Plant sex, date and the
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Sex-Biased Herbivory and Phenology on Baccharis
Table 1. ANOVA of the minimal linear mixed-effects (LME) models to evaluate the effects of plant sex on the number of shoots,
relative growth rate and inflorescence density in three species of Baccharis.
B. dracunculifolia
Source
B. concinna
B. ramosissima
Df
F
p
df
F
p
df
F
P
1, 479
2478.9
,0.0001
1, 479
2886.4
Number of shoots
,0.0001
1, 478
1395.7
,0.0001
Date
Intercept
ns
ns
1, 478
14.0
,0.0005
Plant sex
ns
ns
ns
Date6Plant sex
ns
ns
ns
Relative shoot growth rate
,0.0001
1, 478
143.1
,0.0001
1, 478
239.3
,0.0001
Date
Intercept
1, 479
589.3
ns
1, 478
5.32
,0.05
1, 478
72.8
,0.0001
Plant sex
ns
ns
ns
Date6Plant sex
ns
ns
ns
Inflorescence density
Intercept
1, 477
55.0
,0.0001
Date
1, 477
107.8
,0.0001
Plant sex
Date6Plant sex
1, 477
4.22
1, 477
416.1
,0.0001
1, 478
38.7
ns
1, 478
83.5
,0.0001
,0.0001
ns
1, 28
29.4
,0.0001
ns
,0.05
1, 477
4.31
,0.05
ns
doi:10.1371/journal.pone.0046896.t001
using the software R2.11 [47]. All data are given as average 6
standard error.
peak the opposite trend was detected (Figure 3a). Baccharis concinna
presented inflorescences during the entire year, but the temporal
pattern differed between sexes. For female plants, inflorescence
density was slightly higher during the dry season, whereas males
showed a peak in inflorescence production in the middle of the
rainy season in January. As a whole, inflorescence density was
constantly higher in female plants in this species (Table 1,
Figure 3b). On the other hand, inflorescence density in
B. ramosissima varied greatly during the year but did not differ
between sexes (Table 1). For this species, inflorescences were
produced only once a year, in the middle of the dry season (AprilSeptember) (Figure 3c). In general, the only plant trait considered
in the present study that differed between sexes was the
inflorescence density in B. concinna.
Results
Resource Allocation to Growth and Reproduction
The phenological patterns exhibited by the three species of
Baccharis were quite different (Figures 1, 2, 3). The number of
fourth-level shoots varied significantly during the study period only
for B. ramosissima, increasing after the end of the rainy season in
March. Shoot number did not differ between male and female
plants for all three species (Table 1, Figures. 1a, b, c). Although no
significant temporal differences were observed for B. dracunculifolia,
there was a peak on shoot growth for this species in NovemberDecember, at the beginning of the rainy season (Figure 2a). On the
other hand, relative shoot growth rate varied significantly along
the year for B. concinna and B. ramosissima. In B.concinna, higher
growth occurred from November to February (rainy season)
declining in March, with an additional peak in May (at the
beginning of the dry season). The lowest growth rate was observed
between July and October (dry season, Figure 2b). For
B. ramosissima, a similar pattern was verified: higher shoot growth
rate was observed during the rainy season (November-February),
followed by a steady decline in March reaching almost zero
between July and August (dry season, Figure 2c). Shoot growth
rates were statistically similar between sexes for all species during
this study (Table 1, Figures 2a, b, c).
The pattern of inflorescence production showed marked
contrasts between the three Baccharis species (Figures 3 a, b, c).
Inflorescence density varied significantly along the year for
Baccharis dracunculifolia (Table 1), with two peaks of flowering: in
the middle of the rainy season (December-January) and in the
beginning of the dry season (April-May). Although the total
inflorescence density did not differ between sexes, the temporal
pattern of reproductive investment was sexually distinct for this
species. In the first flowering peak, we observed a higher
inflorescence density for the female gender, whereas in the second
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Sex-mediated Herbivore Attack
Baccharis dracunculifolia supported the highest richness (14 species)
and abundance (20,327 counts) of insect galls among the studied
host species. Both B. concinna and B. ramosissima showed 10 galling
morphospecies each. Baccharis concinna individuals presented a total
abundance of 8,353 insect galls whereas B. ramosissima supported
5,410 insect galls during the study period. Most of the galls were
induced by psyllids belonging to the genus Baccharopelma (Hemiptera: Psyllidae). Baccharopelma dracunculiafoliae induced 80% of the
galls on B. dracunculifolia, whereas Baccharopelma concinnae induced
65% of the galls on B. concinna, the same occurring for
Baccharopelma brasiliensis on B. ramosissima (70% of the galls). The
galls induced by the other insects had a very low relative
abundance on the three Baccharis species.
