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Home , Gastropoda, Rapana, Rapana venosa, Rapa (gastropod)

Marine . ISSN 0173-9565

1 SHORT COMMUNICATION 2 3 Loggerhead turtles Caretta caretta (Linnaeus, 1758) preying 4 on the invading gastropod venosa (Valenciennes, 5 6 1846) in the Rı´o de la Plata 7 Alvar Carranza1,2, Andre´ s Estrades2,3, Fabrizio Scarabino2,4 & Angel Segura2,5 8 9 1 UNDECIMAR, Facultad de Ciencias, Igua´ , Montevideo, Uruguay 10 2 Museo Nacional de Historia Natural, Montevideo, Uruguay 11 3 KARUMBE, Biodiversidad y Conservacio´ n, Av. Rivera, Montevideo, Uruguay 12 4 Direccio´ n Nacional de Recursos Acua´ ticos, Constituyente, Montevideo, Uruguay 2 5 Seccio´ n Oceanologı´a, Facultad de Ciencias, Igua´ , Montevideo, Uruguay 13 14 15 16 17 18 19 Keywords Abstract 20 Biological invasions; Caretta caretta; Here we report the first observations of loggerhead turtles Caretta caretta prey- 21 ; ; Uruguay. ing on a conspicuous molluscan invader, the Rapana venosa.An 22 Correspondence average number of 136 opercula were found in contents of five turtles, 23 Alvar Carranza, UNDECIMAR, Facultad de the curved carapace length ranging in from 51 to 112 cm. No other alimentary 24 Ciencias, Igua´ 4225, C.P. 11400, Montevideo, items were found in the turtles analyzed. We suggest that the Rapa Whelk may 25 Uruguay. constitute up to 100% of the diet for immature and mature loggerheads in the 26 E-mail: [email protected] Rı´o de la Plata estuary (Uruguay), highlighting the plastic nature of the forag- 27 ing behavior of loggerheads. 28 Accepted: 9 November 2010 29 doi:10.1111/j.1439-0485.2010.00424.x 30 31 32 33 34 take feeding migrations over the continental shelf Introduction 35 (Almeida et al. 2000; Laporta & Lopez 2003). Large juve- 36 Loggerhead turtles Caretta caretta (Linnaeus, 1758) are an niles and adults feed in the Southwestern Atlantic shore 37 endangered (IUCN 2009) distributed worldwide, upon a variety of benthic , such as crusta- 38 inhabiting continental shelves, bays, lagoons, and ceans (e.g. Libinia spinosa, Loxopagurus loxochelis), mol- 39 in the temperate, subtropical, and tropical waters of the lusks (Buccinanops cochlidium, Pachycymbiola brasiliana), 40 Atlantic, Pacific, and Indian (Dodd 1988). In the and fishes discarded from coastal fisheries (Estrades et al. 41 Southwestern Atlantic, the occurrence of immature and 2007; Martinez-Souza 2009). Because loggerheads have 42 adult loggerheads from nesting beaches of Brazil, the very powerful jaws, they are capable of crushing the shells 43 USA, and Australia is common (Caraccio et al. 2008). of seemingly invulnerable prey such as the gastropod 44 The nearest nesting colony of loggerhead turtles to the gigas and the bivalves Tridacna maxima and 45 Rı´o de la Plata Estuary is located in the state of Espiritu Tridacna fosor (Mortimer 1995). 46 Santo, Brazil. The classification of developmental stages of Rapana venosa (Valenciennes, 1846), a large, predatory 47 Uruguayan loggerheads are based on nesting data from gastropod and one of the most unwelcome and conspicu- 48 Brazilian rockeries, showing that the minimum nesting ous invading mollusks, was introduced during the 1990s in 49 size of a female is an 83 cm curved carapace length (CCL; the Rı´o de la Plata Estuary (Scarabino et al. 1999; Pastorino 50 Baptistotte et al. 2003). Thus, CCLs from Uruguay, rang- et al. 2000). This species has been shown to be widespread 51 ing from 51 to 112 cm (Lo´pez-Mendilaharsu et al. 2006), in the area, reaching very high densities all along the Rı´ode 52 indicate the presence of both juveniles and mature indi- la Plata Estuary, both in hard and soft bottoms (Giberto 53 viduals. Adult loggerheads nesting in these regions under- et al. 2006; Scarabino et al. 2006; Carranza & Rodrı´guez

