Climatic impact on reproductive success of Emys orbicularis at the northwestern border of the species range (Germany)
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1 Biologia, Bratislava, 59/Suppl. 14: , 2004 Climatic impact on reproductive success of Emys orbicularis at the northwestern border of the species range (Germany) Norbert Schneeweiss Naturschutzstation Rhinluch, Landesumweltamt Brandenburg, Nauener Str. 68, D Linum, Germany; tel.: , fax: , schneeweiss@herpetopia.de SCHNEEWEISS, N., Climatic impact on reproductive success of Emys orbicularis at the northwestern border of the species range (Germany). Biologia, Bratislava, 59/Suppl. 14: , 2004; ISSN Egg-laying dates, hatching success and survival rates of Emys orbicularis hatchlings overwintering in nests were correlated with climatic data (soil temperatures, sunshine hours) for Northeast Germany. An empirically rooted mathematical model was designed to predict the impact of temperature on embryonic development. For four different areas in Brandenburg the suitability of annual incubation conditions was assessed over 40 years, based on the correlation between soil temperature and sunshine duration. In the longterm, the more continental eastern part of Brandenburg has more favourable incubation conditions (55% of 40 years) than the more Atlantic western part (32% of 40 years). Females predominate in wild populations despite temperatures rarely exceeding 28.5 C in natural nests. This suggests a genotypic sex determination under natural incubation conditions. Key words: Emys orbicularis, reproduction, incubation, climate, Germany. Introduction The European pond turtle Emys orbicularis (L., 1758) occurs in Northeast Germany at the northwestern border of its range. This region belongs to the transition zone, the so-called Mecklenburg and Brandenburg transition climate between Atlantic and continental climates. This climate has been suggested to be suboptimal for pond turtles, contributing considerably to the regional decline of the species (BROCKMÜLLER, 1876; KURCK, 1917; KINZELBACH, 1988). However, few data are available to test this hypothesis (SCHNEEWEISS et al., 1998; SCHNEEWEISS &JABLONSKY, 2000). Therefore, the relationship between hatching success and local climate (in particular sunshine hours and soil temperatures) was investigated, resulting in a mathematical model to predict the hatching success in Northeast Germany. Material and methods The research area is located in northern Brandenburg (between and Nand13 30 and E). Egg-laying data and reproduction success were studied in four nesting sites. All hatchlings hibernate there in the nest cavities (SCHNEEWEISS, 2002). Survival rates of overwintering hatchlings and local climatic data were recorded. Hatching largely depends on sufficient soil temperatures during incubation, which are closely related to solar radiation. Thus, soil temperatures were recorded every 72 min in close proximity of clutches. Data loggers were placed in 10 cm depth, corresponding to the average depth of pond turtle nests. Sunshine hours were registered using a Campbell- 131
2 Stokes recorder. In addition, data from nearby weather stations were evaluated. Hatching success was investigated by fencing the nesting sites for capturing hatchlings in autumn or spring. In the year after oviposition, nests were opened and undeveloped or dead eggs were dissected to calculate fertilization and hatching rates. Embryos were preserved and developmental stages determined accordingtoyntema (1968). Based on this and on literature data (MAHMOUD et al., 1973; PIEAU &DORIZZI, 1981; VASSE, 1983), an empirically rooted mathematical model was developed to calculate temperature sums for predicting incubation success. Such models proved to be useful for insects (DENT, 1997). Results A certain minimum ambient temperature is the necessary prerequisite for reptile embryonic development. Thus, for estimating the impact of temperature on incubation under natural conditions, soil temperatures near the clutches have to be correlated with incubation results as mirrored by developmental stages and the hatching success. According to literature data on Emys orbicularis (PIEAU & DORIZZI, 1981; VASSE, 1983) and other emydids (MOLL & LEGLER, 1971; MAH- MOUD et al., 1973), successful embryonic development takes place between 18 and 33 C. During the late embryonic development, the influence of temperature decreases (EWERT, 1985; DEEM- ING & FERGUSON, 1991) in that the correlation between higher temperatures and quicker embryonic growth is reduced compared to earlier stages. However, embryonic growth still needs a minimum temperature of more than C then. Embryonic development does not profit or is even disturbed by temperatures exceeding 33 C(MOLL & LEGLER, 1971; VASSE, 1983), a temperature that is rarely reached in Northeast German nests. Based on these observations and unpublished personal field data, a mathematical model was designed to predict hatching success. Probability of hatching success is measured by the temperature sum which is defined as the sum of the differences between the recorded