First Assessment of the Impact of Recreational Fishing on the Endemic Sicilian Pond Turtle Emys Trinacris (Testudines, Emydidae)

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Herpetology Notes, volume 13: 795-800 (2020) (published online on 30 September 2020)

Sicilians are not easily hooked! First assessment of the impact of recreational fishing on the endemic Sicilian pond turtle Emys trinacris (Testudines, Emydidae)

Luca Vecchioni1,§, Alessia Cicerone1,§, Rita Scardino1, Vincenzo Arizza1, Marco Arculeo1, and Federico Marrone1,*

Abstract. The possible impact of recreational fishing on the Sicilian pond turtle Emys trinacris was investigated in two permanent water bodies in western Sicily (Italy). Overall, 120 specimens were temporarily captured and X-rayed in order to determine the possible presence of fishhooks in their mouth, throat, or gastrointestinal tract. At the studied sites, none of the X- rayed turtles showed any evidence of ingested fishhooks or other fishing gears, thus suggesting limited impact of recreational fishing. However, the occasional but not negligible findings of E. trinacris specimens injured by fishhooks or entangled in abandoned fishing lines prove the actual existence of such impact, raising some concerns about the long-term conservation of this endemic pond turtle. The need of monitoring the possible impacts of angling where pond turtles are present is briefly stressed.

Keywords. Bycatch impact, illegal angling, citizen science, wetland management, Sicily

Introduction tendency of the species (Iannella et al., 2018, and references therein), hinder the connectivity among The Sicilian endemic pond turtle Emys trinacris Fritz, local populations, so that even proximally-located Fattizzo, Guicking, Tripepi, Pennisi, Lenk, Joger and populations should be considered as independent Wink, 2005 is the only autochthonous freshwater turtle units for management purposes and threats to local occurring in Sicily. It is included (sub E. orbicularis populations should be carefully evaluated with a case- (Linnaeus, 1758)) in the Appendix II of the EU Council by-case approach (Vecchioni et al., 2020). In addition Directive 92/43/EEC (“Habitats Directive”) and in the to habitat destruction and fragmentation (Fritz et al., Appendix II of the “Bern Convention on the Conservation 2005), E. trinacris populations are also under pressure of European Wildlife and Natural Habitats”, and listed by invasive alien species (Marrone and Naselli-Flores, as “EN” (i.e.: “Endangered”) in the Italian IUCN red 2015; Ottonello et al., 2016; Naselli-Flores and Marrone, list of threatened species (Rondinini et al., 2013). 2019), hybridisation with introduced E. orbicularis Emys trinacris is widely but non-homogeneously specimens (Vamberger et al., 2015; Scardino et al., distributed in Sicily (Vamberger et al., 2015; Marrone 2020), and possibly parasite spill-over (see discussion et al., 2016; Iannella et al., 2018). Moreover, the on- in Arizza et al., 2016). Another potential threat, which going human-induced aquatic habitat fragmentation has been overlooked up to date, is recreational fishing (Fritz et al., 2005), coupled with the limited dispersal (cf. Steen et al., 2017). In sharp contrast with the detailed information available on the impact of fishing activities on sea turtles, only few data are currently available for freshwater turtles (e.g. Beregi et al., 2003; Nemoz et al., 2004; Steen et al., 2014), and no data at all are available for Italian 1 University of Palermo, Department of Biological, Chemical mainland E. orbicularis populations, nor for E. trinacris. and Pharmaceutical Sciences and Technologies (STEBICEF), Via Archirafi 18, 90123 Palermo, Italy. It is however clear that mortality related to angling * Corresponding author. �� activities can significantly contribute to the decline and § These authors contributed equally to this work local extinction of freshwater turtle populations (Nemoz 796 Luca Vecchioni et al. et al., 2004; Steen et al., 2017), and recent occasional findings of E. trinacris specimens with ingested hooks or entangled in fishing lines in western Sicily suggest that this practice may also threaten Sicilian pond turtles (Table 1). The growing concern regarding the obvious negative impact of fishing on pond turtles, and the absence of an assessment of angling impact on the endemic E. trinacris, prompted us to investigate the impact of recreational fishing on two Sicilian populations.