Marine Ecology (2010) 1–6 ª 2010 Blackwell Verlag GmbH 1

MAEC 424 Dispatch: 20.11.10 Journal: MAEC CE: Ranjani Journal Name Manuscript No. B Author Received: No. of pages: 6 PE: Sharanya C. caretta predation on R. venosa Carranza, Estrades, Scarabino & Segura 1

1 2007; Cortelezzi et al. 2007; Carranza et al. 2008, 2010; La- to report predation by loggerheads on R. venosa in the Rı´o 2 3 franconi et al. 2009), thus constituting both a threat to de la Plata Estuary, (ii) to analyze quantitative aspects of 3 native bivalves (e.g. the blue Mytilus edulis; Scarabi- this novel predator–prey interaction (e.g. gut content analy- 4 no et al. 1999; Carranza et al. 2010) and a potential ses, size–frequency distributions of ingested ) by dis- 5 resource for predators of benthic . Harding & Mann cussing the results in the context of the ecological features 6 (1999) suggested that sea turtles and blue crabs may be of both species. 7 potential predators of R. venosa in . How- 8 ever, until now, there was no evidence of predation on Material and Methods 9 Rapa Whelks in the Rı´o de la Plata Estuary, and there were 10 no previous reports of predation by loggerheads (or any Digestive tract contents were examined from five logger- 11 other predator) on this gastropod in invaded natural habi- turtles stranded on the beaches or captured by the 12 tats worldwide (e.g. Dodd 1988; Harding & Mann 1999; Uruguayan fleet between March 2002 and November 13 Frick et al. 2001). Thus, the objectives of this paper are (i) 2008 (Table 1, Fig. 1). All turtles were found dead and 14 15 Table 1. Identification code, collection dates, Uruguayan locations (latitude and longitude). curved carapace length (CCL), and status (S ⁄ C = stranded or by-catch) of the examined animals. Each code represents one of the five turtles examined. 16 17 code date location latitude longitude sex CCL (cm) S ⁄ C 18 CCV 014 Feb 2002 Carrasco, Montevideo 34° 53¢569 56° 03¢389 N ⁄ A 60.0 Stranded 19 CCV 254 Mar 2006 Carrasco, Montevideo 34° 53¢112 56° 02¢286 Male 105.5 Stranded 20 PRO 1 Mar 2006 Argentine-Uruguayan 35° 58¢000 56° 09¢000 Male 107.0 Trawl by-catch 21 Common Fishing Zone 22 CCV 317 Feb 2008 Carrasco, Montevideo 34° 53¢050 56° 02¢220 Male 108.5 Stranded 23 CCV 318 Feb 2008 Belo Horizonte, Canelones 34° 46¢647 55° 38¢630 Male 109.0 Stranded 24 25 26 27 28 29 30 31 32 33 34

35 LOW RESOLUTION FIG

36 Colour online, B&W in print 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 Fig. 1. Map of the Rı´o de la Plata estuary, indicating locations of collection of sea turtles. 1: Carrasco, Montevideo; 2: Belo Horizonte, Canelones 8 52 and 3: Argentine–Uruguayan Common Fishing Zone. Known records of Rapana venosa are also indicated (gray circles), as well as a coarse charac- 53 terization of sediment type.

