Corbicula Fluminea As New Food Resource for Native and Exotic

Home , Corbicula fluminea

NORTH-WESTERN JOURNAL OF ZOOLOGY 14 (1): 37-43 ©NWJZ, Oradea, Romania, 2018 Article No.: e171502 http://biozoojournals.ro/nwjz/index.html

Corbicula fluminea (Mollusca: Bivalvia) as a new food resource for native and exotic terrapins occurring in NW Iberian Peninsula: an ex situ experiment

Noé FERREIRA-RODRÍGUEZ1,*, César AYRES2 and Isabel PARDO1

1. Departamento de Ecoloxía e Bioloxía Animal. Facultade de Bioloxía. Campus A Lagoas – Marcosende, Universidade de Vigo, Vigo 36310, Spain. 2. Asociación Herpetológica Española. Museo Nacional de Ciencias Naturales. C/ José Gutiérrez Abascal, 2. Madrid, 28006, Spain. *Corresponding autor, N. Ferreira-Rodríguez, Tel: +34 986 812585 Fax: +34 986 812556, E-mail: [email protected]

Received: 14. March 2016 / Accepted: 30. January 2017 / Available online: 19. March 2017 / Printed: June 2018

Abstract. Invasive terrapin species have a major impact on freshwater ecosystems, threatening the endangered species Emys orbicularis. In addition to the widely introduced Mauremys leprosa and Trachemys scripta, new exotic species from the genus Graptemys and Sternotherus are being released in the environment. Furthermore, basins where native and exotic terrapins co-occur have been invaded by the Asian clam Corbicula fluminea. In this work we investigated diet breadth and degree of trophic overlap for one native and four exotic species. Additionally, we aimed to explore the potential of native and exotic terrapins to feed upon C. fluminea. Comparisons among two known E. orbicularis populations were performed to determine if long term co-occurrence with C. fluminea leads to an adaptive feeding behaviour. Our results suggest diet overlap and strong kinematic differences among native and exotic terrapins, with greater feeding capabilities and a competitive advantage for the exotic species. In this regard, the opportunistic behaviour of exotic species contrasts with the adaptive pattern of the native species. Based on our findings, we speculate about three plausible terrapin responses to C. fluminea invasion.

Key words: facilitation, Emys orbicularis, invasive species, interspecific competition.

Introduction (Müller, 1774). Since 1980, C. fluminea has colonized many European river basins, from the Iberian Peninsula in the Biological invasions are an important component of global southwest to Ireland and UK in the north and to Bulgaria change and are a major driver of global biodiversity loss (Vi- and Romania in the east affecting the ecosystems’ structure tousek et al. 1997, Sala et al. 2000). Invasive species interact and functioning (Mouthon 1981, Sousa et al. 2005, Crespo et in many different ways with the species in the recipient al. 2015). The effects of the species on the areas it invades are community, both negatively and positively, or simply cause mostly negative (Boltovskoy et al. 1995). In general, C. reorganization of co-occurrence patterns in native species fluminea has the potential to reduce phytoplankton abun- (Sanders et al. 2003, Brooker et al. 2008). The damage done dance (Cohen et al. 1984, Leff et al. 1990), compete with na- by invasive species on native communities have long been tive bivalves (Strayer 1999, Yeaguer et al. 1999) and modify recognized (Mooney & Cleland 2001). Often, invasive spe- substrate characteristics (Sousa et al. 2009, Sousa et al. 2014). cies interact with one another increasing the impacts upon Additionally, recent studies indicate the existence of positive the recipient community, a process termed ‘invasional melt- effects of C. fluminea on ecosystems, because the accumula- down’ (Simberloff & Von Holle 1999). This interaction be- tion of empty shells provides a suitable habitat for the pro- tween invaders usually involves exotic prey facilitating ex- liferation of typical hard-substrate species (e.g. mayﬂy Caenis otic predators in a one-way facilitation process (Simberloff spp.) on a soft-benthic surface (Gutiérrez et al. 2003, Werner 2006, DeVanna et al. 2011, Meza-Lopez & Siemann 2015). & Rothhaupt 2007). The invasive pond slider, Trachemys scripta (Schoepff, Here we examine the potential of C. fluminea as a new 1792), is the most commonly traded and over-exploited ani- food resource for native and exotic terrapin species, using mal worldwide (Lowe et al. 2000). Since its importation into the case example of the process already occurring in Galician the European Union was banned, the European pet industry inland waters (NW Iberian Peninsula). Our working hy- shifted to trading new species from the genera Graptemys pothesis was that the opportunistic feeding behaviour of ex- and Sternotherus, which include five of the most exported otic terrapins provides a competitive advantage over native turtles from the US (Kopecký et al. 2013, Mali et al. 2014). terrapins following an adaptive feeding behaviour in re- These new imported species are being released in the envi- sponse to C. fluminea invasion. Finally, we speculate about ronment by their owners, with the potential risk that repre- three plausible scenarios concerning native and exotic terra- sent the establishment of naturalized populations for native pin responses to C. fluminea invasion. species (Ayres et al. 2013, García et al. 2015). In addition, the Mediterranean stripe-necked terrapin Mauremys leprosa (Schweiger, 1812) has been widely introduced in an attempt Material and methods to control slugs in gardens (Pleguezuelos 2002). Study site and background The introduction of invasive terrapins has the potential We investigated diet breadth and degree of trophic overlap for to threaten the endangered European pond turtle Emys or- native and exotic species co-occurring in the autonomous Commu- bicularis (Linnaeus, 1758), mainly via resource competition nity of Galicia (NW Iberian Peninsula, Spain). Galicia has an area of (food and space) and pathogen transmission (Cadi & Joly 29,434 km2, characterized by the existence of an extensive hydro- 2003, Pérez-Santigosa et al. 2008, Verneau et al. 2011, Polo- graphic network. The topography of the region determines the exis- Cavia et al. 2014, Iglesias et al. 2015). In Europe, many river tence of short watercourses draining into the Cantabrian-Atlantic Sea basins where native and invasive terrapin species co-occour and rivers with steep slopes draining into the Atlantic Ocean. Emys orbicularis is the most endangered reptile in Galicia with have also been invaded by the Asian clam Corbicula fluminea only three large population groups known in the region (Rivera & 38 N. Ferreira-Rodríguez et al.

