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Local Hybridisation Between Native Triturus Cristatus and Introduced Triturus Marmoratus (Urodela: Salamandridae) in the Netherlands

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Herpetology Notes, volume 8: 549-552 (2015) (published online on 06 December 2015) Local hybridisation between native Triturus cristatus and introduced Triturus marmoratus (Urodela: Salamandridae) in the Netherlands Wouter Beukema1,*, Bobby Bok2, Laura Tiemann3 and Jeroen Speybroeck4 During recent years it has become apparent that the Peninsula (Wielstra et al., 2014a), has hitherto not been Netherlands host a considerable number of introduced listed among the introduced species in the Netherlands. populations of reptiles and amphibians (Creemers A recent record of this species from the Dutch province and van Delft, 2009). The distribution of several of Drenthe motivated the authors to survey two ponds native species has been enlarged through deliberate located in the municipality of Westerveld (Fig. 1A) on introductions outside of historical species ranges, which the 24th and 25th of May 2015. Taking into account the were often found to originate from foreign source dangers associated with ecotourism in combination with populations and represent alien subspecies. Expanding the recent rise of several invasive pathogens (Kik et al., and reproducing populations of species which form no 2011; Martel et al., 2014) we refrain from providing part of the country’s native herpetofauna are however exact locality data here, which is however available upon also present, including (but not limited to) Triturus request. The concerning area consists of mixed forest carnifex (Laurenti, 1768), Elaphe schrenckii Strauch fragments interspersed by small heathlands and several 1873, Rana dalmatina Fitzinger in Bonaparte 1838 and well-vegetated ponds, which were partially dried-out at several South-European Pelophylax taxa (Creemers and the time of the visit. Most of the surrounding land is van Delft, 2009; Felix et al., 2012; Van de Koppel et agricultural. Randomised walks along the edge of the al., 2012; van Delft et al., 2012). Hybridisation of T. ponds were performed at night, during which newts were carnifex with native Triturus cristatus (Laurenti, 1768) located using flashlights. In both of the surveyed ponds across an expanding area in the central Netherlands has we encountered newts, phenotypically attributable to led to an unfortunate case of genetic pollution, as the the following species: adult T. marmoratus (total n = 5), former successfully invades, hybridizes and eventually as well as native T. cristatus (total n = 2) and Lissotriton displaces populations of the latter (Meilink et al., vulgaris (Linnaeus 1758; total n = 7). Additionally, 2015). one pond yielded a single male Ichthyosaura alpestris Triturus marmoratus (Latreille, 1800), a salamandrid (Laurenti 1768), a species of which natural occurrence species which is native to France and the Iberian in the province of Drenthe remains disputed (Creemers and van Delft, 2009). Based on their enlarged tail fins and the presence of dorsal crests and swollen cloacae in males, all encountered newts appeared to be in breeding condition. Several larvae of T. marmoratus 1 Department of Pathology, Bacteriology and Avian Diseases, were observed which were well-recognizable by their Faculty of Veterinary Medicine, Ghent University, greenish dorsal colour and/or greenish blotches. In Salisburylaan 133, 9820 Merelbeke, Belgium. addition, one female newt (TL > 15 cm) was caught 2 St Michaël College, Leeghwaterweg 7, 1509 BS Zaandam, the which was identified as a hybrid between T. cristatus Netherlands and T. marmoratus based on the combination of 3 Department of Neurology, Technische Universität München, vague green marbling on the dorsal side and restricted Ismaninger Straße 22, 81675 Munich, Germany 4Research Institute for Nature and Forest (INBO), Kliniekstraat orange colouration interspersed by tiny white dots on 25, 1070 Brussels, Belgium. the underside (e.g. Vallée, 1959; Arntzen and Wallis, * Corresponding author; e-mail: [email protected] 1991; Fig. 1B). Based on the above, we conclude that 550 Wouter Beukema et al. Figure 1. A: Distribution of Triturus cristatus (red) and Triturus marmoratus (green) in north-western Europe. Both species occur together in the hatched area. The green dot signifies the Dutch invasive population of T. marmoratus in the municipality of Westerveld, of which the habitat is displayed on the inset (photo by Laura Tiemann). B: Ventral view of T. marmoratus (top, middle) and a hybrid T. cristatus -T. marmoratus (bottom) from the Netherlands (photos by Wouter Beukema). T. marmoratus has successfully established itself in the vulnerable on the Dutch Red List (Creemers and van Netherlands and hybridises with native T. cristatus in its Delft, 2009). It however has to be noted that only 3- presumed area of introduction. Due to the limited time 4% of the individuals in French syntopic T. cristatus spent during the survey, the presence of other ponds – T. marmoratus populations comprise F1 