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22001166 SOUTHEASTERN NATURALIST 1V5o(4l.) :1658,9 N–6o9. 64
Effects of the Consumption Behavior of Adult Pomacea
maculata and Pomacea paludosa on Vallisneria americana
Dean Monette1, Sharon Ewe1, and Scott H. Markwith2,*
Abstract - Understanding differences in behavioral characteristics between invasive
non-native species and native species is an important step in preventing, managing, and
mitigating environmental impacts. This study examined the differences between adult
life-stage native Pomacea paludosa (Florida Applesnail) and adult non-native Pomacea
maculata (Giant Applesnail) grazing behavior and rates on Vallisneria americana (Tapegrass),
a plant of restoration importance, to assess the potential ecological impact. We used
an experimental design with entire intact specimens of Tapegrass placed in 8 tanks of each
of 3 treatment groups: (1) grazed by Giant Applesnail, (2) grazed by Florida Applesnail, and
(3) control with no snails. Rates of herbivory on, and physical and total biomass damage to,
Tapegrass by Giant Applesnail were 1.8 cm/hr, 2.5cm/hr, and 4.2 cm/hr, respectively. Rates
of herbivory on, and physical and total biomass damage to, Tapegrass by Florida Applesnail
were 0.2 cm/hr, 1.2 cm/hr, and 1.4 cm/hr, respectively. The mean growth rate of Tapegrass
in tanks containing no snails was 0.13 cm/hr. We used one-way ANOVAs and Tukey posthoc
tests to examine statistically significant differences between the 2 gastropod species for
rates of herbivory on (P = 0.006) and total biomass damage to (P = 0.024) Tapegrass. No statistical
difference between the 2 species was found for the physical damage rate (P = 0.18).
Statistical differences were found between controls without snails and Giant Applesnail and
Florida Applesnail, respectively, for herbivory (P = 0.001, P = 0.05), physical damage (P
= 0.007, P = 0.001) and total damage rates (P = 0.001, P = 0.002). The observed grazing
behavior of adult life-stage specimens of the 2 species differed substantially, with Florida
Applesnail grazing along blade edges and Giant Applesnail completely cutting off blades
from their bases. These results also show that Giant Applesnail consumed and removed
more Tapegrass biomass at a faster rate than the native Florida Applesnail. The introduction
of Giant Applesnail, with its greater herbivory and total biomass damage rates over the native
apple snail and behavior that removes leaf blades, may shift competitive interactions
in Tapegrass communities under pressure from non-native plant invaders such as Hydrilla
verticillata (Waterthyme).
Introduction
Invasive non-native species can alter food webs and habitats, displace native
species, reduce diversity, and impair ecosystem function (DiTomaso 2000,
Simberloff and Schmitz 1997). Understanding behavioral characteristics of invasive
non-native species in their new environments and their interactions with
native species are necessary for the development of management strategies that
prevent or mitigate environmental impacts. Information gaps related to interactions
1Affiliate Faculty, Florida Atlantic University, Department of Geosciences, 777 Glades
Road, Boca Raton, FL 33431. 2Florida Atlantic University, Department of Geosciences,
Boca Raton, FL 33431. *Corresponding author - smarkwit@fau.edu.
Manuscript Editor: Julia Cherry
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of native and non-native species at any of the 3 stages of the invasion process, i.e.,
introduction, establishment, and spread (Kolar and Lodge 2001), can be problematic
for successful management.
Pomacea maculata (Perry) (Giant Applesnail), formerly known as P. insularum,
is an aquatic freshwater snail that is native to South America and invasive in Southeast
Asia, Spain, and parts of the United States (EFSA 2014, Hayes et al. 2012,
Yoshida et al. 2014). Giant Applesnail was likely introduced in the United States
in the 1990s (Burlakova et al. 2010, Rawlings et al. 2007), and is now established
throughout the southeastern US (Byers et al. 2013), including the entire state of
Florida. Because the species has clearly entered the established stage of invasion,
managers will require an understanding of their population dynamics, behavior, and
associated ecological impacts in order to control this species.