Table 1. List of operational taxonomic units into which prey items were grouped and frequency from literature reports of target terrapin’s diet.

Species Reference Country N Porifera Turbellaria Mollusca Annelida Arthropoda Vertebrata Algae Vegetables Seeds Emys orbicularis Çiçek & Ayaz 2011 Turkey 118 _ _ 5 2 18 49 _ 38 _ Ottonello et al. (2005) France 27 _ _ 37 _ 88.9 3.7 _ 88.9 _ Kotenko (2000) Ukraine 17 5.88 _ 88.24 _ 100 41.18 _ 82.35 _ Pérez-Santiagosa et al. (2011) Spain 2 _ _ 50 _ 100 _ _ _ _ Pérez-Santiagosa et al. (2011) Spain 18 _ _ 5.6 _ 100 6 _ 33.3 _ Mauremys leprosa Pérez-Santiagosa et al. (2011) Spain 16 _ _ 0 12.5 50 6.25 _ 100 _ Pérez-Santiagosa et al. (2011) Spain 15 _ _ 0 _ 80 6.7 _ 40 _ Trachemys scripta Pierce (1992) USA 14 _ _ 8.3 _ 66.7 16.7 _ 100 _ Lindeman (2000) USA 55 _ 2 11 4 29 44 42 22 2 Dreslik (1999) USA 27 _ _ 0 _ 50 63 38 63 _ Prévot-Julliard et al. (2007) France 22 _ _ 0 _ 63.63 45.45 _ 95.45 _ Pérez-Santiagosa et al. (2011) Spain 12 _ _ 58.3 _ 50 _ _ 75 _ Pérez-Santiagosa et al. (2011) Spain 8 _ _ 0 _ 50 _ _ 37.5 _ Sternotherus odoratus Patterson and Lindeman (2009) USA 34 _ _ 94 _ 62 6 15 74 15 Wilhelm and Plummer (2012) USA 17 _ _ 80 _ 53 _ 8.3 31.7 48.3 Ford and Moll (2004) USA 239 _ _ 81.92 _ 85.77 12.31 44.62 95.39 63.3 Graptemys pseudogeographica Lindeman (2000) USA 51 10 4 _ _ 27 12 25 _ 2 Moll (1976) USA 80 _ _ 1.2 _ 78 2.5 _ 56.2 _ Vogt (1981) USA 38 _ _ 55 _ 39 28 _ 63 _ Moll (1976) USA 35 _ _ 2.8 _ 100 2.8 _ _ 17.1

Fernández 2004). As part of a broader study on the parasitic status of plied with dechlorinated water in an outdoor facility which allowed E. orbicularis (Iglesias et al. 2015), faeces of one individual captured in the maintenance of ambient temperature and photoperiod (23.13 ± one of the populations (Centeáns ponds: Louro river valley) in April 0.54ºC and 15 h light: 9 h dark). The water depth of the aquarium 2015 were composed primary by C. fluminea shell fragments from was 6.5 cm, such that all turtles could keep their feet on the bottom which evidence we designed this study. (Nishizawa et al. 2014). Corbicula fluminea individuals were collected by hand in near- Diet comparisons shore areas in the River Miño (latitude: -48.816775°, longitude: Following the study by Lindeman (2000), we performed a cluster 6.369403°). In general, exotic terrapins are released into natural eco- analysis based on the data of a community resource-use matrix (a systems by their owners when they reach adult size (Cadi et al. species by diet category matrix, Table 1). The objective was to evalu- 2014). Hence, in order to homogenize experimental conditions and ate the interspecific interactions (competition) in determining food based on previous works (Mitchell 1988, Keller 1997, Lindeman resource use of five target species: the native species E. orbicularis; 2000b, Pérez-Santigosa et al. 2008), all turtles used in the experiment the introduced M. leprosa, the exotic invasive T. scripta and the exot- were considered adults and reflect the largest individuals (average ics G. pseudogeographica (LeSueur, 1817) and S. odoratus (Latreille in plastron length ± SD) that can be found in the environment: E. orbicu- Sonnini & Latreille, 1801). laris (150.02 ± 13.75 mm), M. leprosa (137.80 ± 26.64 mm), T. scripta We reviewed the literature by searching titles, abstracts, and (179.50 ± 15.76 mm), G. pseudogeographica (129.75 ± 33.3 mm) and S. keywords of articles characterizing freshwater turtle diets using the odoratus (78.04 ± 5.34 mm). Males and females were not sexually dif- Institute for Scientiﬁc Information (ISI) Web of Science and ferentiated in the experiment. Turtles were randomly distributed in Google.com search engines in July – August 2015. We screened the aquariums (one turtle was placed in each). Due to the small popula- available abstracts of peer-review articles focused on the five target tion size and the endangered status of E. orbicularis only four speci- species. We used the different diet data obtained for each species mens (replicates) were included in the experiment. The total number into a single matrix as mean percent frequency of occurrence (%F). of turtles used in the experiment was 20 (5 species × 4 turtles) and Only those works containing detailed information about different each was considered one replicate (four replicates per species). prey items were considered for the analysis. We also grouped the re- The density and size of bivalves used in the experiment reflected sulting prey items into one of nine categories (prey taxon): Porifera, the average found in Atlantic estuaries (ca. 400 ind. m-2; Ferreira- Turbellaria, Mollusca, Annelida, Arthropoda, Vertebrata, Algae, Rodríguez & Pardo 2014). Sixty clams per aquarium ranging from 5 Plants and Seeds. When prey items (e.g. Gastropods and Bivalves) to 25 mm were measured with a digital calliper and assigned to one presented different frequency of occurrence inside the same category of four established categories (5 mm shell length increment in the an- (e.g. Mollusca), the greatest was chosen for each category. If results tero-posterior axis, from 5 to 25 mm). At the end of the test period of from a single study made distinction between adult/juveniles or 72-hours, the final number of consumed clams per size class was cal- male/female individuals, adult male were prioritized. culated by subtracting retrieved individuals from the number of clams added. Prey size selection According to Hiddink et al. (2002), the selectivity was estimated Experimental animals were obtained from captivity, semi-natural by the Electivity index, E’. E’ was calculated per size class as: E’= (ci - conditions or areas where C. fluminea has never been recorded: E. or- oi)/ (ci + oi) where ci is number of consumed bivalves per size class bicularis (Avia River), M. leprosa (Avia River), T. scripta (semi- and oi the expected consumption per size class (total number con- natural), G. pseudogeographica (captivity), S. odoratus (captivity). Tur- sumed in the experiment divided by the number of size classes). tles were starved for 48 hours prior to the experiment in 60 litres Positive E’ values indicate a preference, negative ones – rejection. plastic aquariums (50 cm × 30 cm × 30 cm). Aquariums were sup- Size classes that were not eaten at all get the E’-value -1. Terrapins adaptation to Corbicula fluminea 39