hybrids, nearby, and extensive aquatic vegetation which covered while introgression is basically non-existent (Arntzen most of the ponds during our visit, it is likely that only a and Wallis, 1991). Significant genetic pollution of fraction of the actual newt population was observed. the local T. cristatus gene pool by T. marmoratus can In Central France, T. cristatus and T. marmoratus therefore be considered as unlikely, which sets this case are well known to have formed a relatively broad, clearly apart from the introgression and displacement of natural contact zone in which they locally hybridise if local T. cristatus populations on the Dutch Veluwe by environmental conditions are suitable for both species invasive T. carnifex (Meilink et al., 2015). Nevertheless, (e.g. Arntzen and Wallis, 1991; Arntzen et al., 2009). future surveys should aim at discovering to what extent In the Netherlands, a similar situation might exist, introduced populations of T. marmoratus are currently concluding from the enduring presence of both parental present in the Dutch province of Drenthe and what species and at least one large-sized, adult hybrid in impact the species may have on local ecosystems. The the same water body. In contrast to the situation in development of a recent framework in which a great France, the Dutch co-occurrence is not a natural result number of markers specifically designed for the genus of limited niche overlap as evolutionarily established. Triturus can be sequenced on a large scale using next- Hybridisation between T. cristatus and invasive T. generation sequencing methods (Wielstra et al., 2014b) marmoratus in the Netherlands is undesirable, as might be a particularly helpful tool to assess the effects the former is a threatened species which is listed as of ongoing hybridisation. Local hybridisation between native Triturus cristatus and introduced T. marmoratus 551 Figure 2. Triturus marmoratus (A, B, photos by Laura Tiemann) and a hybrid between T. marmoratus and T. cristatus (C, photo by Bobby Bok) from the municipality of Westerveld, Netherlands. Acknowledgements. Ben Wielstra pre-reviewed the manuscript. Arntzen, J.W., Jehle, R., Bardakci, F., Burke, T., Wallis, G.P. We thank Reptile, Amphibian & Fish Conservation Netherlands (2009): Asymmetric viability of reciprocal-cross hybrids (RAVON) for supplying permits to handle amphibians in the between Crested and Marbled newts (Triturus cristatus and field. Triturus marmoratus). Evolution 63: 1191–1202. Creemers, R.C.M, van Delft, J.J.C.W. (2009): De amfibieën en reptielen van Nederland. Nationaal Natuurhistorisch Museum References Naturalis, Leiden, Netherlands. Van Delft, J.J.C.W, Spitzen-van der Sluijs, A.M, Goverse, E, Arntzen, J.W., Wallis, G.P. (1991): Restricted gene flow in a Struijk, R.P.J.H, Creemers, R.C.M. (2012): Risicoanalyse van moving hybrid zone of the newts Triturus cristatus and Triturus de springkikker (Rana dalmatina) in Nederland. Stichting marmoratus in western France. Evolution 45: 805–826. RAVON, Nijmegen, the Netherlands. 552 Wouter Beukema et al. Felix, R., Crombaghs, B., Geraeds, R. (2012): Exotische Mémoires de la Société zoologique de France 31: 1–95. Meerkikkers in Zuid-Limburg. Natuurhistorisch Maandblad Van de Koppel, S., van Kessel, N., Crombaghs, B.H.J.M., Getreuer, 101: 125–130. W., Lenders, H.J.R. (2012): Risk analysis of the Russian Rat Kik, M., Martel, A., Sluiijs, A.S., Pasmans, F., Wohlsein, P., Snake (Elaphe schrenckii) in the Netherlands. Natuurbalans - Grone, A., Rijks, J.M. (2011): Ranavirus-associated mass Limes Divergens BV, Nijmegen, the Netherlands. mortality in wild amphibians, the Netherlands, 2010: a first Wielstra, B., Sillero, N., Vörös, J., Arntzen, J.W. (2014a): The report. Veterinary Journal 190: 284–286. distribution of the crested and marbled newt species (Amphibia: Martel, A., Blooi, M., Adriaensen, C., Van Rooij, P., Beukema, W., Salamandridae: Triturus) – an addition to the New Atlas of Fisher, M.C., Farrer, R.A., Schmidt, B.R., Tobler, U., Goka, K., Amphibians and Reptiles of Europe. Amphibia-Reptilia 35: Lips, K.R., Muletz, C., Zamudio, K.R., Bosch, J., Lötters, S., 376–381. Wombwell, E., Garner, T.W.J., Cunningham, A.A., Spitzen-van Wielstra, B., Duijm, E., Lagler, P., Lammers, Y., Meilink, W.R.M., der Sluijs, A., Salvidio, S., Ducatelle, R., Nishikawa, K., Nguyen, Ziermann, J.M., Arntzen, J.W. (2014b): Parallel tagged amplicon T.T., Kolby, J.E., Van Bocxlaer, I., Bossuyt, F., Pasmans, F. sequencing of transcriptome-based genetic markers for Triturus (2014): Recent introduction of a chytrid fungus endangers newts with the Ion Torrent next-generation sequencing platform. Western Palearctic salamanders. Science 346: 630–631. Molecular Ecology Resources 14: 1080–1089. Meilink, W.R.M., Arntzen, J.W., van Delft, J.J.C.W., Wielstra, B. (2015): Genetic pollution of a threatened native crested newt species through hybridization with an invasive congener in the Netherlands. Biological Conservation 184: 145–153. Vallée, L. (1959): Recherches sur Triturus blasii de l’Isle, hybride naturel de Triturus cristatus Laur. x Triturus marmoratus Latr. Accepted by Iris Starnberger.