Materials and Methods Sampling activities were carried out in June and Figure 1. Location of the two study sites in Sicily, Italy. July 2016 in Sicily in two permanent water bodies: i) “Laghetti Coda di Riccio” (37.8736°N, 13.3997°E), located within the Nature Reserve “Bosco della Ficuzza, Rocca Busambra, Bosco del Cappelliere In the frame of this survey, E. trinacris specimens were e Gorgo del Drago” (province of Palermo), and ii) captured using baited hoop traps; in fact, the presence of “Laghetto Gorgo” (37.4080°N, 13.3269°E), located ingested fishhooks seems not to significantly inhibit the close to Montallegro (province of Agrigento) (Fig. 1). feeding behaviour of aquatic turtles (Steen et al., 2014). Both study sites are man-made lakes where recreational The hoop traps were immersed in water and equipped fishing is not allowed, but where poaching aimed at with a flotation system, so that air-breathing animals Cyprinus carpio Linnaeus, 1758 with baited hooks, and eventually caught could breathe on the surface (Ream Micropterus salmoides (Lacépedè, 1802) with baited and Ream, 1966). The traps were left in the water for hooks and fishing lures is routinely practised (pers. about 48h per session, and then checked for the possible obs.). Moreover, a dead E. trinacris specimen with presence of captured turtles. Details on sampling dates an ingested fishhook was found in “Laghetti Coda di and number of implemented traps are reported in Table 2. Riccio” in May 2015 (Table 1, Fig. 2), thus proving that All captured Sicilian pond turtles were sexed according illegal fishing is actually a threat to pond turtles in this to D’Angelo et al. (2008) and Corti et al. (2011). site. Both locations host abundant populations of the E. Captured individuals were transported to the trinacris (Arizza et al., 2014, 2016; Vamberger et al., “Laboratorio di Biologia Evoluzionistica e delle 2015). Popolazioni” at the Department STEBICEF of the

Table 1. Opportunistic observations of Emys trinacris specimens injured by fishing activities. Table 1. Opportunistic observations of Emys orbicularis trinacris specimens injured by fishing activities.

Locality Date Source Notes Nature Reserve “Bosco della Ficuzza, Rocca, March 2001 CRRFS Ficuzza 1 specimen with a fishhook stuck in the mouth and Busambra, Bosco del Cappelliere e Gorgo del Drago” superficial wounds. Successfully released in the wild Godrano (Tagliavia) March 2001 CRRFS Ficuzza 2 specimens entangled in fishing lines and with superficial wounds. Successfully released in the wild. Piana degli Albanesi April 2001 CRRFS Ficuzza 1 specimen entangled in fishing lines and with superficial wounds. Successfully released in the wild. Nature Reserve “Bosco della Ficuzza, Rocca, April 2002 CRRFS Ficuzza 1 specimen with a fishhook stuck in the mouth and Busambra, Bosco del Cappelliere e Gorgo del Drago” superficial wounds. Successfully released in the wild Madonie mountains March or S. D’Angelo (pers.comm.) 1 specimen with a fishhook stuck in the gastro-intestinal April 2004 tract. The hook was surgically removed by D. Freggi and A. Di Bello, and the specimen was successfully released in the wild. Nature Reserve “Monte Capodarso e Valle dell’Imera July 2013 V. Cumbo (pers.comm.) 1 heavily debilitated specimen with a fishhook in the throat. Meridionale” The specimen died during its transport to the hospital Nature Reserve “Bosco della Ficuzza, Rocca, May 2015 F. Marrone, F. Sacco and 1 dead specimen with a fishhook in the gastro-intestinal Busambra, Bosco del Cappelliere e Gorgo del Drago” R. Scardino (unpubl. data) tract.