Gall abundance showed different patterns of temporal
variation for each Baccharis species (Table 2, Figure 4). Although
no statistically significant difference in gall abundance was
detected on B. dracunculifolia along time (Table 2), a bimodal
pattern of attack was observed, with peaks in the transition
between the rainy and dry season (April-June) and in the
beginning of the rainy season (December) (Figure 4a). For B.
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Sex-Biased Herbivory and Phenology on Baccharis
Figure 2. Average shoot relative growth rates (cm.cm21.day21) in male and female individuals of (a) Baccharis dracunculifolia, (b)
B. concinna and (c) B. ramosissima. Shoot measurements were performed every three weeks during one year (mean 6 s.e.).
doi:10.1371/journal.pone.0046896.g002
similar between male and female individuals in all host species
during the entire study period (Figure 4). Gall abundance
correlated positively with the number of fourth-level shoots on
the three species of Baccharis (Table 2). Relative shoot growth rate
also influenced positively the gall number on B. dracunculifolia and
B. concinna (Table 2). Indeed, a higher gall abundance was
recorded in the periods of greatest relative growth for all host
species, although no significant relationship was detected in
B. ramosissima (Table 2, Figures 2 and 4). Inflorescence density
only affected positively the gall abundance on B. concinna, but this
effect did not differ between sexes.
concinna, gall abundance varied significantly along time (Table 2)
and three peaks were recorded: in the middle of the dry season
(July-August 2001), at the beginning (December 2001), and at
the end (April 2002) of the rainy season. Significant temporal
variations were also recorded for B. ramosissima, and the highest
abundance of insect galls was observed in the rainy season
(October-January) (Figure 4c).
Gall abundance did not differ between sexes in any of the three
species of Baccharis (Table 2, Figure 4), not even in B. concinna
which presented strong intersexual differences in inflorescence
production. Also, the temporal pattern of gall attack was quite
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Sex-Biased Herbivory and Phenology on Baccharis
Figure 3. Average density of inflorescences (mean ± s.e.) in male and female individuals of (a) Baccharis dracunculifolia, (b)
B. concinna and (c) B. ramosissima. Inflorescences were counted every three weeks during one year.
doi:10.1371/journal.pone.0046896.g003
growth and reproduction between sexes. In dioecious species, male
and female individuals have different reproductive functions (i.e.,
pollen donation vs. seed production and fruit maturation) and, in
many cases, fleshy fruits and nutrient-rich seed structures are
energy-costly [38,50–52], thus leading to strong asymmetries in
reproductive investment between sexes. In Baccharis, inflorescences
are small and comparable in size between male and female
individuals of all three species, and seeds are tiny and winddispersed [53]. Thus, female plants probably do not have a
Discussion
Resource Allocation to Growth and Reproduction
Plant sex does not seem to be an important source of variation
in phenology and gall attack on Baccharis, corroborating previous
studies in this speciose genus [9,12,13,33,48,49]. In spite of some
intersexual differences in inflorescence production patterns in
B. dracunculifolia and B. concinna, shoot number and growth rates
were similar between genders in all three species. Thus, we found
little support for the existence of differential resource allocation to
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Sex-Biased Herbivory and Phenology on Baccharis
Table 2. ANOVA of the minimal linear mixed-effects (LME) models to evaluate the effects of date, sex and plant traits on gall
abundance in three species of Baccharis. Non-significant terms were deleted from complete models through stepwise removal.
