Actual and Potential Distribution of the European Pond Turtle, Emys Orbicularis (L., 1758) in Serbia, with Conservation Implications
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ACTA ZOOLOGICA BULGARICA Research Article Acta zool. bulg., Suppl. 10, 2017: 49-56 Actual and Potential Distribution of the European Pond Turtle, Emys orbicularis (L., 1758) in Serbia, with Conservation Implications Ana Golubović1, David Grabovac2 & Miloš Popović3 1University of Belgrade, Faculty of Biology, Institute of Zoology, Studentski trg 16, 11000 Belgrade, Serbia; E-mail: [email protected] 2NGO Riparia, Matije Korvina 9, 24000 Subotica, Serbia; E-mail: [email protected] 3University of Niš, Faculty of Sciences and Mathematics, Department of Biology and Ecology, Višegradska 33, 18000 Niš, Serbia; E-mail: [email protected] Abstract: Although the European Pond Turtle (Emys orbicularis) attracts considerable conservation efforts across its distribution range, in Serbia, it is understudied and assessed as Data Deficient at the national level. We surveyed approximately 10% of the territory of Serbia and noted turtles at 76 separate 10 × 10 km MGRS squares, 43 of which were noted for the first time. Turtles were usually observed in oxbows, scattered small water bodies, canals and in water-filled and vegetated, abandoned gravel pits. Models with these accurate distribution data and set of climate, topographic and land cover variables are used to explain the turtle’s ecological niche and predict where the species presence is to be expected in Serbia. In Vojvodina, turtles are limited to industrial, urban and semi-natural habitats not used for agriculture, while in the rest of Serbia it occurs in more natural habitats and small scale agriculture practice even seems to be preferred. Further studies are necessary for adequate management planning and effective protection of E. orbicu- laris in Serbia. More data on distribution need to be collected, especially in central and southern Serbia. Conservation efforts should focus to prevent illegal collection of turtles and destruction of their habitats i.e. should control illegal dumping places and overusing of agriculture machinery and chemicals. Key words: ecological niche model, species distribution model, Maxent, habitat suitability, Emydidae, Balkans Introduction The European Pond Turtle, Emys orbicularis European Wildlife and Natural Habitats (Council of (Linnaeus, 1758) (Testudines: Emydidae), is the only Europe, 1979). autochthonous species of freshwater turtle in Serbia In Serbia, E. orbicularis was protected as natu- (Krizmanić et al. 2015). Its natural distribution in- ral rarity since 1993 (Official Gazette of the Republic cludes most of Europe (except north and parts of of Serbia, No. 50/93, 93/93) and is now considered centre), western Asia and northern Africa (Arnold strictly protected (Official Gazette of the Republic & Ovenden 2002). At the international level, the of Serbia, No. 5/10). After substantial efforts to col- European Pond Turtle attracts considerable conser- lect all available literature and unpublished field data vation efforts. It was recognized as Near Threatened (Krizmanić et al. 2015), it was assigned to the Data in the IUCN Red List (Tortoise and Freshwater Deficient category at the national level (Red Book of Turtle Specialist Group 2016), listed in Annexes Fauna of Serbia II – Reptiles: Krizmanić & Džukić II and IV of the Habitats Directive (European 2015). Furthermore, the only so far realized pro- Commission, No. 92/43/EEC a, b) and Appendix ject dedicated to E. orbicularis was restricted to the II of the Bern Convention on the Conservation of Vojvodina province, north of the Danube and Sava 49 Golubović A., D. Grabovac & M. Popović rivers (Crnobrnja-Isailović & Mesaroš 2013). (Fourcade et al. 2014). Known occurrences were Consequently, this part of the Pannonian Plain rep- compared to 10000 background (pseudo-absence) resents approximately 68% of the so far known dis- points randomly sampled in 100 km buffer zone tribution range of this species in Serbia (Krizmanić surrounding the confirmed occurrences (Barbet- et al. 2015). On the other hand, the central part of the Massin et al. 2012). country was not previously studied, thus a vast area Environmental parameters were extracted of potentially suitable habitats remained unexplored. from a set of freely available GIS layers: Bioclim The high level of both international and nation- (Hijmans et al. 2005), digital elevation model (EEA al protection, along with general lack of faunistic 2013a), NDVI (LP DAAC 2000) and land cover and ecological records on E. orbicularis in Serbia, (EEA 2013b). All layers were reprojected to ETRS89 raised the urgency for gathering additional data / ETRS-LAEA coordinate reference system and resa- (Krizmanić et al. 2015). This triggered our field mpled to the highest resolution layer, digital elevation studies on the distribution of the turtle and threats model with a pixel size of 25 m2. We used bilinear to its habitats. Here we present all distribution data interpolation for layers with numerical variables and gathered to date on E. orbicularis in Serbia. Also, we near