Emys orbicularis adaptability In order to determine E. orbicularis adaptability to C. fluminea as a new food item, the predation rate of individuals from two large population groups (Louro river valley and Avia River), were exam- ined in a parallel experiment. The first locality, Centeáns ponds at Louro river valley, was invaded by C. fluminea around 2008 (Ayres 2008), while in the second one at Avia River, the invasive clam has never been recorded. Size classes of turtles used in this second experiment were selected to reflect the largest individuals found in Centeáns ponds (average plastron length ± SD: 147.77 ± 17.94 mm) and Avia River (average plastron length ± SD: 153.01 ± 7.81 mm). The total number of turtles used in this experiment was 8 (2 localities × 4 turtles) and each was considered one replicate (four replicates per locality). For this experiment we followed the same methodology as the one used in “Prey size selection” experiment with E. orbicularis Figure 1. Dendrogram (GAAC cluster analyses) summarizing diet re- as predator and C. fluminea as prey. lationships between terrapin species. (So, Sternotherus odoratus; Ts,

Trachemys scripta; Eo, Emys orbicularis; Ml, Mauremys leprosa; Gp, Kinematics and morphological measurements Graptemys pseudogeographica). In addition to the standard measure of plastron length (PL), two morphological parameters, head width (HW) and head height (HH) were measured in each species in an attempt to correlate morpho- item. The electivity index E’ per size class indicates a posi- logical differences with variation in resource use. HW was measured tive selection of M. leprosa and S. odoratus for clams smaller to the nearest 0.1 mm with a Vernier calliper at the greatest width of than 10 mm (E’ > 0). T. scripta positively selected clams the head in a plane with the upper jaw, and HH was measured from smaller than 15 mm (E’ > 0) and avoided the size class 15–19 the basis of the lower jaw to the top the upper jaw. mm (E’ < 0). Larger clams were avoided by G. pseu- Data analysis dogeographica which only fed positively on the 5–9 mm clam Diet analysis - Statistical analyses were performed using the software size class (E’ > 0). The single significant selection was for S. package PRIMER 6. The clustering algorithm used was the Group- odoratus on the smallest clams (t-test = 7.333, d.f. = 2, p = average agglomerative clustering or GAAC. Euclidean distances 0.018). For the rest of the species the differences between were used. positive or negative size classes selection were not statisti- Size selection and Emys orbicularis adaptability - Statistical analyses cally significant (Fig. 2). were performed using SPSS v. 20. E’-values were compared among species (or localities) by using non-parametric Mann-Whitney U-test, as transformation did not normalize the data. The significance of selection was tested with a t-test comparing ci and oi per size class, from all replicates. Prior analysis data were log-transformed. Prefer- ence or avoidance in selectivity is rated significant if ci and oi differ significantly (t-test, p<0.05). Kinematics – Statistical analyses were performed using SPSS v. 15. Tests for differences among species were conducted by using t- test for a standardized animal of 100 mm of plastron length (PL). Spearman correlations coefficients of clam number and size class selections with head morphology (HW and HH, in mm), and standardized head morphology of a 100 mm individual (HW standardized and HH standardized in mm), were calculated by species.

