Short Communication
Print
Short Communication
Turtles and ice: winter activity in non-native turtles in Romania
expand article infoOana Iftime, Alexandru Iftime§
‡ Unaffiliated, Bucharest, Romania
§ “Grigore Antipa” National Museum of Natural History, Bucharest, Romania
Open Access

Abstract

We present records of winter activity of non-native turtles, especially Trachemys scripta, the most common alien turtle in Romania. This species was observed basking in urban park lake settings in the winter months at the beginning of 2024. Trachemys scripta individuals were active during atypically warm days, but not during alternating cold spells with snowfall and ice formation; on warm days, turtles were also observed in the proximity of persisting lake ice. Other aquatic turtle species emerged from hibernation at the end of the winter, when temperatures were considerably higher, nearing 20 °C.

Key Words

alien species in Romania, Graptemys pseudogeographica, Mauremys sp., Trachemys scripta, winter activity in turtles

Numerous species of alien turtles are documented in Romania (Iftime and Iftime 2021). Of these, the most common is Trachemys scripta (Thunberg, 1792), the Pond Slider, a North American turtle that was introduced worldwide, mainly as discarded household pets (TTWG 2021; Uetz et al. 2023). In Romania, its presence in mainly urban waterbodies was widely documented (Sos 2007; Stănescu et al. 2017; Cioflec 2017–2021; Iftime and Iftime 2021), with significant morphological diversity suggesting multiple origins of introduction and intra- and interspecific hybridization (Iftime and Iftime 2022). Reproduction was documented in a few urban settings (Cioflec 2013; Matei and Tudor 2014; Iftime and Iftime 2021; Fănaru et al. 2024). Overwinter survival was considered an important limiting factor in the acclimatation of T. scripta in Europe (see discussion in Schradin 2020), though the species is naturally widespread in a temperate climate and is modelled to be able to live within vast areas of Europe, including neighbouring Bulgaria (Heidy Kikillus et al. 2010; Kornilev et al. 2020).

Here we report on the winter activity of T. scripta in lakes in two urban parks in Bucharest, Romania. The 2023–2024 winter was atypically mild, with mostly positive air temperatures and very low snowfall; however, this was interrupted by short cold spells with occasional snow showers during January 2024, negative temperatures (especially overnight), and ice formation/persistence occurring through early February.

In this context, we performed periodical visual observations of turtle activity in two parks in Bucharest—Morarilor Park (44.4398°N, 26.1705°E) and Circului/State Circus Park (44.4576°N, 26.1127°E). The former hosts a lake of ca. 8000 m2 in area, bordered by concrete embankments but enclosing some reed bed areas. The latter is a slightly smaller lake (ca. 7000 m2 in area), initially 4 m deep but by 2024 much shallower, with earth banks, reed beds, and Indian lotus vegetation. Both lakes were observed to harbour both native and alien turtle species, alongside native waterbirds and opportunistic fish species, both native and alien. We performed visual transects during selected warmer days in January and February. One day was allocated to one park/lake, as we expected activity to be concentrated during maximum insolation at mid-day. We also performed control observations on cold spell days, e.g., on the 20th of January, with snowfall and thin ice cover, when no turtle was observed. The air temperature was measured using a Dwyer WT-10 digital thermometer. The readings were also corroborated with those provided by nearby weather stations.

