Regular issues
Monographs
Special Issues



Southeastern Naturalist
    SENA Home
    Range and Scope
    Board of Editors
    Staff
    Editorial Workflow
    Publication Charges
    Subscriptions

Other EH Journals
    Northeastern Naturalist
    Caribbean Naturalist
    Urban Naturalist
    Eastern Paleontologist
    Eastern Biologist
    Journal of the North Atlantic

EH Natural History Home

Effects of the Consumption Behavior of Adult Pomacea maculata and Pomacea paludosa on Vallisneria americana
Dean Monette, Sharon Ewe, and Scott H. Markwith

Southeastern Naturalist, Volume 15, Issue 4 (2016): 689–696

Full-text pdf (Accessible only to subscribers.To subscribe click here.)

 

Site by Bennett Web & Design Co.
Southeastern Naturalist 689 D. Monette, S. Ewe, and S.H. Markwith 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 Southeastern Naturalist D. Monette, S. Ewe, and S.H. Markwith 2016 Vol. 15, No. 4 690 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. Southeastern Naturalist 691 D. Monette, S. Ewe, and S.H. Markwith 2016 Vol. 15, No. 4 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 Southeastern Naturalist D. Monette, S. Ewe, and S.H. Markwith 2016 Vol. 15, No. 4 692 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. Southeastern Naturalist 693 D. Monette, S. Ewe, and S.H. Markwith 2016 Vol. 15, No. 4 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). Southeastern Naturalist D. Monette, S. Ewe, and S.H. Markwith 2016 Vol. 15, No. 4 694 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 Southeastern Naturalist 695 D. Monette, S. Ewe, and S.H. Markwith 2016 Vol. 15, No. 4 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. Literature Cited Aumen N.G., and R.G. Wetzel (Eds.). 1995. Ecological Studies on the Littoral and Pelagic Systems of Lake Okeechobee, Florida (USA). Archiv Fur Hydrobiologie Advances Limnology 45. 356 pp. Baker, P., F. Zimmanck, and S.M. Baker. 2010. Feeding rates of an introduced freshwater gastropod, Pomacea insularum, on native and nonindigenous aquatic plants in Florida. Journal of Molluscan Studies 76:138–143. Boland, B.B., M. Meerhoff, C. Fosalba, N. Mazzeo, M.A. Barnes, and R.L. Burks. 2008. Juvenile snails, adult appetites: Contrasting resource consumption between two species of applesnails (Pomacea). Journal of Molluscan Studies 74:47–54. Burlakova, L., D. Padilla, A. Karatayev, D. Hollas, L. Cartwright, and K. Nichol. 2010. Differences in population dynamics and potential impacts of a freshwater invader driven by temporal habitat stability. Biological Invasions 12:927–941. Byers, J., W. McDowell, S. Dodd, R. Haynie, L. Pintor, and S. Wilde. 2013. Climate and pH predict the potential range of the invasive apple snail (Pomacea insularum) in the southeastern United States. PLoS ONE 8:e56812. Darby, P.C., R.E. Bennetts, and H. Percival. 2008. Dry-down impacts on apple snail (Pomacea paludosa) demography: Implications for wetland water management. Wetlands 28:204–214. DiTomaso, J.M. 2000. Invasive weeds in rangelands: Species, impacts, and management. Weed Science 48:255–265. Doyle, R., M. Grodowitz, M. Smart, and C. Owens. 2007. Separate and interactive effects of competition and herbivory on the growth, expansion, and tuber formation of Hydrilla verticillata. Biological Control 41:327–338. EFSA, Panel on Plant Health. 2014. Scientific opinion on the environmental risk assessment of the apple snail for the EU. EFSA Journal 12:97. Southeastern Naturalist D. Monette, S. Ewe, and S.H. Markwith 2016 Vol. 15, No. 4 696 Garr, A.L., H. Lopez, R. Pierce, and M. Davis. 2011. The effect of stocking density and diet on the growth and survival of cultured Florida Apple Snails, Pomacea paludosa. Aquaculture 311:139–145. Havens, K., and A. Steinman. 2013. Ecological responses of a large shallow lake (Okeechobee, Florida) to climate change and potential future hydrologic regimes. Environmental Management:1–13. Hayes, K.A., R.H. Cowie, S.C. Thiengo, and E.E. Strong. 2012. Comparing apples with apples: Clarifying the identities of two highly invasive Neotropical Ampullariidae (Caenogastropoda). Zoological Journal of the Linnean Society 166:723–753. Kolar, C.S., and D.M. Lodge. 2001. Progress in invasion biology: Predicting invaders. Trends in Ecology and Evolution 16:199–204. Kyle, C.H., M.K. Trawick, J.P. McDonough, and R.L. Burks. 2009. Population dynamics of an established reproducing population of the invasive apple snail (Pomacea insularum) in suburban southeast Houston, Texas. Texas Journal of Science 61:323–327. Morrison, W.E., and M.E. Hay. 2011. Feeding and growth of native, invasive, and noninvasive alien apple snails (Ampullariidae) in the United States: Invasives eat more and grow more. Biological Invasions 13:945–955. Owens, C.S., R.M. Smarts, and G.O. Dick. 2008. Resistance of Vallisneria to invasion from hydrilla fragments. Journal of Aquatic Plant Management 46:113–116. Rawlings, T., K. Hayes, R. Cowie, and T. Collins. 2007. The identity, distribution, and impacts of non-native apple snails in the continental United States. BMC Evolutionary Biology 7:97. Simberloff, D., and O.J. Schmitz. 1997. Strangers in Paradise: Impact and Management of Nonindigenous Species in Florida. Island Press, Washington, DC. Xii + 467 pp. US Army Corps of Engineers (USACE). 1999. Central and southern Florida comprehensive review study. Jacksonville District Corps of Engineers, Jacksonville, FL. Van, T.K., G.S. Wheeler, and T.D. Center. 1999. Competition between Hydrilla verticillata and Vallisneria americana as influenced by soil fertility. Aquatic Botany 62:225–233. Youens, A.K., and R.L. Burks. 2008. Comparing applesnails with oranges: The need to standardize measuring techniques when studying Pomacea. Aquatic Ecology 42:679–684. Yoshida, K., K. Matsukura, N.J. Cazzaniga, and T. Wada. 2014. Tolerance to low temperature and desiccation in two invasive apple snails, Pomacea canaliculata and Giant Applesnail (Caenogastropoda: Ampullariidae), collected in their original distribution area (northern and central Argentina). Journal of Molluscan Studies 80:62–66. Zieman, J. C. 1974. Methods for the study of the growth and production of Turtle Grass, Thalassia testudinum König. Aquaculture 4:139–143.