Table 2. Synopsis of the origin, sampling sessions and number of captured Emys orbicularis trinacris specimens during the current study

Site Sampling session # of deployed traps # Turtles (tot: m + f + j) Laghetti Coda di Riccio 6 – 8 June 2016 7 17: 14+2*+1 Laghetti Coda di Riccio 20 – 22 June 2016 7 9: 8+1 Laghetti Coda di Riccio 22 – 24 June 2016 7 14: 9+5 Lago Gorgo 27 – 29 June 2016 5 54: 33+21§ Lago Gorgo 29 June – 1 July 2016 5 26: 18+7+1 * 1 female bearing 4 eggs; §: Three females bearing 4, 4, and 5 eggs, respectively.

First assessment of the impact of recreational fishing on Sicilian pond turtles 797

Figure 2. Dead Emys trinacris specimen found in May 2015 in Laghetti Coda di Riccio, with a focus on the ingested fishhook (see Table 1 for details).

University of Palermo (Italy), and X-rayed (40 kV, 150 Sicily. In order to reach these aims, in June 2016 a leaflet mA, 0.06-0.08 s) to determine the possible presence was distributed in local fishing stores, and a Facebook of hooks or Tableother 1.fishing Opportunistic gears observationsin their gastrointestinal of Emys orbicularis page trinacris (“Save specimens the injured Emys by”; fishing https://www.facebook.com/ activities. tracts. According to Gibbons and Greene (1979) and savetheemys/) was published and promoted online Locality Date Source Notes Hinton et al. (1997), the implemented radiographic (Supplementary Fig. 1A, 1B and Table S1). approach is Nature not harmfulReserve “Bosco for bothdella Ficuzza, adults Rocca, and turtle March 2001 CRRFS Ficuzza 1 specimen with a fishhook stuck in the mouth and Busambra, Bosco del Cappelliere e Gorgo del Drago” superficial wounds. Successfully released in the wild embryos. All X-ray plates are available from the authors Godrano (Tagliavia) ResultsMarch 2001 CRRFS Ficuzza 2 specimens entangled in fishing lines and with superficial on request. After radiographic analyses, all pond turtles wounds. Successfully released in the wild. Overall, 120 pond turtles were captured and sexed were releasedPiana at degli their Albanesi point of capture. Before being April 2001 CRRFS Ficuzza 1 specimen entangled in fishing lines and with superficial released into the wild, the captured individuals were (Table 2). In “Laghetti Coda di Riccio” 40wounds. specimens Successfully released in the wild. marked withNature nail polish Reserve to “Bosco exclude della them Ficuzza, from Rocca, X-raying of AprilE. trinacris 2002 were CRRFS caught, Ficuzza with a sex 1 specimen ratio strongly with a fishhook stuck in the mouth and in case theyBusambra, were recaptured Bosco del Cappelliere in subsequent e Gorgo sampling del Drago” skewed toward males (3.9 males persuperficial female). wounds. In Successfully released in the wild sessions. Madonie mountains “LaghettoMarch or Gorgo”S. D’Angelo 80 specimens (pers.comm. were) 1 caught,specimen with again a fishhook stuck in the gastro-intestinal withApril a sex2004 ratio skewed toward males (1.8tract. males The hook per was surgically removed by D. Freggi and In addition to the fieldwork, a “Citizen Science” A. Di Bello, and the specimen was successfully released programme was launched with the aim of engaging local female). Such a male-biased sex ratio is commonin the wild. in E. anglers, andNature collection Reserve of “Monte other Capodarsodata on thee Valle incidental dell’Imera trinacrisJuly 2013 (e.g. Ottonello V. Cumbo et (pers.comm al., 2017),.) and 1 heavilyit can debilitatedalso be specimen with a fishhook in the throat. catch of bothMeridionale” native and non-native freshwater turtles in likely ascribed to the fact that during theThe egg-layingspecimen died during its transport to the hospital Nature Reserve “Bosco della Ficuzza, Rocca, May 2015 F. Marrone, F. Sacco and 1 dead specimen with a fishhook in the gastro-intestinal Busambra, Bosco del Cappelliere e Gorgo del Drago” R. Scardino (unpubl. data) tract.

