Biol Invasions (2019) 21:59–66

https://doi.org/10.1007/s10530-018-1803-3 (0123456789().,-volV)
(0123456789().,-volV)

ORIGINAL PAPER

Herbivory can mitigate, but not counteract, the positive

effects of warming on the establishment of the invasive
macrophyte Hydrilla verticillata
Clementina Calvo . Roger P. Mormul . Bruno R. S. Figueiredo .
Eduardo R. Cunha . Sidinei M. Thomaz . Mariana Meerhoff

Received: 26 January 2018 / Accepted: 2 August 2018 / Published online: 9 August 2018
 Springer Nature Switzerland AG 2018

Abstract Hydrilla verticillata is a submerged,
rooted macrophyte native to Asia and Australia, but
currently attains broad distribution across all conti-
nents. Its success as an invasive species depends on the
simultaneous influence of abiotic and biotic factors on
different components of its performance. We con-
ducted a factorial experiment to test the short-term
responses of Hydrilla, present since 2005 in the upper
Parana River (Brazil), to a native herbivore (apple
snail Pomacea canaliculata) and increased water
temperature, using two different spatial arrangements
of macrophyte fragments (one simulating early estab-
lishment phase and other simulating late establishment
Electronic supplementary material The online version of
this article (https://doi.org/10.1007/s10530-018-1803-3) con-
tains supplementary material, which is available to authorized
users.
C. Calvo (&)  M. Meerhoff
Departamento de Ecologı́a y Gestión Ambiental, Centro
Universitario Regional del Este (CURE) - Universidad de
la República (UdelaR), Maldonado, Uruguay
e-mail: clemen.calvo@gmail.com
R. P. Mormul  B. R. S. Figueiredo  E. R. Cunha 
S. M. Thomaz
Núcleo de Pesquisa em Limnologia, Ictiologia e
Aquicultura (Nupélia) - Universidade Estadual de
Maringá (UEM), Maringá, Brazil
M. Meerhoff
Department of Bioscience, Aarhus University, Silkeborg,
Denmark
phase). Temperature, herbivory and plant spatial
arrangement individually, and in some cases through
their interactions, caused changes in the growth likely
indicating impacts for the ecological responses of
Hydrillas establishment. Snail herbivory decreased
plant growth thus exerting biotic resistance, while
higher temperature increased Hydrillas invasiveness.
According to our results and other pieces of evidence,
invasions of Hydrilla might worsen under the future
climate warming scenario, but herbivores might
locally mitigate invasion speed or magnitude.
Keywords Invasion process  Temperature  Spatial
aggregation  Pomacea canaliculata  Grazing 
Aquatic plant
Introduction
Several species of aquatic plants are among the most
problematic invaders (Luque et al. 2014). Herbivores
may increase biotic resistance to invasive plants
through grazing pressure, thus reducing their success-
ful establishment (Coetzee and Hill 2012; Alofs and
Jackson 2014; Ribas et al. 2017). However, the spatial
arrangement of plants (e.g., whether they are closely
or sparsely distributed) may modify the strength of
herbivores effects (Hahn and Orrock 2015). Different
plant spatial arrangements may occur in different
invasion phases. For example, during the early