2 Marine Ecology (2010) 1–6 ª 2010 Blackwell Verlag GmbH Carranza, Estrades, Scarabino & Segura C. caretta predation on R. venosa 1

1 Table 2. Digestive tract analysis summary. Identification code, item, and presence or number of items (total wet weight, g) found inside entire 2 digestive tract (stomach and ⁄ or intestines) of the examined loggerheads. When possible, gut content was isolated to digestive tract location (intes- ⁄ ⁄ 3 tine or stomach); N F indicates opercula were not found in the indicated region, N A indicates tract location was not available as the contents could not be isolated to a particular tract region. In all cases, Rapa whelks accounted for 100% of gut content. 4 5 code item all tract (total) intestine stomach 6 CCV 014 Opercula 16 (26) 16 (26) N ⁄ F 7 Foot ⁄ visceral mass ⁄ Present Present N ⁄ F 8 Shell fragments Present Present N ⁄ F 9 CCV 254 Opercula 150 (702) N ⁄ AN⁄ A 10 Foot ⁄ visceral mass ⁄ mantle Present N ⁄ AN⁄ A 11 Shell fragments Present N ⁄ AN⁄ A 12 Rapana egg capsules Present N ⁄ AN⁄ A ⁄ ⁄ 13 PRO 1 Opercula 118 (583) N ANA Foot ⁄ visceral mass ⁄ mantle Present N ⁄ AN⁄ A 14 Shell fragments Present N ⁄ AN⁄ A 15 Rapana egg capsules Present N ⁄ AN⁄ A 16 CCV 317 Opercula 129 (1946) 117 (196) 12 (22) 17 Foot ⁄ visceral mass ⁄ mantle (1366) (891) (475) 18 Shell fragments (362) (347) (15) 19 Rapana egg capsules N ⁄ FN⁄ FN⁄ F 20 CCV 318 Opercula 144 (649) 132 (214) 12 (21) Foot ⁄ visceral mass ⁄ mantle (137) (131) (106) 21 Shell fragments (177) (173) (4) 22 Rapana egg capsules N ⁄ FN⁄ FN⁄ F 23 24 25 were identified and classified by size (CCL) and gender. During this season, average salinity ranges from 10 to 25 26 The turtles were examined to analyze diet and the entire (Guerrero et al. 1997). 27 contents of the gut, stomach and ⁄ or intestinal tract were Stranded turtles were fresh and, based on their general 28 collected following necropsies. The mouth cavity and condition, most likely died 48–72 h before being ana- 29 esophagus of each specimen were also inspected. Identity, lyzed. Analyses revealed high numbers of opercula belong- 30 quantity, and wet weight of prey items were determined. ing to Rapana venosa, as well as mantle and foot tissue, 31 Diet data are presented in Table 2 as the number and wet shell remnants, and ovigerous capsules from the whelks. 32 weight for each item, discriminated by their location Opercula were all fairly well preserved. In all the exam- 33 along the digestive tract (when available). ined turtles, the whelk accounted for 100% of gut con- 34 To depict both the feeding preferences of Caretta caret- tent. The average number of opercula was 135.6. One 35 ta and to identify on which population component of turtle (CCV 254) contained some 150 opercula, represent- 36 Rapana venosa it is preying, we estimated the shell length ing 702 g in wet weight, together with some egg capsules 37 of the gastropod based on opercula measurements. To of the whelk (Table 2). 38 this end, the ingested opercula were measured for their The least-squares linear regression model, based on 39 maximum linear dimension, and then the shell length of maximum opercula linear dimension, explained nearly 40 the gastropods was estimated using a regression model. 60% of the variance in shell length (R2 = 0.59, P < 0.05; 41 The shell length versus operculum relationship was gener- y = 27.72 + 1.31x). Using this model and based on the 42 ated using 250 live-collected whelks from Maldonado Bay 559 opercula examined, the average shell length of the 43 (April 2010), ranging in size from 52 to 120 mm in shell ingested gastropods was 89.05 mm, ranging from 55.31 to 44 length (Carranza et al. 2010). With this model, we con- 117.06 mm. There were clear differences in the average 45 structed a shell length frequency distribution of the gas- shell length of the gastropods ingested among turtles, 46 tropods found in the digestive tract of the examined with one individual (CCV 014) showing a preference for 47 loggerhead individuals. comparatively small-sized gastropods (Fig. 2). 48 49 Results Discussion 50 51 In the zone where turtles were collected in the Rı´odela To our knowledge, this is the first report of loggerhead 52 Plata, seawater temperatures reach maximum seasonal turtles preying on the invading gastropod Rapana venosa, 53 values (average = 22 °C; SD = 1.1 °C) in austral summer. and the first record of any predator of the in an