Table 2. Synopsis of the origin, sampling sessions and number of captured Emys trinacris specimens during the current study.�

Table 2. Synopsis of the origin, sampling sessions and number of captured Emys orbicularis trinacris specimens during the current study

798 Luca Vecchioni et al. season females are known to feed less than males, Discussion thus being less sensitive to baited traps. In addition, in It is currently widely accepted that one of the main “Laghetto Gorgo” a juvenile Trachemys scripta elegans threats faced by marine turtles is mortality due to (Wied-Neuwied, 1839) specimen was caught, but was accidental catches during fishing activities (e.g. excluded from subsequent analyses. Caracappa et al., 2018; Arizza et al., 2019, and references All 120 E. trinacris specimens were X-rayed; among therein). In the Mediterranean Sea, it has been estimated them, four females (three from “Laghetto Gorgo”, and one from “Laghetti Coda di Riccio”) were found gravid that tens of thousands individuals of the loggerhead sea (Table 2). None of the X-rayed turtles displayed any turtle Caretta caretta (Linnaeus 1758) die every year evidence of the presence of ingested fishhooks or other because of fishing-related issues. Conversely, although fishing gears (Fig. 3). it is known that recreational fishing negatively affects The attempts to actively involve citizens and anglers emydid turtles (Nemoz et al., 2014; Steen et al., 2017), through the leaflet and the Facebook page “Save the to date no data were available for Sicilian Emys trinacris Emys” did not lead to any result. To date (16 April populations, making our pilot studies necessary. 2020), not a single alert was received. Conversely, During this study, no hooks or fishing lines were found through the courtesy of the people and institutions listed in the mouth, throat, oesophagus, or gastrointestinal in the acknowledgement section, several opportunistic tract of the 120 analysed individuals, thus suggesting observations of Emys trinacris specimens injured by a limited impact of recreational fishing at the two study fishing activities could be collected (Table 1). areas, especially when compared to the high incidence of fishhooks observed in aquatic turtles in the few other available studies (Nemoz et al., 2004; Steen et