B. dracunculifolia
Source
df
F
Intercept
1, 476
502.71
B. concinna
p
Df
B. ramosissima
F
P
df
F
P
,0.0001
1, 476
434.8
,0.0001
1, 478
274.0
,0.0001
Date
ns
1, 476
7.39
,0.01
1, 478
20.5
,0.0001
Plant sex
ns
ns
Date6Plant sex
ns
ns
Number of shoots
1, 476
72.3
Relative shoot growth rate
1, 476
13.4
Inflorescence density
,0.0001
1, 476
21.6
,0.0001
ns
ns
1, 478
5.84
,0.05
,0.0001
1, 476
6.15
,0.05
ns
ns
1, 476
7.23
,0.01
ns
doi:10.1371/journal.pone.0046896.t002
reproductive investment greater enough than males to produce
differences in meristem number and plant growth.
In the case of B. concinna, females indeed produced a
significantly higher number of inflorescences than males. However, this species is wind-pollinated [40] and has the smallest
inflorescences among the three species studied here. This
differential investment did not affect plant growth and shoot
production, which remained roughly similar for both sexes during
the entire year, suggesting the absence of trade-offs in this species
(i.e., male B. concinna individuals had both highest growth rate and
inflorescence density early in the rainy season, in DecemberFebruary). Similarly, Antos and Allen [52] did not find a
significant correlation between reproductive effort and growth in
either sex of the shrub Oemleria cerasiformis (Rosaceae). Temporal
variations in inflorescence production may represent a response to
other factors that regulate reproductive investment (e.g. availability of light and soil nutrients and moisture) [38,50,52]. Thus, the
small wind-pollinated inflorescences of B. concinna are likely
relatively inexpensive in terms of resource allocation and
affordable throughout the year for both genders.
For B. dracunculifolia, the timing of reproduction was different
between sexes. Although male plants started reproduction earlier,
females bloomed in January, in the peak of the rainy season, and
this massive investment probably limited their inflorescence
production for the rest of the season. The low reproductive male
investment in January may have been caused by their higher
resource allocation to growth in the previous month, saving energy
for inflorescence production later in the season (see Figure 2a).
The pattern detected here was opposite to the observed by
Espı́rito-Santo et al. [33], who reported a higher male investment
early in the season related to pollinator attraction, and a late
female reproductive investment due to seed maturation (especially
in June). However, this previous study was much more limited in
time (March-June), and there were strong inter-annual variations
in reproductive investment of B. dracunculifolia (i.e., no inflorescences in June in the present study). Thus, our results suggest that
sexual differences in phenology may not be determined only by
male and female reproductive functions (pollen donation vs. seed
production and fruit maturation), and are also affected by abiotic
(e.g., water availability) and biotic (e.g., interspecific competition
for pollinators) pressures. In this way, long-term studies are
necessary to detect temporal patterns in reproductive investment
in dioecious plants.
For the studied Baccharis species, the majority of changes in
phenological events was not related to plant sex, but varied
between species and is likely associated with resource availability
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in each plant population. In B. dracunculifolia and B. concinna, the
higher number of fourth-level shoots and relative shoot growth
rate occurred during the rainy season. In contrast, B. ramosissima
produced new branches and flowers in the dry season, when shoot
growth rate was reduced. Thus, this species may have not been
able to sustain growth and reproduction simultaneously, especially
in periods of resource scarcity. In B. ramosissima, inflorescences of
both sexes are similar in size and pollination is performed by social
bees [40]. Blooming in the middle of the dry season is not unusual
in some tropical environments, since the low air humidity
contributes to increase nectar concentration and leaf fall may
improve flower visibility by pollinators [54]. In the case of
B. ramosissima, it is likely that this strategy reduces competition for
pollinators with the sympatric B. dracunculifolia. These two species
are very similar in architecture [22] and in inflorescence
morphology. Since B. ramosissima populations are usually much
less dense when co-occurring with B. dracunculifolia (M. M. Espı́ritoSanto, personal observation), it is likely that there was a strong
evolutionary pressure for niche differentiation causing both sexes
of B. ramosissima to reproduce very synchronously during periods of
water scarcity but high pollinator availability.
Sex-mediated Herbivore Attack
The gall abundance on the studied species of Baccharis did not
conform to the pattern predicted by the sex-biased herbivory
hypothesis. On the other hand, this result corroborates several
other studies related to this genus in Brazil [9,12,13,49,55].