Giant Applesnail’s full environmental impacts are difficult to estimate, but may
include alteration of littoral and near-shore vegetation communities critical to the
endangered Rostrhamus sociabilis plumbeus (Vieillot) (Everglades Snail Kite), as
well as other migratory water birds and to sport fishing (Aumen and Wetzel 1995,
Havens and Steinman 2013, USACE. 1999). Habitat in the Greater Everglades that
supports the only native Pomacea species in Florida, Pomacea paludosa (Say)
(Florida Applesnail), is now invaded by Giant Applesnail. Within their area of
range overlap within the Greater Everglades, both apple snails utilize Vallisneria
americana Michx. (Tapegrass) as habitat and as a food resource (D. Monette unpubl.
data). Tapegrass communities are also under pressure from competitive interactions
with the invasive plant Hydrilla verticillata (L.f.) Royle (Waterthyme), which has a
competitive advantage under nutrient-enriched conditions (Owens et al. 2008, Van
et al. 1999) that are common to waterways where the snail ranges overlap. Consequently,
studies examining the differences between Florida Applesnail and Giant
Applesnail grazing rates on Tapegrass will provide a better understanding of the
ecological impacts of non-native and native grazers on this ecologically valuable
plant community impacted by multiple threats.
Studies examining food-resource utilization are often designed to capture food
preferences and rates of consumption without understanding where the physical
damage to the plant occurs (Baker et al. 2010, Boland et al. 2008, Morrison and
Hay 2011). Food presentation normally does not include the visual arrangement of
the whole plant structure, but only small pieces or reconstituted plant fragments to
capture food preferences or herbivory rates. The aim of this study was to investigate
Giant Applesnail and Florida Applesnail consumption behavior at the adult life stage
when presented the whole plant of Tapegrass, quantifying vegetation impact resulting
from grazing. We hypothesized that Giant Applesnail would have significantly
greater herbivory rates. The results of this study provide a better understanding of the
impacts of differing grazing behaviors of adult Giant Applesnail and Florida Applesnail
on a plant of restoration importance under controlled conditions that simulate
field environments.
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Methods
Tapegrass plants were harvested completely intact, including belowground biomass
so the specimens could be maintained alive, from Lake Okeechobee Florida
and acclimated for 8 months at Florida Atlantic University Everglades Botanical
Greenhouse. To test consumption behavior, we placed 1 Tapegrass plant with 5
blades in each of 24 ten-gallon (3.8-liter) tanks in the indoor climate-controlled
Biogeography Lab at Florida Atlantic University. The mean total blade length
for Tapegrass plants used in the study was 167 cm (± 34.17 SE). Each tank was
equipped with its own lighting and Tetra-carbon filtration. Lighting was digitally
timed for 12-hour day and night cycle. We filled tanks with dechlorinated water, and
kept them in a climate-controlled facility. To check that the temperature remained
at a constant 23 °C, we recorded the temperature both at the beginning and end of
the study. Tank substrate consisted of crushed coral aragonite sand with grain size
of approximately 2 to 5.5 mm (Garr et al. 2011). Tanks were lined with an opaque
sheet of paper to obstruct direct line of sight between adjacent tanks. We ran all
tanks a week prior to snails being introduced in June 2012. Each Tapegrass plant
was cleaned of any periphyton, detritus, and algae prior to being placed within its
own pot filled with potting soil. We then laid a top layer consisting of crushed coral
aragonite over the soil to maintain surface consistency with the tank and nestled the
Tapegrass pot within the tank substrate so the base of the plant was even with the
top of this coral aragonite substrate layer.
We used wild-caught adult male snails during this study to avoid potential
behavioral effects of captive rearing and egg production. We collected Florida
Applesnail snails from a quarry outside of Jacksonville, FL, and Giant Applesnail
specimens collected from Lake Okeechobee, FL. Snails varied in size, with Florida
Applesnail and Giant Applesnail snails ranging in weight from 14.2 g to 28.9 g
(mean ± SE = 23.5 ± 1.5 g) and 55.6 g to 135.3 g (mean ± SE = 91.9 ± 9.8 g), respectively.
Giant Applesnail is naturally a much larger species that reaches the adult
life-stage at a larger size than Florida Applesnail, and the size ranges used for this
study approximate the adult size ranges of the 2 species, respectively (Darby et al.