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establishment phase, fragments of several invasive
macrophytes are usually isolated and biomass is low,
and then, herbivores are less likely to find the
macrophyte fragments. Conversely, in later establish-
ment phases, invasive macrophytes usually form
dense beds, increasing the probability of herbivores
finding and consuming the macrophyte fragments
(e.g., Roberts and Poore 2006). This pattern can result
in a paradox for herbivorys role on plant control,
depending on the balance between the invasive plant
relative biomass and the likelihood of plant finding
and consumption by herbivores.
Climate warming could also alter herbivory
strength (e.g., Lemoine et al. 2014), often leading to
stronger consumer control on resources (e.g., OCon-
nor 2009). However, rising temperatures may inten-
sify both herbivore feeding activity (Heiler et al. 2008)
and also the growth of no native plants (McKee et al.
2002; Li et al. 2017). Thus, under a climate warming
scenario, we would expect opposite effects of these
two processes with unpredicted outcomes, since the
former could strengthen biotic resistance, while the
later could enhance traits related to invasiveness. In
practice, to achieve a successful invasion, growth rate
of the invasive plant species should be faster than the
enhancement of grazing pressure of native herbivores.
Hydrilla verticillata (L.f.) Royle (family Hydrochar-
itaceae, hereafter Hydrilla) is a submerged, rooted
macrophyte native to Asia and Australia, but it
currently attains broad distribution across all conti-
nents, except Antarctica (Langeland 1996; Sousa
2011). Hydrilla has many reproduction strategies,
such as branch fragmentation, and production of
turions, tubers and seeds (Langeland 1996). Plant
fragmentation is one of the main mechanisms allowing
long distance dispersal (Owens et al. 2008). These
vegetative propagules can root into sediment and
rapidly develop a new plant (Cook and Lüönd 1982).
Once established, the monospecific mats can be dense,
leading to strong intra-specific (Wang et al. 2008) and
inter-specific (Mony et al. 2007) competition for
space, nutrients and light. Hydrilla was first recorded
in the Upper Paraná River, Brazil, in 2005, from where
it spread rapidly (Sousa 2011) so far causing the
displacement of native species of macrophytes and
modification of other communities (Sousa et al. 2010),
and problems to navigation and recreation (S.
M. Thomaz, unpublished). Although Hydrilla is now
widespread in the Upper Paraná basin, so far it only
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C. Calvo et al.
forms dense mats in reservoirs, in the river Paraná
main and secondary channels (Sousa 2011), whereas
in floodplain lakes Hydrilla occurs in sparse, low-
biomass temporary mats (Sousa et al. 2010). The
unsuccessful colonization of lakes by Hydrilla is
attributed to the strong herbivory by the abundant and
native apple snail Pomacea spp. (Cruz et al. 2015)
along with other herbivorous and shredder fishes
(Ribas et al. 2017). The effects of individual stressors
including abiotic filters, competition and herbivory on
Hydrilla have been investigated in the Upper Paraná
and in other ecosystems (e.g., Mony et al. 2007; Wu
et al. 2009; Cruz et al. 2015). However, the simulta-
neous influence of abiotic and biotic factors on
Hydrillas performance has received less attention in
ecosystems where it is a recent invader.
Understanding the response of Hydrilla to the
interaction between biotic resistance and climate
warming in different invasion phases could contribute
to predict its successful invasion under different future
scenarios. Thus, we conducted a factorial experiment
to test the short-term responses of Hydrilla to
herbivory and to increased water temperature, using
two different spatial arrangements of macrophyte
fragments (sparse—simulating early establishment
phase; patched—simulating late establishment phase).
Based on the above mentioned observations (Cruz
et al. 2015) and theoretical expectations (OConnor
2009; Yvon-Durocher et al. 2011), our overall hypoth-
esis is that biotic resistance through warming-en-
hanced herbivory has stronger negative effects on
Hydrilla than the potential positive effects of warming
on plants’ performance, and that spatial arrangement
of plants may, although to a lesser extent, attenuate the
impact of herbivory. Thus, we expected that enhanced
snail herbivory at higher temperatures would decrease
net growth and development of key plant structures,
with relatively stronger impacts in the late establish-
ment phase (i.e. patched arrangement) than in the early
phase (i.e. sparse arrangement).
Methods
Experimental design
We conducted a fully factorial microcosm experiment
in August 2014 at an experimental site within the State