Results

Diet comparisons Our review on diet data and their similarity resulted in a Figure 2. The electivity index E’ of five terrapin species relative to C. predicted specific pattern on dietary habits between species. fluminea size class. Positive E’ values indicate positive selection of the size class and negative values rejection. Bars represent 1 Stan- Diet data from a total of 845 individual terrapins were ob- dard Error. tained from the literature: E. orbicularis (n=182), M. leprosa (n=31), T. scripta (n=138), G. pseudogeographica (n=408) and S. odoratus (n=290). The pattern presented in Figure 1 shows a Emys orbicularis adaptability bifurcated tree where the kinosternid S. odoratus splits as the Emys orbicularis’ electivity index E’ per size class indicates most different group from the other four species in the that individuals from Centeáns ponds (Louro river valley) GAAC dendrogram. Between these, the dietary overlap was positively selected clams smaller than 10 mm (E’ > 0), while highest between the emydids E. orbicularis and T. scripta, and avoiding larger clams (E’ < 0). Either positive or negative between the batagurid M. leprosa and the emydid G. pseu- size class selections were not statistically significant. On the dogeographica. other hand, individuals of the species from the Avia River did not select C. fluminea as food item (E’ = 0). Prey size selection The size selection experiment suggests that the native E. or- Kinematics bicularis was unable to feed upon C. fluminea as a new food The kinematic results derived from head measurements and

40 N. Ferreira-Rodríguez et al.

Table 2. Standardized head morphological variables (head width (HW) and head height (HH)) ± standard deviation for a 100 mm (PL) terrapin.

Variable E. orbicularis M. leprosa T. scripta S. odoratus G. pseudogeographica N 3 5 2 4 4 HW (mm) 17.70 (1SD: 0.25) 17.48 (1SD: 0.30) 17.11 (1SD: 0.57) 22.44 (1SD: 0.33) 18.29 (1SD: 0.69) HH (mm) 12.62 (1SD: 0.32) 9.50 (1SD: 1.30) 12.95 (1SD: 0.13) 16.99 (1SD: 0.40) 13.40 (1SD: 0.30)

Table 3. T-test comparisons between standardized head morphological measures of the 5 studied species (PL=100 mm). Bold indicate significant differences for one or both kinematic variables characterizing terrapins head.

HW HH Species t-test d.f. p-value t-test d.f. p-value E. orbicularis*M. leprosa 0.494 6 0.639 1.783 6 0.125 E. orbicularis*T. scripta 0.116 3 0.346 -0,783 3 0.491 E. orbicularis*S. odoratus -10.553 5 0.000 -8.094 5 0.000 E. orbicularis*G. pseudogeographica -0.689 5 0.521 -1.762 5 0.138 M. leprosa*T.scripta 0.637 5 0.552 -1.579 5 0.175 M.leprosa*S. odoratus -10.924 7 0.000 -4.934 7 0.002 M. leprosa*G. pseudogeographica -1.148 7 0.289 -2.598 7 0.036 T. scripta*S. odoratus -8.698 4 0.001 -6.787 4 0.002 T. scripta*G. pseudogeographica -1.075 4 0.343 -1.022 4 0.365 S. odoratus*G. pseudogeographica 5.374 6 0.002 7.256 6 0.000

Table 4. Spearman correlation analyses between morphological measures and clam prey selection (n = 18).

HW HH Non-standarized Standarized Non-standarized Standarized r p r p r p r p Clam number -0.341 0.167 0.208 0.408 0.046 0.857 0.543 0.020 5–9 -0.112 0.658 0.324 0.190 0.165 0.513 0.409 0.092 10–14 0.547 0.019 0.274 0.271 0.550 0.018 0.006 0.982 Size class (mm) 15–19 0.546 0.019 0.273 0.274 0.549 0.018 0.000 1.000 20–24 0.547 0.019 0.274 0.271 0.550 0.018 0.006 0.982