We observed activity and basking/swimming behaviour of T. scripta during the warmer, sunny days, occurring even between the harshest cold spells of January. In the Morarilor Park lake, T. scripta individuals (both T. s. scripta, T. s. elegans, and hybrids/intergrades thereof; see discussion in Iftime and Iftime 2022, for subspecific identification) were found active on the 5th, 19th, and 26th of January and the 3rd, 8th, and 24th of February, while in the Circului Park lake the same species was active on the 4th, 7th, and 23rd of February (Table 1). During most of these days, turtle activity (basking, swimming) took place despite the partial ice cover present (Figs 1, 2). Some turtles were active even near the ice edge (Figs 3, 4). Most individuals were quite large adults, and likely the same few (5–6) individuals were seen active through the coldest part of the winter. We noted behaviour patterns that aid in retaining heat, such as group basking, basking on wood, and heat-conserving postures (Figs 5, 6), while other basking sites were readily available (mostly at reedbed edges) and predators were absent. No other turtle species, native or alien, were observed except during the last days of February (23rd and 24th) when the weather was noticeably milder and there was no more ice.Then, we observed other species active alongside Trachemys—the native European Pond Turtle, Emys orbicularis (Linnaeus, 1758), and alien turtles: False Map Turtle Graptemys pseudogeographica (Gray, 1831) and a possible hybrid/introgressive Mauremys (sinensis (Gray, 1834) × reevesi (Gray, 1831), Chinese Striped-necked × Reeves’ Turtle, Fig. 7; see Lee et al. 2019).

Table 1.

Winter observations of turtles in two park lakes in Bucharest, Romania.

Site Date (2024) Observation hours, weather conditions Individuals observed
Lake in Morarilor Park 05.01 14.00–15.30 h, ca. 15–16 °C, weak W wind, sunny, no ice Trachemys scripta, 11 ex., basking and swimming
19.01 14.45–15.30 h, ca. 12 °C, cloudy, variable wind, ca. 60–70% of lake covered by thin ice Trachemys scripta, 4 ex., swimming
26.01 14.45–15.15 h, ca. 6–7 °C, cloudy, weak cold wind, ca. 85% of lake covered by thin ice Trachemys scripta, 3 ex., swimming
03.02 13.00–15.15 h, 8–9 °C, cold N wind, sunny, ca. 10–20% of lake covered by thin ice Trachemys scripta, 13 ex., basking and swimming
08.02 14.00–16.00 h, 17 °C, sunny, weak N wind, no ice Trachemys scripta, 30 ex., basking and swimming
24.02 13.00–15.30 h, 20 °C, mostly sunny, no ice Trachemys scripta, 52 ex., basking and swimming;
Emys orbicularis, 5 ex., basking;
Graptemys pseudogeographica, 1 ex., basking
Lake in Circului Park 04.02 13.00–15.00 h, 12 °C, cold wind, sunny, ca. 30% of lake covered by ice Trachemys scripta, 6 ex., basking and swimming
07.02 12.50–15.45 h, 15–18 °C, cold WSW wind, mostly sunny, no ice Trachemys scripta, 17 ex., basking and swimming
23.02 14.00–16.00 h, 16–18 °C, sunny, weak wind, no ice Trachemys scripta, 60–70 ex., basking and swimming;
Mauremys sinensis × reevesii, 1 ex., basking;
Graptemys pseudogeographica, 1 ex., basking
Figure 1. 

Habitat in Morarilor Park, 26.01.2024, photo O. Iftime.

Figure 2. 

Habitat in Circului Park, 04.02.2024, photo O. Iftime.

Figure 3. 

Trachemys scripta swimming at the ice edge, Morarilor Park, 26.01.2024, photo O. Iftime.

Figure 4. 

Trachemys scripta swimming near ice edge, Circului Park, 04.02.2024, photo A. Iftime.

Figure 5. 

Group basking in Trachemys scripta, Morarilor Park, 08.02.2024, photo O. Iftime.

Figure 6. 

Heat-conserving posture when basking on wood in Trachemys scripta, Morarilor Park, 08.02.2024, photo O. Iftime.

Figure 7. 

Possible introgressive Mauremys, Circului Park, 23.02.2024, photo O. Iftime.

Our observations revealed a different winter activity pattern for the observed species, with sporadic emergence between cold spells exhibited only by T. scripta, whereas the other turtle species, both native and non-native, emerged only when the weather became consistently warmer at the end of the cold season.

