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Chelonia mydas (Green Sea Turtle) forage at Higher Rates on Native Caribbean Seagrasses Despite Higher Coverage of Non-native Halophila stipulacea
Elizabeth C. Shaver, Danielle A. Keller, Joseph P. Morton, and Brian R. Silliman

Caribbean Naturalist, No. 55

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Caribbean Naturalist 1 E.C. Shaver, D.A. Keller, J.P. Morton, and B.R. Silliman 22001188 CARIBBEAN NATURALIST No. 5N5o:1. –575 Chelonia mydas (Green Sea Turtle) forage at Higher Rates on Native Caribbean Seagrasses Despite Higher Coverage of Non-native Halophila stipulacea Elizabeth C. Shaver1,*, Danielle A. Keller2, Joseph P. Morton1, and Brian R. Silliman1 Abstract - Since 2002, the non-native seagrass Halophila stipulacea has spread throughout subtidal habitats in the Caribbean. The ecological effects of the seagrass are still poorly understood, and the impacts of this invasion on the ecology of endangered Chelonia mydas (Green Sea Turtle), which graze on native Caribbean seagrasses, are of special concern. We conducted short-term (30-min) observational surveys of the feeding behavior of 20 individual turtles within 3 bays in St. John, US Virgin Islands that had mixed assemblages of native and invasive seagrasses, and recorded bites taken by turtles on each seagrass type. We found that while turtles consumed H. stipulacea, they disproportionately foraged on native seagrass species (99.98% of bites). For example, though average cover was higher for H. stipulacea than for native seagrasses, C. mydas consumption of native seagrasses was 53-times higher than of the non-native species. These patterns suggest that, at least for the present time, C. mydas in St. John prefer native seagrasses over H. stipulacea. Whether these feeding patterns impact plant community structure should be further investigated experimentally. Introduction Invasive plant species can have irreversible negative effects on the structure and functioning of ecosystems, including altering fauna communities and food-web dynamics (Vila et al. 2010, Vitousek et al. 1997, Wright et al. 2014). Yet, predicting how native herbivores will respond to invading plant species can be difficult and complex. The enemy-release hypothesis suggests that native generalists naturally prefer native plants (Colautti and MacIsaac 2004, Keane and Crawley 2002), which would allow invasive plants to proliferate. In contrast, some studies have found aquatic generalists, including crayfish and beavers, to prefer exotic plants over native species, providing natural consumer control over exotic species (Parker and Hay 2005, Parker et al. 2007). Though research on non-native plants often examines the role of herbivores in controlling invasions (Lake and Leishman 2004), it is also important to assess how herbivores are affected, especially in the case of endangered species. Native to the Indian Ocean, the seagrass Halophila stipulacea Forsskål has spread to 18 Caribbean islands since 2002 (Ruiz and Ballantine 2004). Despite 1Division of Marine Science and Conservation, Nicholas School of the Environment, Duke University, 135 Duke Marine Lab Road, Beaufort, NC 28516, USA. 2Institute of Marine Sciences, University of North Carolina at Chapel Hill, 3431 Arendell Street, Morehead City, NC 28557, USA. *Corresponding author - Manuscript Editor: Kathleen Sullivan Sealey Caribbean Naturalist E.C. Shaver, D.A. Keller, J.P. Morton, and B.R. Silliman 2018 No. 55 2 its rapid expansion, its effects on local ecological communities and feeding relationships in food webs remain largely unknown. Throughout its native range H. stipulacea is a fast-growing, dense, mat-forming species that occurs in shallows, but also up to depths of 45 m, and acts as a food source for Dugong dugon (Müller) (Dugong), Chelonia mydas L. (Green Sea Turtle), Eretmochelys imbricata L. (Hawksbill Turtle), and various fishes (Mariani and Alcoverro 1999, Spalding et al. 2003, Turkozan and Durmus 2000). Throughout its native range, H. stipulacea acts as an important food resource for sea turtles (Spalding et al. 2003, Turkozan and Durmus 2000). Recent field assessments of the willingness of C. mydas to consume H. stipulacea demonstrate that they will feed on this novel food source (Becking et al. 2014). These tests, however, did not examine rates of consumption on native versus invasive seagrasses to gain insight into the C. mydas’ potential feeding preferences. Here, we directly observed 20 individual C. mydas feeding in bays with mixed patches of non-native H. stipulacea and native Caribbean Thalassia testudinum Banks ex König (Turtle Grass), Syringodium filiforme Kuetz. (Manatee Grass), and Halodule wrightii Ascherson (Shoal Grass) to determine the relative foraging rates and develop a better understanding of Green Sea Turtle consumption on this invading seagrass. Methods We selected 3 bays in St. John, US Virgin Islands, where we repeatedly observed Green Sea Turtles where both native seagrasses and the non-native Halophila stipulacea were present. These bays included Francis Bay and Maho Bay (located on the northern coast of the island), and Saltpond Bay (located on the southern coast of the island). In January 2015, we