interpolation for layer with categorical predic- constructed an ecological niche model and a habitat tors (i.e. land cover). Bioclim is a set of 19 variables suitability map, to aid in future research and conser- representing biologically meaningful interpretation vation actions. of precipitation and temperature over a 30 years pe- riod. We selected only five Bioclim variables which are not autocorelated and enable simple, straightfor- Materials and Methods ward interpretation of the results. These were: annual We performed field surveys from May to September mean temperature and precipitation variables, their 2015, corresponding to the period of highest activity seasonality and isothermality. GRASS GIS v. 7.0.1 of the animals. Most of the effort was dedicated to software (Neteler et al. 2012) was used to calculate small ponds near large watercourses which were ne- slope, aspect northeness and aspect eastness from the glected in previous studies (Velika Morava, Zapadna digital elevation and also to produce average, mini- Morava, Južna Morava, Drina, Kolubara, Mlava, mal and maximal value NDVI layers out of the origi- Pek and Timok). Beside targeted surveys in 2015, nal 15-days NDVI composite acquired in 2009–2013. the data included individual observations covering NDVI (Normalized Difference Vegetation Index) or period from 2001 to 2016, and significant proportion so called “greenness index” provides remote sensed, of these observations came from numerous volun- usually satellite acquired, data about plant productiv- teers. Turtles were usually recorded during aerial or ity i.e. photosynthetic activity. We believe this index water-surface basking (including the use of binocu- could detect aquatic habitats and/or dense vegetation lars) and on few occasions they were caught in fun- surrounding ponds where the turtles naturally occur. nel traps (150 cm long and 50 cm in diameter) baited Our ecological niche model thus included variables with fish offal. The data used in this study included describing climate (Bioclim), topography (slope and only species presence, regardless of its population aspect) and species habitats (land cover and NDVI) size. (Table 1). To make an overview of known distribution After fitting the ecological niche model, we of the pond turtles in Serbia, gathered data were evaluated its performance, using the modified null- first overlapped with recently published records by model validation procedure of Raes & ter Steege Krizmanić et al. (2015) and shown as a MGRS 10 (2007). This involved sampling the same number of × 10 km map. We created an ecological niche model random points as the original number of occurrences to get insights into the ecological requirements and and fitting the null-model. To minimise the chance potential distribution of E. orbicularis (details in: of error, the procedure was repeated 100 times. At Guisan & Zimmermann 2000, Elith & Leathwick the end, we compared AUC values of species niche 2009, Sillero 2011) using Maxent v. 3.3.3k model and 100 randomly constructed null-models (Phillips & Dudík 2008). Maxent was run through using one sample t-test (one tailed test, alternative the ‘dismo’ package in R v. 3.3.1 (R Core Team hypothesis μ < μ0). After model validation, final maps 2016). Before any analysis, occurrences (observa- were shown as Maxent’s logistic output and visually tions of turtles given in Table S1.1) were subsampled arranged in QGIS v. 2.16.1 (QGIS Development by randomly selecting single occurrence within each Team 2009). 10 × 10 km MGRS square. This procedure helps to Contribution of variables was assessed using remove sampling bias and increases model accuracy Maxent’s contribution table and Jackknife analysis. 50 Actual and Potential Distribution of the European Pond Turtle, Emys orbicularis (L., 1758) in Serbia... Fig. 1. Records of European Pond Turtle in Serbia shown Fig. 2. Habitat suitability (with MGRS grid) for the Europe- on MGRS map (zone 34T). Letters represent large 100 an Pond Turtle in Serbia predicted by the Maxent ecological × 100 km MGRS squares displayed as thick lines, while niche model using a set of climatic, topographic and habitat small grid cells are given in thin lines delimiting areas of layers. The levels of gray on the map are showing Maxent’s 10 × 10 km logistic output, i.e. probability of species presence ranging between 0 and 1. Numbered Rivers: 1. Danube, 2. Sava, 3. Tisa, 4. Velika Morava, 5. Zapadna Morava, 6. Južna Mora- va, 7. Drina, 8. Kolubara, 9. Mlava, 10. Pek, 11. Timok, 12. Toplica, 13. Binačka Morava In the Jackknife procedure the model was fitted mul- ease the interpretation of the results (Supplementary tiple times and each time one of the variables was data 2). excluded from it. In addition, univariate models were fitted and the gain of all fits was visually compared. Variables that best explain the species’ ecological Results niche should have good gain when used alone and Data gathered during this study covered 100 MGRS decrease the model gain if excluded. Effects of the squares of 10 × 10 km, which is about 10% of the most important variables on the species distribution territory of Republic of Serbia.