the statistical tests applied (Tables 2, 3) indicated that S. odo- Shively & Vidrine 1984, Lindeman 2000, 2006, Wilhelm & ratus had a significantly higher HW and HH than the other Plummer 2012, Richards-Dimitrie et al. 2013). Moreover, a four species. On the other hand, M. leprosa presented the shift to a C. fluminea based diet was reported in other Grap- smallest HH values, which also differed significantly from temys and Sternotherus species (Lindeman 2006, Atkinson G. pseudogeographica. 2013, Selman & Lindeman 2015). HH standardized values were positively correlated (Ta- In our diet comparison analysis we studied only the food ble 4) with the number of eaten clams. Non-standardized resource dimension because all five species have the poten- variables HW and HH were positively correlated with terra- tial to overlap in their basking substrate preferences, with pin selection of the three higher clam size classes (Table 4). the exception of S. odoratus which exhibits bottom-walking habits (Ernst 1986, Janzen et al. 1992, Lindeman 1999, 2000, Cadi & Joly 2003). As shown by Lindeman (2000), our results Discussion can be explained through similar feeding habits of phylogenetically related species which necessarily leads to competi- Our results revealed an opportunistic feeding behaviour of tion for resources (MacArthur & Levins 1967, Tucker et al. exotic terrapins compared to native terrapins, which may 1995). Our data review confirmed these findings and sup- follow an adaptive way in the acquisition of C. fluminea as port the existence of food competition among phylogeneti- new food item. The capacity of exotic species to feed on C. cally related species (Lindeman 2000, Sfenthourakis et al. fluminea in invaded areas may provide an advantage over 2005, Segurado et al. 2012). In one side, our GAAC analyses native species which were less efficient in the use of this new indicated that G. pseudogeographica will have the potential to food resource. outcompete native species. On the other hand, S. odoratus Our findings were in agreement with those obtained for was the most dissimilar species, an outgroup in food re- G. pseudogeographica and S. odoratus in their native habitats, source use and phylogenetically distant from the other four where the species actively feed on Zebra (Dreissena polymor- studied species (Gaffney & Meylan 1988, Guillon et al. 2012). pha) and Quagga mussels (D. bugensis) after their invasion The main implication of these diet differences is that it (Lindeman 2006, Bulté & Blouin-Demers 2008, Patterson & probably allows the two exotic terrapin species to coexist Lindeman 2009). The use of C. fluminea as food item has also without competition for food resources but they may dis- been reported for three Nearctic exotic species (T. scripta, G. place native species. Therefore, studies comparing life his- pseudogeographica and S. odoratus) in invaded areas but never tory attributes between species would be important to assess for the native E. orbicularis and M. leprosa (Ford & Moll 2004, invasion risk and detect indicative traits of inter-speciﬁc Terrapins adaptation to Corbicula fluminea 41 competition (Segurado & Figueiredo 2007). E. orbicularis, creating scope for adaptive change. Secondly, We know little about how the invasive C. fluminea could due to their feeding capabilities, T. scripta, S. odoratus and G. facilitate the establishment and success of exotic predators. pseudogeographica could become abundant and it could pro- Nevertheless, our results have shown that the introduced C. vide biotic resistance against C. fluminea invasion. Thirdly, in fluminea is a potential food item easily exploited by exotic the case of M. leprosa, its kinematic characteristics are pre- terrapin species. By contrast, the effect on the native E. or- venting C. fluminea feeding capability and the potential bicularis requires an adaptive period for recognition of C. competition with other exotic species should indirectly lead fluminea as food resource. We note large differences in the to its disadvantage. exploitation of this new food item between native and exotic In conclusion, under the possibility of these future sce- terrapins. For the native E. orbicularis, after an adaptive pe- narios, as other authors have suggested, governments riod of a few years co-occurring with the invasive clam, the should regulate the importation of species and activate early species is able to feed upon small individuals. In contrast, warning and rapid response frameworks to prevent new in- despite that adult T. scripta specimens switch to a herbivo- vasions, more economic and efficient measures than poste- rous diet as they mature (Bouchard & Bjorndal 2006), ex- rior control interventions (Cadi & Joly 2003; Bellard et al. perimental animals directly fed on a wide size rage of clams 2013). Therefore, studies focused on other terrapin species in the first contact with the species, reflecting its opportunis- and their assessment for invasion risk may be required be- tic feeding behaviour (reviewed by Ramsay et al. 2007, fore importation of new species. Pérez-Santigosa et al. 2011). Nevertheless, a longer period without feeding could have influenced C. fluminea consumption. Acknowledgments. We thank Claudio M. Padilla for his help in Kinematics was found to be determinant in the ability of statistical analyses. We thank to Luis González Rodríguez and Rubén different species to feed upon diverse clam sizes. Collins and Forján Castro (Plant and Soil Science Group, University of Vigo) for Lindeman (2006) pointed out that body size and trophic providing the installations. We thank to Pablo Garcia-Diaz for his morphology of G. pseudogeographica influence the size of comments and suggestions that greatly improved the manuscript. molluscan prey consumed. Therefore, the exotic species We also thank the three anonymous reviewers for their constructive which are able to feed on bigger clams (e.g. T. scripta, G. comments. Financial support (to N. F-R.) came from a pre-doctoral pseudogeographica and S. odoratus) will have an advantage fellowship from the autonomous government of Galicia (Xunta de over the native ones that cannot (Carlson et al. 2009, Galicia Plan I2C, PRE/2013/400).

DeVanna et al. 2011, Jackson 2015). These results demon- strated differences in the exploitation of resources by the studied species. As shown, kinematic characteristics are References roughly related to number and size of consumed clams (in- Amarasekare, P. (2003): Competitive coexistence in spatially structured dicated by the correlation with head morphological meas- environments: a synthesis. Ecology Letters 6: 1109-1122. ures). A more efficient use of C. fluminea as a food resource Atkinson, C.L. (2013): Razor-backed musk turtle (Sternotherus carinatus) diet occurred in the highest height and broadest head species (S. across a gradient of invasion. Herpetological Conservation and Biology 8: odoratus), the most molluscivorous species (Table 1; Teran et 561-570. Ayres, C. (2008): A new record of Asian clam Corbicula fluminea (Müller, 1774) al. 1996, Lindeman 2000). On the other hand, all species feed in Galicia (Iberian Peninsula) - Ribeiras do Louro e Gandaras de Budiño upon the smaller clams despite of their capability to feed wetland. Aquatic Invasions 3: 439-440. upon larger ones which likely reflects a preference for food Ayres, C., Calviño, M., Cordero-Rivera, A. (2010): Water lilies, Nymphaea alba, in the summer diet of Emys orbicularis in northwestern Spain: use of emergent items easier to obtain (MacArthur & Pianka 1966). resources. Chelonian Conservation and Biology 9: 128-131. One of the primary explanations for the success of in- Ayres, C., Alvarez, A., Ayllon, E., Bertolero, A., Buenetxea, X., Cordero-Rivera, vaders is the absence of competitors. Previous works based A., Curco-Masip, A., Duarte, J., Farfan, M.A., Ferrandez, M., Franch, M., Fortuño, L., Guerrero. J., Hernandez-Sastre, P.L., Lacomba, I., Lorente, L., on E. orbicularis faeces analysis did not show evidence of Miguelez-Carbajo, D., Pinya, S., Rada, V., Romero, D., Sanchez, J., Sancho, changes in invertebrate community composition after C. V., Valdeon, A. (2013): Conservation projects for Emys orbicularis in Spain. fluminea invasion (Ayres et al. 2010, Iglesias et al. 2015). Herpetology Notes 6: 157-164. Bellard, C., Thuiller, W., Leroy, B., Genovesi, P., Bakkenes, M., Courchamp, F. Hence, in addition to shared trophic resources by native and (2013): Will climate change promote future invasions? Global Change exotic species (mainly arthropods), the introduction of C. Biology 19: 3740-3748. fluminea in Galician watercourses represent a new food item Boltovskoy, D., Izaguirre, I., Correa, N. (1995): Feeding selectivity of Corbicula more efficiently exploited for exotic terrapins which could fluminea (Bivalvia) on natural phytoplankton. Hydrobiologia 312: 171-182. Bouchard, S.S., Bjorndal, K.A. (2006): Ontogenetic diet shifts and digestive constitute an opportunistic advantage over the native E. or- constraints in the omnivorous freshwater turtle Trachemys scripta. bicularis. In this regard, previous findings have shown that Physiological and Biochemical Zoology 79: 150-158. under co-occurrence of native and exotic species in the same Brooker, R.B., Maestre, F.T., Callaway, R.M., Lortie, C.L., Cavieres, L.A., Kunstler, G., Liancourt, P., Tielbörger, K., Travis, J.M.J., Anthelme, F., ponds, competition can lead to ecological displacement of Armas, C., Coll, L., Corcket, E., Delzon. S., Forey, E., Kikvidze, Z., Olofsson, native species to other resources or even to competitive ex- J., Pugnaire, F., Quiroz, C.L., Saccone, P., Schiffers, K., Seifan, M., Touzard, clusions (Amarasekare 2003). Hence, the biotic interactions B., Michalet, R. (2008): Facilitation in plant communities: the past, the present, and the future. Journal of Ecology 96: 18-34. (e.g. space competition) among these native and exotic ter- Bulté, G., Blouin-Demers, G. (2008): Northern map turtles (Graptemys rapin species will determine the structure of future terrapin geographica) derive energy from the pelagic pathway through predation on assemblages (Morin 1999). zebra mussels (Dreissena polymorpha). Freshwater Biology 53: 497-508. Cadi, A., Joly, P. (2003): Competition for basking places between the According to Carlsson et al. (2009), here we speculate endangered European pond turtle (Emys orbicularis galloitalica) and the about three plausible terrapin responses to C. fluminea inva- introduced Red eared slider (Trachemys scripta elegans). Canadian Journal of sion. Firstly, C. fluminea fits within the feeding capabilities of Zoology 81: 1392-1398.