Figure 3. X-ray of two Emys trinacris specimens from Laghetti Coda di Riccio (24 June 2016). First assessment of the impact of recreational fishing on Sicilian pond turtles 799 al., 2014). However, the occasional but not negligible References findings of E. trinacris individuals injured by fishhooks Arizza, V., Sacco, F., Russo, D., Scardino, R., Arculeo, M., or entangled in fishing lines (Table 1) unequivocally Vamberger, M., Marrone, F. (2016): The good, the bad and the prove that the impact of angling on E. trinacris is ugly: Emys trinacris, Placobdella costata and Haemogregarina definitely existing, although it is possibly exerted below stepanowi in Sicily (Testudines, Annelida and Apicomplexa). the detection threshold of present work. It is also to be Folia Parasitologica 63: 2016.000. stressed that the protected status of the two investigated Arizza, V., Russo, D., Marrone, F., Sacco, F., Arculeo, M. (2014): Morphological characterization of the blood cells in sites possibly limit the angling activities, although most the endangered Sicilian endemic pond turtle, Emys trinacris of the observations of aquatic turtles injured by fishing (Testudines: Emydidae). Italian Journal of Zoology 81: 344– activities in Sicily actually occurred within protected 353. areas (Table 1). Arizza, V., Vecchioni, L., Caracappa, S., Sciurba, G., Berlinghieri, The complete failure of our “Citizen Science” F., Gentile, A. et al. (2019): New insights into the gut programme despite the guarantee of anonymity given to microbiome in loggerhead sea turtles Caretta caretta stranded on the Mediterranean coast. PLoS ONE 14: e0220329. the possible reports is a clear “alarm bell” highlighting Beregi, A., Molnár, V., Lukács, Z., Baska, F. (2003): Coelotomische the absence of environmental consciousness in a vast entfernung eines angelhakens aus einer sumpfschildkröte (Emys part of Sicilian citizenship, which needs to be sensitised orbicularis). Kleintierpraxis 48: 41–45. towards respecting local biodiversity. The realisation Caracappa, S., Persichetti, M.F., Piazza, A., Caracappa, G., Gentile, of national and local awareness campaigns aimed A., Marineo, S., et al. (2018): Incidental catch of loggerhead sea at enhancing correct behaviours among anglers and turtles (Caretta caretta) along the Sicilian coasts by longline fishery. PeerJ 6: e5392. promoting types of fishing with the lowest possible Corti, C., Capula, M., Luiselli, L., Sindaco, R., Razzetti, E. (2011): impact on non-target species is desirable. Fauna d’Italia, vol. XLV, Reptilia, Calderini. Bologna, Italy. XII In conclusion, fishhook ingestion and entangling in + 869 pp. ISBN 9788850653621 abandoned fishing lines are an actual but yet overlooked D’Angelo, S., Galia, F., Lo Valvo, M. (2008): Biometric threat to the long-term survival of freshwater turtle characterization of two Sicilian pond turtle (Emys trinacris) populations, and the monitoring of their possible impacts populations of south western Sicily. Revista Española de Herpetología 22: 15–22. should be considered in the management programmes Fritz, U., Fattizzo, T., Guicking, D., Tripepi, S., Pennisi, M.G., of the sites where pond turtles are present, with a special Lenk, P., et al. (2005): A new cryptic species of pond turtle focus on those sites where angling is practised. from southern Italy, the hottest spot in the range of the genus Emys (Reptilia, Testudines, Emydidae). Zoologica Scripta 34: Acknowledgements. The Italian “Ministero dell’Ambiente e 351–371. della Tutela del Territorio e del Mare” is gratefully acknowledged Gibbons, J.W., Greene, J.L. (1979): X ray photography: a technique for having provided the permit to allow sampling of E. trinacris to determine reproductive patterns of freshwater turtles. in Sicily (Prot. 0006880/PNM; 05/04/2016). The “Dipartimento Herpetologica 33: 86–89. Regionale dell’Acqua e dei Rifiuti, Servizio 3 – Infrastrutture per Hinton, T.G., Fledderman, P.D., Lovich, J.E., Congdon, J.D., le acque” of the “Assessorato Regionale dell’Energia e dei servizi Gibbons, W.J. (1997): Radiographic Determination of Fecundity: di pubblica utilità (Regione Sicilia)” is kindly acknowledged is the Technique Safe for Developing Turtle Embryos? Chelonian for the authorisation to conduct the sampling activities in Conservation Biology 2: 409–414. Laghetto Gorgo (prot. 26158-2016). The CRRFS (“Centro Iannella, M., Cerasoli, F., D’Alessandro, P., Console, G., Biondi, Recupero Fauna Selvatica di Ficuzza”, Italy), dr. Valentina M. (2018): Coupling GIS spatial analysis and Ensemble Niche Cumbo (Istituto Zooprofilattico Sperimentale, Palermo, Italy), Modelling to investigate climate change-related threats to the dr. Stefania D’Angelo (WWF Nature Reserve ‘Lago Preola e Sicilian pond turtle Emys trinacris, an endangered species from Gorghi Tondi’, Mazara del Vallo, Italy), dr. D. Freggi (Centro the Mediterranean. PeerJ 6: e4969. Recupero Tartarughe Marine, Lampedusa, Italy) and prof. A. Marrone, F., Naselli-Flores, L. (2015): A review on the animal Di Bello (Università di Bari, Italy) are kindly acknowledged for xenodiversity in Sicilian inland waters (Italy). Advances in the unpublished observations they provided. Dr. Pietro Valenti Oceanography and Limnology 6: 2–12. (Università di Palermo, Italy) kindly assembled the image Marrone, F., Sacco, F., Kehlmaier, C., Arizza, V., Arculeo, M. (2016): reported in Figure 2. Some like it cold: The glossiphoniid parasites of the Sicilian endemic pond turtle Emys trinacris (Testudines, Emydidae), an example of “parasite inertia”? Journal of Zoological Systematics and Evolutionary Research 54: 60–66. Naselli-Flores, L., Marrone, F. (2019): Different invasibility of permanent and temporary waterbodies in a semiarid Mediterranean Island. Inland Waters 9: 411–421. 800 Luca Vecchioni et al.