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  • Effects of Low Temperature on Testicular Cells in the Marbled Newt, Triturus Marmoratus (Caudata, Salamandridae)

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    HERPETOLOGICAL JOURNAL, Vol. 2, pp. 125- 132 ( 1992) EFFECTS OF LOW TEMPERATURE ON TESTICULAR CELLS IN THE MARBLED NEWT, TRITURUS MARMORATUS (CAUDATA, SALAMANDRIDAE) FRANCISCO EZ BENITO FRAILE, AR MIGUEL AND RICARDO PANIAGUA' J. SA , M Y PAZ DE Department of Cell Biology and Genetics, University of Alca/6 de Henares, £-28871 Alcala de Henares, Madrid, Sp ain 'Authorfo r correspondence (Accepted 17.6.91) ABSTRACT The response of the different germ cell types and glandular tissue of the testis to low temperatures (4°C) and long photoperiods ( l 6L:8D) was studied in the marbled newt (Triturus marmoratus) by histologic quantitative methods in the three periods of the annual cycle: quiescence (January-March), germ cell proliferation up to round spermatids (April-June), and spermiogenesis (July-September). Together with each group of cold-exposed newts, another group was maintained at mild temperature (20°C) over the same long photoperiod. At tbe beginning and end of each period, initial and final wild controls were collected. In the quiescent period, only spermatogonial proliferation was observed in the initial and final controls as well as in the cold-exposed newts. The newts kept at 20°C developed spermatogenesis up to the round spermatid level. At the end of the germ cell proliferation period, the final controls showed round spermatids; the newts exposed to 20°C developed complete spermatogenesis; and the newts maintained at 4°C only presented spermatogonial proliferati_on. At the end of the spermiogenesis period, the final controls and the newts kept at 20°C showed complete spermatogenesis and developed glandular tissue whereas the newts exposed to 4°C only had round spermatids and had no glandular tissue.
  • Reproductive Characteristics of Two Triturus Species (Amphibia: Caudata)

    Reproductive Characteristics of Two Triturus Species (Amphibia: Caudata)

    Arch Biol Sci. 2020;72(3):321-328 https://doi.org/10.2298/ABS200328026V Reproductive characteristics of two Triturus species (Amphibia: Caudata) Tijana Vučić1,2,*, Ana Ivanović1, Sonja Nikolić1, Jovana Jovanović1 and Milena Cvijanović2 1Institute of Zoology, Faculty of Biology, University of Belgrade, Studentski trg 16, 11000 Belgrade, Serbia 2Department of Evolutionary Biology, Institute for Biological Research “Siniša Stanković”- National Institute of the Republic of Serbia, University of Belgrade, Bulevar despota Stefana 142, 11060 Belgrade, Serbia *Corresponding author: [email protected] Received: March 28, 2020; Revised: June 10, 2020; Accepted: June 11, 2020; Published online: June 17, 2020 Abstract: During three consecutive years, we compared the reproductive characteristics and oviposition dynamics of two crested newt species, Triturus ivanbureschi and T. macedonicus. These two well-defined species are of special interest because of complex interactions at their contact zone, which include hybridization, species replacement and asymmetric mitochondrial DNA introgression. In common garden experiments, females were introduced to conspecific males, to males of other species and to hybrid males. We monitored the total number and size of the deposited eggs, as well as the dynamics and duration of oviposition during three consecutive years. The number of deposited eggs of Triturus species was much higher than previously reported. Triturus macedonicus lay more eggs that were of larger size in comparison to T. ivanbureschi. Also, the onset of T. macedonicus oviposition was considerably delayed compared to T. ivanbureschi. These are fundamental data, important for understanding complex species interactions in their contact zones. Keywords: life history traits; hybrid zone; Salamandridae; Triturus INTRODUCTION the maximum number of eggs that can be laid in a given season, but some eggs might not be deposited Triturus newts, a monophyletic group of nine species [3,14,15].