Marine Ecology (2010) 1–6 ª 2010 Blackwell Verlag GmbH 3 C. caretta predation on R. venosa Carranza, Estrades, Scarabino & Segura 1

1 apeake Bay. However, to date, there have been no 2 published reports on this particular interaction. In the 3 Rı´o de la Plata Estuary, the high number of con- 4 sumed by turtles demonstrates the importance of the 5 whelk for turtle diets. We believe that the reported 100% 6 gut content measurement is not an overestimation of the 7 importance of the whelk. Although opercula may persist 8 longer in the digestive tract, we also found soft tissues of 9 the Rapa Whelk, which are much more sensitive to diges- 10 tion than other prey usually consumed by the loggerhead LOW RESOLUTION FIG 11 (e.g. fishes, crabs) (F. Scarabino and A. Estrades, personal 12 communication). This predator–prey interaction is none- 13 theless particularly relevant from both ecological and 14 socioeconomic perspectives, as the loggerhead turtle is a 15 charismatic, flagship and endangered species, and R. ven- 16 osa is considered to be among the 100 worst alien species 17 in the European Invasive Alien Species Gateway (DAISIE 18 2010), one of two marine gastropods on this list. 19 Although there were differences in the range of shell 20 lengths of ingested gastropods among turtles, all esti- 21 mated figures suggest that Caretta caretta preys on adult 22 R. venosa (Saglam & Duzgunes 2007; Saglam et al. 2009). 23 These authors reported that the size at maturity of R. 24 venosa is about 40 mm, and all the examined opercula 25 suggest that ingested gastropods are larger than this fig- 26 ure. Harding (2003) analyzed the predation patterns of 27 the blue crab Callinectes sapidus on the Rapa Whelk in 28 Chesapeake Bay, and suggested that the rapid growth and 29 shelf features of R. venosa create both a and a size 30 refuge for blue crab predation at a shell length of 60– 31 80 mm. However, this is not the case for this predator– 32 prey interaction, as loggerheads prey upon whelks well 33 above these sizes. Further, the maximum estimated size 34 for an ingested whelk was 117 mm, very close to the maxi- 35 mum size (120 mm) reported for the study area (Giberto 36 et al. 2006). In a wider context, the estimated size range 37 Fig. 2. Upper panel: shell-length frequency distribution of ingested 9 of Rapa Whelks found in loggerhead gut contents falls Rapana venosa. Measurements were estimated by means of a regres- 38 within the published range of sizes observed in established sion model based on the relationship of to shell length 39 (see text for details). Lower panel: Mean (± SD) shell length of populations (Giberto et al. 2006; Lafranconi et al. 2009) 40 ingested Rapana venosa discriminated by loggerhead individuals. in the Rı´o de la Plata area. Although one turtle (CCV 41 254) contained some egg capsules of the whelk, this 42 should not be interpreted as evidence of foraging on egg 43 invaded . Whereas loggerhead post-hatchlings capsules, as eggs can be attached the shell (F. Scarabino, 44 feed on a variety of neustonic items, evidence of their personal communication). The timing of the observations 45 pelagic existence (Boyle & Limpus 2008), immature and also suggests that the predation events coincided with the 46 mature stages present a benthic foraging ecology, also summer reproductive period of the whelk (Pastorino 47 supplementing their natural diets with discarded fish et al. 2000; Giberto et al. 2006; Carranza et al. 2010). 48 from fisheries (Plotkin et al. 1993; Tomas et al. 2001). In 49 this context, several authors reported shelled gastropods Conclusions 50 in the loggerhead diets (Dodd 1988; Frick et al. 2001; 51 Tomas et al. 2001; Estrades et al. 2007; Martinez-Souza Understanding ecosystem responses to human-induced 52 2009; Wallace et al. 2009). Harding & Mann (1999) sug- change is a challenge for the scientific community 53 gested that sea turtles can be predators of whelks in Ches- worldwide, as species interactions are often non-linear