Furthermore, the present study involved multiple hosts and galling
species, and closely followed temporal changes in gall abundance
and host resource availability along one year. Therefore, we have
consistent support to reject the male-biased attack prediction of the
sex-biased herbivory hypothesis.
The absence of the gender-related gall attack is explained by the
lack of differences in plant growth rate and meristem availability
(estimated indirectly by the number of fourth-level shoots) between
male and female plants. Indeed, meristem number was already
reported as the most important plant trait driving gall abundance
and species richness across several species of Baccharis [22]. This
assertion is reinforced by the positive relationship between gall
abundance and shoot number and plant growth rate in the present
study. However, other plant traits not evaluated here such as
nutrient content, secondary chemistry and physical defenses can
differ between sexes and affect gall attack (see [8]). Although we
did not quantify plant defenses, there is some evidence that
carbon-based compounds such as tannins are not abundant and
do not vary between sexes in B. dracunculifolia [12,48], but nothing
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Sex-Biased Herbivory and Phenology on Baccharis
Figure 4. Average number of galls (mean ± s.e.) on male and female individuals of (a) Baccharis dracunculifolia, (b) B. concinna and (c)
B. ramosissima. Galls were counted every three weeks during one year.
doi:10.1371/journal.pone.0046896.g004
Gall abundance was influenced by plant phenology, being
mainly affected by temporal variations in shoot growth rates.
Indeed, gall attack was higher mostly during the rainy season,
when shoot growth was more vigorous in all three species.
Although the number of fourth-level shoots was the most
important plant trait affecting gall abundance at the individual
level, statistically significant temporal variations in this variable
were only detected in B. ramosissima. However, shoot production in
this species increased during the dry season and may be related to
flowering, when shoot growth and gall attack were both low. For
is yet known for B. concinna and B. ramosissima. Furthermore, gallinducing insects are capable of manipulating chemical composition, growth rates and developmental patterns of the attacked
plant organ [19,20,56], and are able to overcome chemical and
physical defenses regardless of plant gender. Thus, the similarities
in gall abundance between male and female individuals in this host
genus are likely related to plant vigor and availability of young
tissues for gall induction, but leaf nutrients and defenses deserve
further investigation.
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Sex-Biased Herbivory and Phenology on Baccharis
B. dracunculifolia, other studies detected an increase in the number
of fourth-level shoots and galls in March-April, right before the
second peak of flowering [12,33]. However, such phenological
pattern was only observed for male plants of this species in the
present study, and a higher gall attack did not track shoot number.
Thus, it seems that plant growth rates are more important in
determining temporal variations in gall attack, whereas the
number of fourth-level shoots is responsible for spatial, individual
differences in plant susceptibility.
and temporal changes in gall abundance are synchronized with
resource availability (e.g. young tissues and vigorous growth)
throughout the year. The absence of sex-biased herbivory can be
more frequent than usually reported, since studies that fail to
detect intersexual variation on herbivore attack in other system are
probably underrepresented in the literature.
Acknowledgments
We are very grateful to CF Sperber, CM Jacobi, FAO Silveira, KD Floate,
SP Ribeiro, TG Cornelissen, and two anonymous reviewers for their
valuable suggestions on earlier versions of the manuscript, and to FR
Andrade-Neto, R Pereira and BG Pacheco for field assistance.
Conclusion
Overall, the Baccharis species studied here did not exhibit sexual
dimorphisms on vegetative traits that are usually related to distinct
reproductive functions. The absence of differential reproductive
allocation may have contributed to similar growth and shoot
production between male and female plants. As a bottom-up
consequence, plant gender is a weak predictor, or even an
irrelevant variable influencing gall abundance in this host plant
genus. In spite of that, the plant traits evaluated here are important
drivers of gall attack both in space (between individuals) and time,
Author Contributions
Conceived and designed the experiments: MMES GWF. Performed the
experiments: MMES FSN. Analyzed the data: MMES JOS. Contributed
reagents/materials/analysis tools: JOS MMES. Wrote the paper: MMES
JOS FSN GWF.
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