42 N. Ferreira-Rodríguez et al.

Cadi, A., Delmas, V., Prévot‐Julliard, A. C., Joly, P., Pieau, C., Girondot, M. Lowe, S.J., Browne, M., Boudjelas, S. (2000): 100 of the world’s worst invasive (2004): Successful reproduction of the introduced Slider turtle (Trachemys alien species. IUCN/SSC Invasive Species Specialist Group (ISSG). scripta elegans) in the south of France. Aquatic Conservation: Marine and Auckland, New Zealand. Freshwater Ecosystems 14: 237-246. MacArthur, R.H., Pianka, E.R. (1966): On the optimal use of a patchy Carlsson, N.O.L., Sarnelle, O., Strayer, D.L. (2009): Native predators and exotic environment. American Naturalist 100: 603-609. prey – an acquired taste? Frontiers in Ecology and the Environment 7: 525- Macarthur, R., Levins, R. (1967): Limiting similarity, convergence and 532. divergence of coexisting species. American Naturalist 101: 377-387. Çiçek, K., Ayaz, D. (2011): Food composition of the European pond turtle (Emys Mali, I., Vandewege, M., Davis, S.K., Forstner, M.R.J. (2014): Magnitude of the orbicularis) in Lake Sülüklü (Western Anatolia, Turkey). Journal of freshwater turtle exports from the US: long term trends and early effects of Freshwater Ecology 24: 571-578. newly implemented harvest management regimes. Plos One 9: 1-10. Cohen, R.R.H., Dresler, P., Phillips, E., Cory, R.L. (1984): The effect of the Meza-López, M., Siemann, E. (2015): Experimental test of the Invasional Asiatic clam, on phytoplankton of the Potomac River, Maryland. Limnology Meltdown Hypothesis: an exotic herbivore facilitates an exotic plant, but the and Oceanography 29: 170-180. plant does not reciprocally facilitate the herbivore. Freshwater Biology 60: Collins, D., Lindeman, P.V. (2006): The influence of body size and trophic 1475-1482. morphology on the size of molluscan prey of female Texas map turtles Mitchell, J.C. (1988): Population ecology and life histories of the freshwater (Graptemys versa). Herpetological Review 37: 416-418. turtles Chrysemys picta and Sternotherus odoratus in an urban Lake. Crespo, D., Dolbeth, M., Leston, S., Sousa, R., Pardal, M.A. (2015): Distribution Herpetological Monographs 2: 40-61. of Corbicula fluminea in the invaded range: a geographic approach with notes Moll, D. (1976): Food and feeding strategies of the Ouachita map turtle on species traits variability. Biological Invasions 17: 2087-2101. (Graptemys pseudogeograica ouachitensis). American Midland Naturalist 96: DeVanna, K., Bodamer, B.L., Wellington, C.G., Hammer, E., Mayer, C.M., 478-482. Bossenbroek, J.M. (2011): An alternative hypothesis to invasional meltdown Mooney, H.A., Cleland, E.E. (2001): The evolutionary impact of invasive in the Laurentian Great Lakes region: facilitation by Dreissena. Journal of species. PNAS 98: 5446-5451. Great Lakes Research 37: 632-641. Mouthon, J. (1981): Sur la présence en France et au Portugal de Corbicula Dreslik, M.J. (1999): Dietary notes on the Red-eared slider (Trachemys scripta) (Bivalvia, Corbiculidae) originaire d’Asie. Basteria 45: 109-116. and River cooter (Pseudemys concinna) from southern Illinois. Transactions of Nishizawa, H., Tabata, R., Horia, T., Mitamura, H., Arai, N. (2014): Feeding the Illinois State Academy of Science 92: 233-241. kinematics of freshwater turtles: what advantage do invasive species Ernst, C.H. (1986): Ecology of the turtle, Sternotherus odoratus, in southeastern possess? Zoology 117: 315-318. Pennsylvania. Journal of Herpetology 20: 341-352. Ottonello, D., Salvidio, S., Rosecchi, E. (2005): Feeding habits of the European Ferreira-Rodríguez, N., Pardo, I. (2014): Abiotic controls on population pond terrapin Emys orbicularis in Camargue (Rhône delta, Southern France). structure of the invasive Corbicula fluminea (Müller, 1774) in the River Miño Amphibia-Reptilia 26: 562-565. estuary. Fundamental and Applied Limnology 184: 329-339. Patterson, J.C., Lindeman, P.V. (2009): Effects of Zebra and Quagga mussel Ford, D.K., Moll, D. (2004): Sexual and seasonal variation in foraging patterns (Dreissena spp.) invasion on the feeding habits of Sternotherus odoratus in the Stinkpot, Sternotherus odoratus, in southwestern Missouri. Journal of (Stinkpot) on Presque Isle, northwestern Pennsylvania. Northeastern Herpetology 38: 296-301. Naturalist 16: 365-374. Gaffney, E.S., Meylan, P.A. (1988): A phylogeny of turtles. pp 157-219.In: Pérez-Santigosa, N., Diaz-Paniagua, C., Hidalgo-Vila, J. (2008): The Benton, M.J. (eds.), The Phylogeny and Classification of the Tetrapods. reproductive ecology of exotic Trachemys scripta elegans in an invaded area of Clarendon Press, Oxford. southern Europe. Aquatic Conservation 18: 1302-1310. García‐Díaz, P., Ross, J.V., Ayres, C., Cassey, P. (2015): Understanding the Pérez-Santigosa, N., Florencio, M., Hidalgo-Vila, J., Díaz-Paniagua, C. (2011): biological invasion risk posed by the global wildlife trade: propagule Does the exotic invader turtle, Trachemys scripta elegans, compete for food pressure drives the introduction and establishment of Nearctic turtles. with coexisting native turtles? Amphibia-Reptilia 32: 167-175. Global Change Biology 2: 1078-1091. Pierce, L. (1992): Diet content and overlap of six species of turtle among Wabah Guillon, J.M., Guéry, L., Hulin, V., Girondot, M. (2012): A large phylogeny of River. Eastern Illinois University, Illinois. turtles (Testudines) using molecular data. Contributions to Zoology 81: 147- Pleguezuelos, J.M. (2002): Atlas y libro rojo de los anfibios y reptiles de España. 