2008, Kyle et al. 2009, Youens and Burks 2008). We fed catfish chow to collected
snails (Garr et al. 2011) for ~8 weeks during acclimation in the greenhouse staging
facility to ensure snail specimens were healthy, and then starved them 24 hours
prior to their use in the study.
We used an experimental design with 8 tanks of each of 3 treatment groups (for a
total of 24 tanks): (1) grazed by Giant Applesnail, (2) grazed by Florida Applesnail,
and (3) control with no snails. Due to a priori knowledge concerning variation in
grazing behavior among species and snail and plant size variation, we chose to use a
threshold in the interaction, i.e., 50% damage to the plant, to mark the point of experiment
completion for each replicate instead of setting a time limit for the experiment
duration. Because time was recorded for each replicate, we were able to then standardize
measurements as rates for analysis. We uniquely marked each plant blade by
pinholes at the base and blade tip of the plant (Zieman 1974), recorded the length of
each blade, and summed up the total blade length. Tanks were checked every 4 hours
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to remove any floating leaf blades. At the completion of each experimental replicate,
we measured the remaining plant blades and recorded snail weights.
We removed and measured all floating blades, which we recorded as physical
damage. Physical damage rate was determined per tank by totaling the lengths of
floating blades then dividing by time of the study duration in hours. Herbivory rate
was calculated per tank by the difference between the pre- and post-study total blade
length minus both physical damage and remaining blades, all divided by the sample
time in hours. The total damage rate is the difference between pre- and post-study
measurements of all blades divided by sample time in hours. Figure 1 illustrates
the differences between these measurements. Statistical analysis was conducted in
STATA Release 9 (STATA Corp., College Station, TX) using separate 1-way ANOVAs
for herbivory rate, physical damage rate, and total damage rate to determine
significant differences between controls, i.e., tanks without snails, and treatments
including each snail species. Each treatment group, including controls, contained
8 replicates. Tukey post-hoc tests were conducted to examine differences among
treatment groups, i.e., control vs. Giant Applesnail, control vs. Florida Applesnail
treatments, and snail treatments compared to each other.
Results
The overall study continued for 152 hours, with both species causing substantial
total damage to Tapegrass. On average, Giant Applesnail trials lasted 29 hrs (SE ±
4.49 hrs), with a range of 16–52 hrs. The average duration for Florida Applesnail
trials was 80 hrs (SE ± 20.44), with trials as short as 16 hrs and lasting as long as
152 hrs. Subsequently, rates of herbivory on, physical damage to, and total biomass
damage to Tapegrass by Giant Applesnail were 1.8 cm/hr (SE ± 0.47 cm/hr), 2.5
Figure 1. Diagram of grazing-
impact measurement
differences for herbivory,
physical damage, and total
damage.
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cm/hr (SE ± 0.82 cm/hr), and 4.2 cm/hr (SE ± 1.05 cm/hr), respectively (Fig. 2).
Florida Applesnail rates of herbivory, physical damage, and total biomass damage
were 0.2 cm/hr (SE ± 0.14 cm/hr), 1.2 cm/hr (SE ± 0.33 cm/hr), and 1.4 cm/hr (SE
± 0.39 cm/hr), respectively (Fig. 2). The mean growth rate of Tapegrass in tanks
containing no snails was 0.13 cm/hr (SE ± 0.01 cm/hr).
The 1-way ANOVA models found significant differences between groups for
herbivory (F(2, 21) = 12.88, P < 0.001), physical damage (F(2, 21) = 6.25, P =
0.007), and total biomass damage rates (F(2, 21) = 11.46, P < 0.001). Tukey posthoc
tests (α = 0.05) resulted in statistical differences between Giant Applesnail and
Florida Applesnail herbivory rates and total biomass damage rates (Fig. 2), but no
statistical difference was found for physical damage between Giant Applesnail and
Florida Applesnail treatments. Statistically significant differences were also found
with Tukey post-hoc tests (α = 0.05) between controls without snails and both Giant
Applesnail and Florida Applesnail herbivory, physical damage, and total biomass
damage rates (Fig. 2).