conducted surveys to determine the percent cover of seagrass vegetation, including all 3 native Caribbean seagrasses: Turtle Grass, Manatee Grass, and Shoal Grass, the invasive H. stipulacea, macro-algae, and bare substrate. To do this, snorkelers performed eight 25-m transect-line surveys perpendicular to shore starting ~3 m from shore where seagrass meadows began. Snorkelers visually estimated the percent cover of each seagrass species or substrate type in 10-cm2 quadrats at the 0-m, 5-m, 10-m, 15-m, 20-m, and 25-m marks, for a total of 48 quadrats per site. We used Welch’s 2-sample t-tests to compare differences in the percent cover of vegetation types across and between bays. In addition, we observed 20 individual C. mydas in Saltpond Bay (n = 3), Maho Bay (n = 8), and Francis Bay (n = 9) to determine their foraging preferences for the native or invasive seagrasses (Ballorain et al. 2010). Snorkelers located 1 turtle, allowed for a 5-min acclimation period for C. mydas to adjust to the presence of snorkelers, then recorded bites taken on all seagrass species for 30 min. Surveys were conducted at a distance of ~2 m, where data could be obtained but snorkelers did not interfere with the behavior of C. mydas. At this distance, observers noted no behavioral changes such as halted foraging or swimming away. We ran 1-way analysis of variance (ANOVA) to assess differences in C. mydas grazing between seagrasses. We analyzed all data in R version 3.3.2 (R Core Team 2016). Caribbean Naturalist 3 E.C. Shaver, D.A. Keller, J.P. Morton, and B.R. Silliman 2018 No. 55 Results Across the 3 bays, we found that bare substrate accounted for most of the benthos in our seagrass vegetation surveys (mean percent cover ± SD; total = 65.4 ± 31.1%; Maho Bay = 71.7 ± 34.6%; Francis Bay = 70.4 ± 25.2%; Saltpond Bay = 54.1 ± 30.2%). H. stipulacea was significantly higher in percent cover than the native seagrasses across sites (P = 0.025, t = -2.246, df = 260.62); it was 2.2 times higher in Francis Bay (native = 8.8 ± 13.5%; invasive = 19.2 ± 22.7%; P = 0.0079, t = -2.730, df = 76.35) and 3.9 times higher in Saltpond Bay (native = 9.2 ± 11.7%; invasive = 35.6 ± 31.9%; Welch’s 2-sample t-test: P < 0.0001, t = -5.380, df = 59.46; Fig. 1a). However, in Maho Bay the native seagrasses were 9.7 times higher in percent cover than H. stipulacea (native = 20.1 ± 27.7%; invasive = 2.1 ± 11.1%; P < 0.001, t = 4.185, df = 61.83; Fig. 1A). Macro-algae were relatively low in percent cover overall and across bays (total = 3.0 ± 7.3%; Maho Bay = 6.1 ± 11.3%; Francis Bay = 1.7 ± 3.8%; Saltpond Bay = 1.1 ± 2.3%). Figure 1. (A) Percent cover of native Caribbean seagrasses (light gray) and the invasive seagrass Halophila stipulacea (dark gray) and (B) the number of bites taken by Chelonia mydas (Green Sea Turtle) over a 30-min period in 3 bays in St. John, US Virgin Islands. Data are shown as means ± 1 standard error. Caribbean Naturalist E.C. Shaver, D.A. Keller, J.P. Morton, and B.R. Silliman 2018 No. 55 4 During the 30-min observation period, we found that C. mydas had an average of 294.9 ± 61.5 bites of seagrass across all seagrass species. Overall, C. mydas fed at significantly higher rates on the native seagrasses relative to H. stipulacea (P less than 0.0001, t = -19.37, df = 19.33; Fig. 1B), even in Francis and Saltpond Bay where H. stipulacea was more abundant than the native species. For instance, the consumption of H. stipulacea accounted for only 0.02% of all recorded bites (H. stipulacea = 5.3 ± 6.1 average bites; native seagrasses = 289.6 ± 65.4 average bites). We also observed turtles avoiding seagrass patches dominated by H. stipulacea and even spitting out blades of this species. These findings held true across all 3 bays; we found no difference in consumption of the native seagrass (F2,17 = 0.66, P = 0.53) or H. stipulacea (F2,17 = 1.07, P = 0.364) across bays. Discussion Despite the extensive cover of H. stipulacea across 3 bays in St. John, we found that foraging by C. mydas was rare on this non-native seagrass species (Fig. 1). For instance, the incidence of turtle foraging on native seagrasses was 53-times higher despite 33% lower average cover relative to the non-native H. stipulacea across all bays. Our observations that C. mydas grazed on but then expelled blades of the non-native seagrass further suggests that those turtles highly prefer seagrasses native to the Caribbean over H. stipulacea. This finding, however, should be investigated by conducting controlled preference-studies in the laboratory or field at multiple locations. It has been shown, however, that native grazers can eventually adapt to consuming non-native species and feed on them to a greater degree over time after the initial invasion (MacArthur and Pianka 1966, Parker et al. 2006). Here, we observed C. mydas feeding on H. stipulacea in all 3 bays, though the proportion of bites on the invasive species was low relative to native seagrasses. In Maho Bay, we observed 1 C. mydas feeding on 14 blades of H. stipulacea, accounting for 5.9% of its total grazing. This observation, in addition to reports of C. mydas feeding on H. stipulacea in Bonaire (Becking et al. 2014), suggest that C. mydas may adapt to this novel resource or