158. Dirección General de Conservación de la Naturaleza, Madrid. Gutiérrez, J.L., Jones, C.G., Strayer, D.L., Iribarne, O.O. (2003): Mollusks as Polo-Cavia, P., López, P., Martín, J. (2014): Interference competition between ecosystem engineers: the role of shell production in aquatic habitats. Oikos native Iberian turtles and the exotic Trachemys scripta. Basic and Applied 10: 79-90. Herpetology 28: 5-20. Hiddink, J.G., Marijnissen, S.A.E., Troost, K., Wolff, W.J. (2002): Predation on 0- Prévot-Julliard, A.-C., Gousset, E., Archinard, C., Cadi, A., Girondot, M. (2007): group and older year classes of the bivalve Macoma balthica: interaction of Pets and invasion risks: is the Slider turtle strictly carnivorous? Amphibia- size selection and intertidal distribution of epibenthic predators. Journal of Reptilia 28: 139-143. Experimental Marine Biology and Ecology 269: 223-248. Ramsay, N.F., Ng, P.K.A., O’Riordan, R.M., Chou, L.M. (2007): The Red-eared Iglesias, R., García-Estévez, J.M., Ayres, C., Acuña, A., Cordero-Rivera, A. slider (Trachemys scripta elegans) in Asia: a review. Biological Invaders in (2015): First reported outbreak of severe spirorchiidiasis in Emys orbicularis, Inland Waters: Profiles, Distribution, and Threats 2:161-174. probably resulting from a parasite spillover event. Diseases of Aquatic Richards-Dimitrie, T., Gresens, S.E., Smith, S.A., Seigel, R.A. (2013): Diet of Organisms 113: 75-80. northern Map turtles (Graptemys pseudogeographica): sexual differences and Jackson, M.C. (2015): Interactions among multiple invasive animals. Ecology 96: potential impacts of an altered river system. Copeia 2013: 477-484. 2035-2041. Rivera, A.C., Fernández, C.A. (2004): A management plan for the European Janzen, F.J., Paukstis, G.L., Brodie, E.D. (1992): Observations on basking pond turtle (Emys orbicularis) populations of the Louro river basin behavior of hatchling turtles in the wild. Journal of Herpetology 26: 217-219. (Northwest Spain). Biologia, Bratislava 59: 161-171. Kopecký, O., Kalous, L., Patoka, J. (2013): Establishment risk from pet-trade Sala, O.E., Chapin, F.S., Armesto, J.J., Berlow, E., Bloomfield, J., Dirzo, R., freshwater turtles in the European Union. Knowledge and Management of Huber-Sanwald, E., Huenneke, L.F., Jackson, R.B., Kinzig, A., Leemans, R., Aquatic Ecosystems 410: art.02. Lodge, D.M., Mooney, H.A., Oesterheld, M., Poff, N.L., Sykes, M.T., Walker, Kotenko, T.I. (2000): The European pond turtle (Emys orbicularis) in the steppe B.H., Walker, M., Wall, D.H. (2000): Global Biodiversity Scenarios for the zone of the Ukraine. Stapfia 69: 87-106. Year 2100. Science 287: 1770-1774. Leff, L.G., Burch, J.L., McArthur, J.V. (1990): Spatial distribution, seston Sanders, N.J., Gotelli, N.J., Heller, N.E., Gordon, D.M. (2003): Community removal, and potential competitive interactions of the bivalves Corbicula disassembly by an invasive species. PNAS 100: 2474-2477. fluminea and Ellipo complanata, in a coastal plain stream. Freshwater Biology Segurado, P., Figueiredo, D. (2007): Coexistence of two freshwater turtle species 24: 409-416. along a Mediterranean stream: The role of spatial and temporal Lindeman, P.V. (1999): Surveys of basking map turtles Graptemys spp. in three heterogeneity. Acta Oecologica 32: 134-144. river drainages and the importance of deadwood abundance. Biological Segurado, P., Kuninc, W.E., Filiped, A.F., Araújo, M.B. (2012): Patterns of Conservation 88: 33-42. coexistence of two species of freshwater turtles are affected by spatial scale. Lindeman, P.V. (2000): Resource use of five sympatric turtle species: effects of Basic and Applied Ecology 13: 371-379. competition, phylogeny, and morphology. Canadian Journal of Zoology 78: Selman, W., Lindeman, P.V. (2015): Life history and ecology of the Pascagoula 992-1008. map turtle (Graptemys gibbonsi). Herpetological Conservation and Biology 10: Lindeman, P.V. (2000b): Evolution of the relative width of the head and 781-800. alveolar surfaces in Map turtles (Testudines: Emydidae: Graptemys). Sfenthourakis, S., Tzanatos, E., Giokas, S. (2005): Species co-occurrence: the case Biological Journal of the Linnean Society 69: 549-576. of congeneric species and a causal approach to patterns of species Lindeman, P.V. (2006): Zebra and Quagga mussels (Dreissena spp.) and other association. Global Ecology and Biogeography 15: 39-49. prey of a Lake Erie population of Common map turtles (Emydidae: Graptemys geographica). Copeia 2006: 268-273. Terrapins adaptation to Corbicula fluminea 43