University of Maringá (UEM), Brazil. In a 16-days
Herbivory can mitigate, but not counteract, the positive effects of warming on the…
experiment, we analysed the importance of biotic
resistance and climate warming in different phases of
macrophyte invasion. In order to simulate biotic
resistance and climate warming, we used respectively,
a native herbivore (apple snail Pomacea canaliculata,
with presence-absence, hereafter Pomacea) and
manipulated water temperature (ambient temperature
(min–max: 15.5–23.7 C) and increased tempera-
ture & 2.5 C over the ambient). We used different
spatial arrangement of macrophyte fragments to
simulate invasion phases, where sparse macrophyte
beds resembled the early establishment (survival
phase, sensu Blackburn et al. 2011) and dense
macrophyte beds resembled a late establishment
success (reproduction phase, sensu Blackburn et al.
2011) of Hydrilla (leading to eight treatments repli-
cated seven times; total n = 56, Online resource 1).
Macrophyte and snails were collected in the Paraná
River, Brazil (228450 S; 538150 W) and kept separately
in oxygenated tanks. The plants were washed to
remove attached material and apical portions of the
fragments were cut in 20 cm-long pieces, removing all
lateral branches and roots. Macrophyte fragments
were shaken to remove the excess of water and
weighted (fresh biomass).
Experimental units consisted of 40-L rectangular
aquaria (width = 25 cm; length = 35 cm; height = 50
cm) filled with de–chlorinated tap water and contain-
ing 15 fragments of Hydrilla. Each fragment was tied
to a small weight, keeping the fragments attached to
the bottom. Fragments were allocated either in a
sparse distribution across the bottom of the aquarium
(‘‘sparse’’) or grouped together (‘‘patched’’). Her-
bivory was a binary factor, whereas for herbivore
presence, two juveniles of the apple snail P. canalic-
ulata were added in the tanks (initial shell heights:
18.9 ± 1.3 and 13.9 ± 1.0 mm, initial fresh weights:
2.1 ± 0.4 and 0.9 ± 0.1 g; chosen to homogenize
among the individuals collected). Two different water
temperature regimes were considered with means of
21.2 C (‘‘low’’) and of 23.7 C (‘‘high’’) (t test;
P \ 0.001), matching predictions of temperature
increase for the forthcoming decades for the region
(Marengo et al. 2010). The low temperature treatment
was performed inside a greenhouse with transparent
plastic roof, while the high temperature treatment was
performed outdoors. Temperature was left to follow
natural weather variations, differing from experiments
that use a fixed and constant increase in temperature.
61
We measured solar radiation using a digital lux meter
(Instrutherm, model LD-209) and small disparities in
solar radiation reaching the aquaria were equalized in
both sites by putting a thin shade cloth over the
aquaria. Solar radiation ranged from 600 to 19,000 lx,
according to weather conditions of each day.
Oxygen concentration, conductivity, pH and tem-
perature were measured with portable equipment in all
aquaria every day at 6 am and at 3 pm, at minimal and
maximal incident solar radiation (Online resource 1).
After 16 days, the relative growth rates (RGR) of total
macrophyte (i.e. fragments plus new lateral branches
and roots) were calculated as: (ln Xf - ln Xi)/Dt,
where Dt is time in days, and Xf and Xi the final and
initial fresh weight, respectively.
In addition to obtaining plant RGR, we also used as
response variables the number of new lateral branches
and roots, and the dry biomass of the fragments
without branches, the biomass of new branches only
(representing the branches that grew during the
experiment) and the biomass roots. The plant material
was dried in an oven at 60 C until reaching constant
weight, and the main fragments and newly formed
branches and roots were weighted separately. Snail
growth was monitored every 5 days along the exper-
iment and RGR was estimated as for the macrophytes.
Data analysis
A three-way ANOVA was applied to test the effects of
the factors: spatial arrangement (two levels), her-
bivory (two levels), temperature (two levels), and their
interactions, on the RGR of Hydrilla (based on total
biomass), dry weight of fragments (DW), and number
and dry weight of newly formed branches and roots at
the end of the experiment. A two-way ANOVA was
used to test the effects of temperature and macrophyte
arrangement on the RGR of the snails. All response
variables met the assumptions of normality and
heterogeneity of variance (Underwood 1997). Signif-
icant differences among treatments were identified
using Tukey post hoc test.
Results
As we predicted, herbivory significantly and nega-
tively affected Hydrilla’s total biomass RGR, decreas-
ing an average of 40% respective to the no herbivory
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62 C. Calvo et al.