4 Marine Ecology (2010) 1–6 ª 2010 Blackwell Verlag GmbH Carranza, Estrades, Scarabino & Segura C. caretta predation on R. venosa 1

1 and hard to predict (Walther et al. 2002). Given that Cortelezzi A., Rodrigues Capı´tulo A., Boccardi L., Arocena R. 2 the whelk represented 100% of the gut content of the (2007) Benthic assemblages of a temperate estuarine system 3 analyzed turtles, Caretta caretta may well be an impor- in : transition from a freshwater to an estua- 4 tant population control for this extremely successful rine zone. Journal of Marine Systems, 68, 569–580. 5 invading gastropod. The lack of estimates of the popula- DAISIE European Invasive Alien Species Gateway. (2010) 6 tion sizes of both Rapana venosa and loggerhead in the Rapana venosa. Last updated 30 October 2006, accessed 2 7 Rı´o de la Plata Estuary and of the predation rates of the August 2010. 5 8 sea turtles on these gastropods, preclude a quantitative Dodd C.K. (1988) Synopsis of the biological data on the log- 9 estimation of the impact of this trophic relationship for gerhead sea turtle Caretta caretta (Linnaeus, 1758). US Fish and Wildlife Service. Biological Reports, 88, 1–110. 10 these populations. However, our findings highlight the Estrades A., Souza G., Scarabino F., Laporta M., Miller P., 11 plasticity of the opportunistic, generalist foraging strat- Rinderknecht A., Sa´nchez P. (2007) Ecologı´a alimenticia de 12 egy of loggerheads (Dodd 1988; Wallace et al. 2009), la tortuga Cabezona (Caretta caretta) en la plataforma 13 and demonstrate a novel trophic link between one of uruguaya: resultados preliminares. Libro de Resu´ menes de 14 the more conspicuous invading mollusks and a seriously las III Jornadas de Conservacio´n e Investigacio´n de Tortugas 15 threatened species. Marinas en el Atla´ntico Sur Occidental, 26 al 28 de octubre 16 de 2007, Piria´polis, Uruguay. 17 Acknowledgements Frick M., Williams K., Pierrad L. (2001) Summertime foraging 18 and feeding by immature Loggerhead sea turtles (Caretta 19 The fieldwork was done with the kind collaboration of caretta) from Georgia. Chelonian Conservation and Biology, 20 Alejandro Fallabrino, Philip Miller and Ernesto ‘Coca’ 4, 178–181. 21 and all the crew of the Fishing Ship Floppy. Financial sup- Giberto D.A., Bremec C.S., Schejter L., Schiarti A., Mianzan 22 port from The Rufford Small grants for Nature Conserva- H., Acha E.M. (2006) The invasive rapa whelk Rapana 23 tion to A.C. is acknowledged. Leandro Bugoni is also venosa (Valenciennes 1846): status and potential ecological 24 acknowledged for sharing relevant literature. impacts in the Rı´o de la Plata estuary, -Uruguay. 25 Journal of Shellfish Research, 25, 919–924. 26 Guerrero R.A., Lasta C.A., Acha E.M., Mianzan H.W., Fram- References 27 in˜an M.B. (1997). Atlas Hidrogra´fico del Rı´o de la Plata. ????, 28 Almeida A.P., Baptistotte C., Schineider J.A. (2000) Logger- Buenos Aires: 109 pp. 6 29 head turtle tagged in Brazil found in Uruguay. Marine Harding J.M. 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