Shively, S.H., Vidrine, M.F. (1984): Fresh-water mollusks in the alimentary tract Verneau, O., Palacios, C., Platt, T., Alday, M., Billard, E., Allienne, J.-F., Basso, of a Mississippi Map turtle. Proceedings of the National Academy of C., Du Preez, L.H. (2011): Invasive species threat: parasite phylogenetics Sciences 47: 27-29. reveals patterns and processes of host-switching between non-native and Shine, R. (2012): Invasive species as drivers of evolutionary change: cane toads native freshwater turtles. Parasitology 138: 1778-1792. in tropical Australia. Evolutionary Applications 5: 107-116. Vitousek, P.M., D'Aantonio, C.M., Loope, L.L.L., Rejmánek, M., Westbrooks, R. Simberloff, D., Von Holle, B. (1999): Positive interactions of nonindigenous (1997): Introduced species: a significant component of human-caused global npecies: invasional meltdown? Biological Invasions 1: 21-32 change. New Zealand Journal of Ecology 21: 1-16. Simberloff, D. (2006): Invasional meltdown 6 years later: important Vogt, R.C. (1981): Food partitioning in three sympatric species of Map turtle, phenomenon, unfortunate metaphor, or both? Ecology Letters 9: 912-919. genus Graptemys (Testudinata, Emydidae). American Midland Naturalist Sousa, R., Guilhermino, L., Antunes, C. (2005): Molluscan fauna in the 105: 102-111. freshwater tidal area of the River Minho estuary, NW of Iberian Peninsula. Wilhelm, C.E., Plummer, M.V. (2012): Diet of radiotracked Musk turtles, Annales de Limnologie, International Journal of Limnology 41: 141-147. Sternotherus odoratus, in a small urban stream. Herpetological Conservation Sousa, R., Gutiérrez, J.L., Aldridge, D. (2009): Non indigenous bivalves as and Biology 7: 258-264. ecosystem engineers. Biological Invasions 11: 2367-2385. Werner, S., Rothhaupt, K.O. (2007): Effects of the invasive bivalve Corbicula Sousa, R., Novais, A., Souza, A.T., Ilarri, M. (2014): Engineering by the invasive fluminea on settling juveniles and other benthic taxa. Journal of the North Asian clam Corbicula fluminea: effects on macrozoobenthic assemblages. 99th American Benthological Society 26:673-680. ESA Annual Convention, Safford. Yeaguer, M.M., Neves, R.J., Cherry, D.S. (1999): Competitive interactions Strayer, D.L. (1999): Effects of alien species on freshwater molluscs in North between early life stages of Villosa iris (Bivalvia: Unionidae) and adult Asian America. Journal of the North American Benthological Society 18: 74-98. clams (Corbicula fluminea). Proceedings of the First Freshwater Mollusk Teran, A.F., Vogt, R.C., Gomez, M.F.S. (1995): Food habits of an assemblage of Conservation Society Symposium, Chattanooga. five species of turtles in the Rio Guapore, Rondonia, Brazil. Journal of Herpetology 29: 536-547. Tucker, A.D., FitzSimmons, N.N., Gibbons, J.W. (1995): Resource partitioning by the estuarine turtle Malaclemys terrapin: trophic, spatial, and temporal foraging constraints. Herpetologica 5: 167-181.