Nemoz, M., Cadi, A., Thienpont, S. (2004): Effects of recreational Scardino, R., Mazzoleni, S., Rovatsos, M., Vecchioni, L., Dumas, fishing on survival in an Emys orbicularis population. Biologia F. (2020): Molecular cytogenetics characterization of the Sicilian 14: 185–189. endemic pond turtle Emys trinacris (Testudines, Emydidae). Ottonello, D., D’Angelo, S., Oneto, F., Malavasi, S., Zuffi, M.A.L. Genes 11: 702. (2016): Feeding ecology of the Sicilian pond turtle Emys Steen, D.A., Hopkins, B.C., Van Dyke, J.U., Hopkins, W.A. (2014): trinacris (Testudines, Emydidae) influenced by seasons and Prevalence of ingested fish hooks in freshwater turtles from five invasive alien species. Ecological Research 32: 71–80. rivers in the southeastern United States. PLoS ONE 9: e91368. Ottonello, D., Oneto, F., Malavasi, S., Zuffi, M.A.L. (2017): Steen, D.A., Robinson Jr, O.J. (2017): Estimating freshwater Preliminary Data on the Population of the Sicilian Pond Turtle, turtle mortality rates and population declines following hook Emys trinacris Fritz et al. 2005 (Emydidae) Inhabiting the ingestion. Conservation Biology 31: 1333–1339. Gorgo Tondo Basso in the “Lago Preola e Gorghi Tondi” Nature Vamberger, M., Stuckas, H., Sacco, F., D’Angelo, S., Arculeo, Reserve, Sicily, Italy. Acta Zoologica Bulgarica 2017: 121–127. M., Cheylan, M., et al. (2015): Differences in gene flow in a Ream, C., Ream, R. (1966): The Influence of Sampling Methods twofold secondary contact zone of pond turtles in southern Italy on the Estimation of Population Structure in Painted Turtles. (Testudines: Emydidae: Emys orbicularis galloitalica, E. o. American Midland Naturalist 75: 325–338. hellenica, E. trinacris). Zoologica Scripta 44: 233–249. Rondinini, C., Battistoni, A., Peronace, V., Teofili, C. (2013): Lista Vecchioni, L., Marrone, F., Arculeo, M., Fritz, U., Vamberger, Rossa IUCN dei Vertebrati Italiani. Comitato Italiano IUCN e M. (2020): Stand out from the Crowd: Small-Scale Genetic Ministero dell’Ambiente e della Tutela del Territorio e del Mare, Structuring in the Endemic Sicilian Pond Turtle. Diversity Roma. 12: 343.

Table S1. List of fishingSupplementary tackle shops material involved in the Citizen Science programme (June 2016) (see text). Table S1. List of fishing tackle shops involved in the Citizen Science programme (June 2016) (see text).

Name Country Locality Address Blu Profondo Italy Palermo V.le L. da Vinci, 241 Lombardo Pesca Italy Palermo Via Orsa Maggiore, 30 L’arte della pesca Italy Palermo Via E. Giafar, 82 Tutto per la pesca Italy Palermo Via P. di Villafranca, 27 Linea Mare Italy Palermo Via Bennici Giuseppe, 53 Alta Marea Italy Palermo Via Serradifalco, 258 Alta Marea Italy Palermo Via E. Notarbartolo, 56 Filpesca Italia Italy Palermo Via G. F. la Ferla, 19 Mineo Riccardo Italy Palermo Via F. Crispi, 121 Team il Pescatore Italy Palermo Via F. Crispi, 262 Zanca Mare Italy Palermo Via Gulì Comandante Simone, 27 Consiglio Siciliano Pesca/Caccia Italy Palermo Piazza Tommaso Natale, 98 Pescamania Italy Palermo Via S. Lorenzo, 21 Olympus Italy Palermo Via Juvara Aloisi, 54/C Mare Blu Italy Palermo Via Messina Marine, 105 Di Franco Nunzio Italy Palermo Via Guadagna, 69 Blufin Pesca Sport Italy Palermo Via dei Cantieri, 35

Accepted by Wouter Beukema