Table 1 Main effects of experimental factors: herbivory (H), weight (DW)), number and biomass (g DW) of lateral branches
temperature (T) and arrangement (A), and their interactions, on and number and biomass (g DW) of roots of H. verticillata
the RGR of total biomass (g d-1), biomass of fragments (g dry
Herbivory Temperature Arrangement H*T T*A H*A H*T*A
F df p F df p F df p F df p F df p

RGR total 21.92 48 *** ns ns ns ns ns ns

Fragments 48.89 48 *** 9.33 48 ** 10.06 48 ** ns ns ns ns
No. branches ns 19.01 48 *** ns ns ns ns ns
Branches 7.56 48 ** 48.28 48 *** ns ns ns ns ns
No. roots 87.75 48 *** ns ns 5.06 48 * ns ns ns
Roots 181.61 48 *** ns ns ns 5.45 48 * ns ns
Statistical results of ANOVA tests are shown, indicating respective F-values and degrees of freedom (df)
ns not significant P [ 0.05; *P \ 0.05; **P \ 0.01; ***P \ 0.001

treatments (see Table 1 for detailed results of ANOVA
tests). Temperature and spatial arrangement of the
fragments had no significant effects on Hydrilla’s
RGR, although plants showed a trend to grow faster in
the sparse distribution and we observed enhanced
plant growth at high temperature (in the absence of
herbivores) (Table 1, Fig. 1a). A marginally signifi-
cant interaction occurred between temperature and
herbivory (P = 0.06, Table 1), with higher tempera-
ture increasing the snails effects on macrophytes when
aggregated.
Biomass of fragments was mostly affected by
herbivory and secondly by temperature and spatial
arrangement. The lowest biomass was observed under
the herbivory treatments (25% mean reduction respec-
tive to the no herbivory treatments; * 0.4 g DW)
(Fig. 1b). Higher temperature also had a negative
effect (15% lower biomass than in the low temperature
treatments; Table 1; Fig. 1b). Spatial arrangement of
fragments also had significant effects, with higher
biomass in the sparse treatments (* 0.2 g DW)
(Table 1; Fig. 1b). No significant interactions
occurred among the main factors.
Similarly to the results obtained for RGR and
biomass of fragments, herbivory reduced the biomass
of Hydrilla’s lateral branches
(0.37 ± 0.02–0.31 ± 0.02 g DW; Table 1), but not
branches number. Both the number and biomass of
new branches were boosted in the high temperature
treatments (Table 1; Fig. 1c, d; the number of new
branches increased almost 30% and the biomass
almost doubled). Spatial arrangement did not affect
branches at all (neither biomass nor number). There
was no significant interaction among factors for these
response variables (Table 1).
Both the number and biomass of Hydrillas roots
were strongly and negatively affected by herbivory,
with some minor interactive effects of temperature and
spatial arrangement for number and biomass respec-
tively (Table 1; Fig. 1e, f).
Discussion
In this short-term mesocosm experiment we demon-
strate that, despite decreasing Hydrilla’s growth,
snails were not able to fully prevent its establishment,
since plant growth was positive and formation of new
branches and roots occurred even in treatments subject
to herbivory. On the other hand, the positive effect of
warming on macrophytes was indicated by a remark-
able promotion of potential propagules (lateral
branches). The simultaneous analysis of both factors,
herbivory and temperature, revealed a potential mit-
igation role of Pomacea on the establishment of
Hydrilla under a warmer scenario, but also the
impossibility of stopping the colonization by detached
fragments.
Grazing-driven macrophyte fragmentation might
enhance the dispersion of Hydrilla in the wild
(Pieczynska 2003; Ribas et al. 2017), potentially
complementing the colonization by specialized
organs, such as turions and seeds (Barrat-Segretain
et al. 1998; Riis and Sand-Jensen 2006). When in a

123
Herbivory can mitigate, but not counteract, the positive effects of warming on the… 63

Fig. 1 Relative growth rate (RGR, g d-1) of total macrophyte
biomass (g) (a), final biomass (g dry weight) of the fragments (b),
number and biomass (DW g) of new branches grown during the
experiment (c and d, respectively) and number and biomass (DW
g) of roots grown during the experiment (e and f, respectively), in
absence (left) and presence (right) of herbivory by P. canalic-
ulata, under low and high temperatures and with aggregation
treatments (white, sparse, and black, patched). Mean values and
standard errors are shown. Letters indicate significant differences
in Tukey post hoc tests