Figure 2. Pomacea maculata (Giant Applensail) and P. paludosa (Florida Applesnail) treatments
and control (no snails present) treatment rates for (A) total biomass damage (cm/hr)
with control V. americana (Tapegrass) growth rates (cm/hr), (B) herbivory (cm/hr) with
control Tapegrass growth rates (cm/hr), and (C) physical damage (cm/hr) with control Tapegrass
growth rates (cm/hr). Different letters above box-and-whisker plots for each treatment
indicated significant differences among treatments (P ≤ 0.05).
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Discussion
Specimens in the adult life-stage of Giant Applesnail and Florida Applesnail
exhibited top-down grazing pressure on Tapegrass, but, as hypothesized, Giant
Applesnail demonstrated significantly greater herbivory rates under controlled conditions.
Similarities in consumption behaviors between adults of the 2 species were
observed, with both beginning to graze near the base or middle of the plant, but
subsequent unanticipated behavior deviations, which could only be observed under
experimental conditions where the snails were presented the entire plant, resulted
in different destructive capabilities. Florida Applesnail predominately grazed along
the edges of the blades, whereas Giant Applesnail chewed completely through the
blades, i.e., severing the majority of the blade completely from its base, resulting
in significantly greater total biomass damage rates by Giant Applesnail. This difference
in behavior may be a consequence of snail mass and the blade’s ability to
support the weight of each herbivore species. Florida Applesnail consumption behavior
caused less biomass removal, which left more tissue and may be beneficial
for post-grazing compensatory regrowth. In contrast, the substantial loss of photosynthetic
material due to Giant Applesnail grazing could dramatically reduce the
plant’s ability to sustain growth over time.
Tapegrass communities are under pressure from abiotic and biotic factors. The
abiotic factors include increasing nutrients from non-point source pollution, and
biotic factors include invading non-native species, both plant (e.g., Waterthyme)
and animal (e.g., Giant Applesnail). Studies have shown that established Tapegrass
communities can competitively suppress invading Waterthyme under natural
low-nutrient conditions (Doyle et al. 2007, Owens et al. 2008), but competitive
interactions between the 2 plants can shift under varying conditions affecting sunlight
(Van et al. 1999) and substrate availability. When substrate with enhanced
nutrients becomes available, Waterthyme can establish (Owens et al. 2008),
increasing the likelihood of species persistence and further expansion. Giant Applesnail
occurs in both Waterthyme and Tapegrass communities (D. Monette, unpubl.
data), and its destructive grazing behavior introduces the potential for altering the
competitive balance in areas of interactions. Biomass removal by cutting plants at
the base creates an opening in the canopy near the water surface, increasing sunlight
and substrate availability and allowing neighboring and invading plant species,
such as Waterthyme, to utilize the available energy for additional tissue growth
(Van et al. 1999).
Because Giant Applesnail population growth may alter plant competitive interactions,
changes to community structure may follow. Submerged aquatic vegetation
community composition may subsequently favor less-palatable plant species with
faster growth rates, or species that are resistant to Giant Applesnail’s grazing behavior.
In comparison, native communities have evolved under the less-damaging
grazing pressure of Florida Applesnail, which appears to be found less often in
Tapegrass populations compared to other native plant communities (D. Monette,
unpubl. data) and may have less influence on the competitive balance among plants
than Giant Applesnail. However, Giant Applesnail and Florida Applesnail do not
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avoid each other in the wild, and both species have been found together within
Tapegrass communities (D. Monette, unpubl. data). It is not yet known whether the
co-occurrence of both species and their consumption behaviors in the same community
will result in additive effects and an increase in total damage, snail–plant
interaction pressure, and grazing duration.
Conclusion
The results of this study suggest that the introduction of the non-native
Giant Applesnail has the potential to alter existing Tapegrass communities due to
the invader’s grazing behavior and greater herbivory and total biomass damage
rates over the native apple snail. Follow-up studies should be performed to examine
how Giant Applesnail top-down grazing pressure may affect other plant species
and identify specific snail species densities that may tip the competitive balance
between plant species interactions and shape species composition.
Acknowledgments
We thank the anonymous donors to the Florida Atlantic University Geoscience Department
Graduate Scholarship who made that competitive scholarship possible and for the
scholarship committee for selecting this research. We also appreciate the anonymous reviewers
whose suggestions strengthened the manuscript.
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