Trachemys scripta is capable of prolonged anoxic overwintering (ca. 45 days at 3–5 °C; Stecyk et al. 2007). However, it is sensitive to freezing temperatures (especially as nest-wintering hatchlings) (Baker et al. 2010), and deviations from optimal overwintering temperatures can have a negative impact on the health and survival of T. scripta (Máté 2015). Also, prolonged cold spells/harsher winters can induce mass mortality in T. scripta adults. Examples include cases reported by Stoyanov (2015) from Bulgaria, where the species is likewise alien. We observed a similar incident in March 2012 at the Botanical Garden of Bucharest, where at least a dozen T. scripta died due to deep and prolonged freezing of their aquatic habitat, while we recorded no dead individuals of E. orbicularis, a species also present there. As both temperature and photoperiod influence its metabolic activity (Reyes and Milsom 2010), T. scripta can emerge and be active in the winter in its native range, where activity during warmer winter days, even along or under ice, was observed (Ernst et al. 1994). Trachemys scripta was sometimes observed to reduce or completely skip hibernation in the mild climate of its non-native range in southern Spain (Pérez-Santiagosa et al. 2013). Our records establish that T. scripta is also capable of sporadic winter activity in Romania, i.e., in a non-native range and a temperate climate, when subject to unseasonably warm weather and in an urban setting. It has been postulated that such overwinter activity gives T. scripta an advantageous „early start” in an alleged competition with other (including native) turtle species for basking spots (Pérez-Santiagosa et al. 2013). However, our observations suggest otherwise, as E. orbicularis and G. pseudogeographica take advantage of the larger, pre-warmed T. scripta by climbing and basking on top of them, though alternative basking spots are quite plentiful (Figs 8, 9), adding to the observations by Kleewein (2015). Winter activity (and associated behaviour patterns) in T. scripta may rather be indicative of different ecological characteristics, which would in fact minimize interspecies competition (cf. Kleewein 2015), a hypothesis that remains to be clarified by more detailed investigation.

Figure 8. 

Emys orbicularis basking on top of group basking Trachemys scripta, Morarilor Park, 24.02.2024, photo O. Iftime.

Figure 9. 

Graptemys pseudogeographica basking on top of Trachemys scripta, Circului Park, 23.02.2024, photo O. Iftime.

Despite the unseasonably warm winter, other alien turtles and the native E. orbicularis did not start activity until the very end of the winter period (end of February), when temperatures increased and there was no ice, suggesting opportunistic winter activity is absent or much rarer in such species.