that there may be variation in feeding preferences between individuals or populations in different locations (Araújo et al. 2011, Fuentes et al. 2006). The adaptation of native consumers to invading plants can serve as important biological-control agents, as seen with large mammals on the invasive marsh grass Phragmites australis (Cav.) Steud. (Common Reed; Silliman et al. 2014) or groupers on the invasive Pterois volitans L. (Red Lionfish; Mumby et al. 2011). Our study’s results are limited to 1 island and 20 individuals; thus, increased spatiotemporal research on more individuals is required to determine how C. mydas and H. stipulacea will affect one another’s populations. These observations are similar to those by other researchers who showed that juvenile Green Sea Turtles in Australia foraged on specific seagrass and macroalgae based on preference rather than the abundance of those prey (Fuentes et al. 2006). As such, there are several factors that could affect turtle foraging and preference on different prey species, including characteristics of C. mydas and their seagrass or macroalgae prey. For instance, juvenile C. mydas have been shown to feed on Caribbean Naturalist 5 E.C. Shaver, D.A. Keller, J.P. Morton, and B.R. Silliman 2018 No. 55 different prey than sub-adults or adults (Arthur et al. 2008). Although we did not determine the size or life stage of the C. mydas observed in this study, future research should seek to examine different life stages and their preferences for the native seagrasses vs. H. stipulacea. Turtles also often select foraging material based on characteristics such as higher nutrients and protein, lower fiber (e.g., cellulose), and microbiota (Bjorndal 1980, 1985; Van Houten et al. 2010). As H. stipulacea blades are often smaller and thinner than the Caribbean Turtle Grass, these factors likely affect C. mydas preferences, however future research should investigate nutritional differences between these species. Our finding that Green Sea Turtles appear to prefer the native seagrasses indicates that these animals could also play an important role in determining the relative abundance of native versus non-native seagrass species in St. John, USVI. For instance, strong preferences against H. stipulacea may lead to an increase in the magnitude of grazing pressure on the native seagrass species, which in turn could enhance the expansion of H. stipulacea. Indeed, a feedback between increased expansion and reduced top-down control on H. stipulacea could lead herbivores to concentrate grazing on remaining patches of native seagrass vegetation (Fourqurean et al. 2010). In an Indonesian protected area where the conservation of sea turtles has been successful, the resulting hyper-abundance of turtles and their grazing overwhelmed seagrass beds to the point of complete habitat collapse (Christianen et al. 2014). Although previous studies have cited a combination of recreational and commercial boat traffic as 2 main causes facilitating H. stipulacea invasion in the Caribbean (Willette et al. 2014), our study suggests that grazing by C. mydas could serve to facilitate continued expansion if herbivores graze almost exclusively on the native seagrasses. Likewise, the loss of native seagrasses could have significant implications for already-endangered populations of C. mydas in the Caribbean. Controlling the invading seagrass H. stipulacea could therefore be important for securing sustainable food sources for these turtles. Though further research should be conducted on this topic in many other locations, our study highlights potentially important implications of the invasive H. stipulacea on the local C. mydas populations in St. John, USVI. Determining whether C. mydas adapt to or are negatively affected by this seagrass requires further monitoring. It is worth noting that severe storms, which may occur more frequently in the region in the years ahead due to the effects of climate change, can also have a siginficant impact on the seagrass beds and their utilization by turtles. In 2017, St. John, USVI, suffered extensive damage from Hurricane Irma and Maria, but it is unknown at this time how seagrass communities were impacted. Further research could shed light on the effects those very severe storms had on seagrasses in the waters off St. John and on the Green Sea Turtle populations there. Acknowledgments We thank the students of the Duke University Marine Ecology 2015 travel course for their assistance in conducting fieldwork: Aitana Zermeno, Catherine Chen, Laura Damiani, Caribbean Naturalist E.C. Shaver, D.A. Keller, J.P. Morton, and B.R. Silliman 2018 No. 55 6 Betsy Mansfield, Emily Graves, Katie Beachem, Kelsey Quaile, Laura Bennett, Lauren Ellis, Morgan Vrana, Nicole Rice-Clewell, and Peter Adler. We are also grateful to the staff of the Virgin Islands Environmental Resource Station for their assistance and hospitality. Research was conducted under the Virgin Islands National Park Service Permit #VIIS- 2015-SCI-0006, VIIS-2014-SCI-0017, and VICR-2014-SCI-004. The National Science Foundation supported E.C. Shaver (DGE No. 1106401), D.A. Keller (DGE No. 1144081), and B.R. Silliman (BIO-OCE 1056980). 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