123
64
fixed location, Hydrilla’s detached fragments usually
allocate biomass to the roots (Thiébaut and Martinez
2015), particularly under low nutrient availability (Yu
et al. 2010). Despite observing this phenomenon, in
our experiment the main effect of herbivory was a
significant reduction in the biomass of all plant
structures analyzed, regardless of differences in mag-
nitude among them. Overall, the relative growth rate
of the total biomass and the biomass of main fragments
(major contributors to total biomass), were lower in
the presence of grazers. The apple snail P. canalicu-
lata, like many other snail species, can consume
significant volumes of plants (including Hydrilla,
Cruz et al. 2015), often affecting plant community
composition (Carlsson et al. 2004; Strayer 2010).
Under high grazing pressure, Hydrilla often decreases
the production of structures such as branches and roots
(Owens et al. 2006), which was also confirmed here.
Similarly, root reduction due to direct grazing could
have important implications in the establishment
phase after Hydrilla’s arrival to novel sites, because
rooted fragments can grow more effectively than non-
rooted ones (Chadwell and Engelhardt 2008). In
addition, likely as a result of direct consumption, P.
canaliculata promoted the occurrence of smaller
vegetative fragments (as seen by Ribas et al. 2017),
which generally have relatively lower chances than
larger fragments of regenerating as a new macrophyte
(Lin et al. 2012). The kind of damage caused by P.
canaliculata on Hydrilla is often wanted by freshwater
managers who often search for potential biological
control agents for invasive macrophytes (Cuda et al.
2011). Within their native range, apple snails seemed
partly effective in reducing (but not prevent totally)
the early growth of Hydrilla, exerting biotic resistance
thus decreasing the invasibility of the habitat.
Without herbivores, we found a trend for a greater
growth rate of the total biomass of Hydrilla under
higher temperatures, despite both temperature treat-
ments covered a range suitable for its growth (Madsen
and Smith 1999). In addition of favoring Hydrilla’s
growth, the most relevant effect of increasing temper-
ature could be an enhanced propagule pressure, as
more and heavier branches were generated. In con-
trast, the growth of the fragments was lower at the high
temperature treatment, which could indicate that
changes in temperature may change the allocation of
biomass by Hydrilla, as seen in other macrophyte
species (Li et al. 2017). Such differential biomass
123
C. Calvo et al.
allocation could suggest possible responses against
environmental changes (Pyankov and Ivanov 2000)
and may have consequences for the invasive process
(Umetsu et al. 2012). Besides promoting branch
development, high temperature can also enhance
branch breaking (Pesacreta 1990), thus promoting
dispersal and colonization due to fast regeneration and
high rates of establishment (Pesacreta 1990; Dong
et al. 2010). Increased temperature also reduced the
negative effects of herbivory on root production (as
indicated by the significant interaction between her-
bivory and temperature; Table 1; Fig. 1e). Therefore,
increasing temperatures in the future could overall
increase the invasiveness of Hydrilla.
The spatial arrangement of Hydrilla in the aquaria
was relevant only for the development of its main
fragments, which performed significantly better at the
sparse treatment that simulated the early establishment
of detached fragments. If there is enough space,
Hydrilla usually elongates its fragments to improve
light acquisition, concentrating its biomass near the
water surface (Madsen and Owens 2000; Sousa et al.
2010). Its high biomass production and elongation
rates (Langeland 1996; Hofstra et al. 1999), are in
occasions faster than those of similar but native
macrophytes (Silveira et al. 2009; Fleming and Dibble
2015). In contrast, the clumping of Hydrilla’s frag-
ments negatively impact the plant growth (Jiang et al.
2010), besides increasing chances of herbivores find-
ing and consuming the plant.
In summary, our results showed evidence that
herbivory, temperature, and with minor importance
plant spatial arrangement, were relevant for the
establishment success of Hydrilla, as they affected at
least one of the response variables (i.e. growth of the
whole macrophyte, growth of main fragments, and
number or weight of new branches and roots). Our
results also indicate that herbivorous snails can
represent biotic resistance in the invasive process of
Hydrilla, particularly in the establishment phase. The
effects could, potentially, mitigate the speed or
magnitude of the colonization of the macrophyte in
certain types of water bodies where snails are abun-
dant. However, due to its many adaptive traits and
competitive abilities, in combination with an
increased propagule pressure due to high temperature
(which enhances invasiveness), invasions of Hydrilla
might overall worsen in the future potentially coun-
teracting the local control of grazers. Warming may
Herbivory can mitigate, but not counteract, the positive effects of warming on the…
also affect native and other non-native species that
coexist with Hydrilla and thus potentially modify the
outcome of this herbivore-plant interaction. Mul-
tispecies experimental studies are therefore needed
to increase the accuracy of predictions and interpret
the implications of our results at the ecosystem level.
Acknowledgements Clementina Calvo acknowledges the
Agencia Nacional de Investigación e Innovación (ANII,
Uruguay) for funding her MSc. We are also grateful to the
State University of Maringá (UEM, Brazil) for supplies and
facilities provided to perform the experiment. Mariana Meerhoff
thanks the support of ANII and PEDECIBA. Roger P. Mormul
and Sidinei M. Thomaz acknowledge the National Council for
Scientific and Technological Development (CNPq) for
providing continuous funding through a Scientific Productivity
grant.
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