References

  • Baker PJ, Iverson JB, Lee Jr RE, Costanzo JP (2010) Winter severity and phenology of spring emergence from the nest in freshwater turtles. Naturwissenschaften 97: 607–615. https://doi.org/10.1007/s00114-010-0675-x
  • Ernst CH, Lovich JE, Barbour RW (1994) Turtles of the United States and Canada. Smithsonian Institute Press, 578 pp.
  • Fănaru G, Petrovan S, Băncilă RI, Vizireanu MG, Drăgan O, Vlad SE, Rozylowicz L, Cogălniceanu D (2024) Nesting ecology and confirmed breeding of the invasive pond slider Trachemys scripta in an urban environment, Romania. European Journal of Wildlife Research 70: 61. [art.3] https://doi.org/10.1007/s10344-024-01815-1
  • Heidy Kikillus K, Hare KM, Hartley S (2010) Minimizing false-negatives when predicting the potential distribution of an invasive species: a bioclimatic envelope for the red-eared slider at global and regional scales. Animal Conservation 13, Suppl. 1(2010): 5–15. https://doi.org/10.1111/j.1469-1795.2008.00299.x
  • Iftime A, Iftime O (2021) Alien species in Romania – fishes, amphibians, reptiles. Travaux du Museum National d’Histoire Naturelle „Grigore Antipa” 64(1): 131–186. https://doi.org/10.3897/travaux.64.e67558
  • Iftime A, Iftime O (2022) Variability and hybridization in the introduced pond slider turtle Trachemys scripta in Romania. The Herpetological Bulletin 161: 20–23. https://doi.org/10.33256/hb161.2023
  • Kleewein A (2015) Interactions between Emys orbicularis and allochthonous turtles of the family Emydidae at basking places. Hyla 2015(1): 11–17.
  • Kornilev YV, Lukanov S, Pulev A, Slavchev M, Andonov K, Vacheva E, Vergilov V, Mladenov V, Georgieva R, Popgeorgiev G (2020) The alien Pond Slider Trachemys scripta (Thunberg in Schoepff, 1792) in Bulgaria: Future prospects for an established and reproducing invasive species. Acta Zoologica Bulgarica 72(4): 571–581.
  • Lee Y, Lin J-W, Tseng S-P, Chen T-S, Lin S-M (2019) Human disturbance as a possible cause of genetic introgression from exotic into native Mauremys turtles. Animal Conservation 22(6): 556–567. https://doi.org/10.1111/acv.12494
  • Matei I, Tudor M (2014) Competition on microhabitat quality between the pond slider (Trachemys scripta) and European pond turtle (Emys orbicularis). A case study in two quasi isolated water bodies in Constanta city. p. 188. In: Popa LO, Adam C, Chișamera G, Iorgu E, Murariu D, Popa O P (Eds) International Zoological Congress of “Grigore Antipa” Museum, 19–22 November 2014, Bucharest – Romania, Book of Abstracts, 230 pp.
  • Máté P (2015) Examination of succesfull wintering of turtles. PhD dissertation thesis. Szent István University, Gödöllő, Hungary.
  • Pérez-Santigosa N, Hidalgo-Vila J, Díaz-Paniagua C (2013) Comparing activity patterns and aquatic home range areas among exotic and native turtles in southern Spain. Chelonian Conservation and Biology 12(2): 313–319. https://doi.org/10.2744/CCB-1028.1
  • Reyes C, Milsom WK (2010) Circadian and Circannual Rhythms in the Metabolism and Ventilation of Red-Eared Sliders (Trachemys scripta elegans). Physiological and Biochemical Zoology 83(2): 283–298. https://doi.org/10.1086/597518
  • Schradin C (2020) Successful reproduction of Trachemys scripta in the Altrhein of Kehl (Germany) and simultaneous increase in population estimate. The Herpetological Bulletin 154: 1–7. https://doi.org/10.33256/hb154.17
  • Sos T (2007) Emys orbicularis vs Trachemys scripta elegans. Migrans (Milvus Group) 9(1–2): 7–9.
  • Stănescu F, Sos T, Samoilă C, Cogălniceanu D (2017) Trachemys scripta in the East and South European Region. A review of the invasion extent. Poster presentation, 7th ESENIAS Workshop with Scientific Conference ’Networking and Regional Cooperation Towards Invasive Alien Species Prevention and Management in Europe’, 28–30 March 2017, IBER-BAS, ESENIAS, Sofia, Bulgaria.
  • Stecyk JAW, Paajanen V, Farrell AP, Vornanen M (2007) Effect of temperature and prolonged anoxia exposure on electrophysiological properties of the turtle (Trachemys scripta) heart. American Journal of Physiology-Regulatory, Integrative, and Comparative Physiology 293: R421–R437. https://doi.org/10.1152/ajpregu.00096.2007
  • Stoyanov A. (2015) Registered high mortality of allochthon Red-eared Sliders (Trachemys scripta elegans) in an artificial pond in Sofia, Bulgaria. Hyla 2015(1): 65–69.
  • TTWG [Turtle Taxonomy Working Group] [Rhodin AGJ, Iverson JB, Bour R, Frit, U, Georges A, Shaffer HB, van Dijk PP] (2021) Turtles of the World: annotated checklist and atlas of taxonomy, synonymy, distribution, and conservation status (9th edn.). In: Rhodin AGJ, Iverson JB, van Dijk PP, Stanford CB, Goode EV, Buhlman KA, Mittermeier RA (Eds) Conservation biology of freshwater turtles and tortoises: A compilation project of the IUCN/SSC Tortoise and Freshwater Turtle Specialist Group. Chelonian Research Monographs 8: 1–472.
login to comment