temperature (or the upper limit) and the minimum limit 18 C. Thus, the temperature sum uses all measurements of soil temperature above 18 C and below an upper limit that is set with 33 C for the incubation start. The formula acknowledges the gradually decreasing influence of temperature during embryonic development in that the values for the upper limit decrease with time. The formula is as follows: WSum n = WSum (n 1) + t n f(t n,os n,us) { OSn US T n >OS n f(t n,os n,us)= T n US US T n OS n 0 T n <US OS n =34 C e WSum (n 1) /200 WSum 0 =0 US =18 C WSum n temperature sum for n measurements during incubation period. A direct physical unit is not possible because of the non-linearity of the function. Thus, a special unit is introduced here: maturity degree (md); t n frequency of measurements (reference frequency: 20/d, 20 measurements/d = t n =1);T n n temperature measurements (in C); OS n maximum temperature limit for n measurements (in C); US minimum temperature limit (18 C) Some examples: If soil temperatures are above 25 C at the beginning of incubation (June, July), higher temperatures play a minimal role for the obtained WSum n value towards the end of the incubation period. But if incubation starts with relatively low temperatures, high temperatures are more important towards the end of the incubation period. The obtained temperature sums WSum n allow: (i) to assess the suitability of nesting sites, and (ii) to predict hatching success for individual clutches according to climatic and local nesting site conditions. The latter topic is of high conservational relevance for the endangered German pond turtle populations. The temperature sums help to decide whether a certain clutch should be better artificially incubated to avoid loss due to suboptimal environmental conditions. Moreover, as there exists a positive correlation between sunshine hours and temperature sums, it is possible to calculate the reproductive success of E. orbicularis based on sunshine hours. Using long-term data of German meteorological stations, the suitability of the climatic conditions in Brandenburg could be assessed over a 40-year period (SCHNEEWEISS, 2002). Only summer sunshine hours (1 June 31 August) have been considered here because the crucial embryonic development takes place then. Effect of sunshine hours and soil temperatures on reproduction Turtles hatched at different rates in 1994, 1995, 1997, and No hatching success was recorded in 1996 and 1998 (n = 3 and n = 5 clutches; SCHNEEWEISS, 2002) (Fig. 1). Obviously, a minimal temperature sum of approximately md is required for successful hatching (Fig. 2). If temperature sums exceed 132
3 Fig. 1. Hatching success (hatchling number/egg number) and corresponding temperature sums for 1995 to For an explanation of maturity degree (md) see text. Fig. 2. Correlation of temperature sums for individual clutches and developmental stages of the most developed embryo of each clutch (developmental stages according to YNTEMA, 1968; md = maturity degree). Fig. 3. Correlation of summer sunshine hours and temperature sums (TSUM). these values during summer, incubation success increases. On the other hand, the more the temperature sum drops below md, the lesser the incubation success will be. For making the estimation of incubation success easier, the correlation between temperature sums and sunshine hours has been divided into three classes (Fig. 3): A sum of summer sunshine hours (1 June 31 August) of more than 675 h and a temperature sum of more than 310 md corresponds to favourable conditions for embryonic development. If the sunshine hours and the accumulative temperature are below 675 h/310 md and higher than 580 h/240 md, incubation success is medium to moderate. Within this range, hatching can still be successful under suitable climatic and habitat conditions, like an extraordinarily warm and sunny September. Below 580 h/240 md, hatching success is impossible and incubation conditions are thus classified as insufficient. 133
4 Estimation of reproductive success over 40 years Hatching success depends on soil temperatures during incubation, which are positively correlated with sunshine hours (Fig. 3). Thus, hatching success could be assessed for 40 years ( ) based on data on the summer sunshine durations from four meteorological stations in Brandenburg. Observations during the 1990s served as basis for estimating the relationship between sunshine hours, soil temperatures and hatching success. In 1996 and 1998, none of the monitored clutches hatched until the end of the summer. During winter, all embryos died. In 1992, 1994, 1995, 1997, and 1999 hatching was successful at different rates. Based on this and on the correlation of sunshine hours and temperature sums, three categories were defined for incubation conditions between June and August (Fig. 3): favourable: > 675 sunshine hours moderate to medium: sunshine hours insufficient: < 580 sunshine hours In northwest and east Brandenburg, the clutches had good incubation conditions in 53% or 55% of the years between 1949 and 1999, respectively. In northwest Brandenburg, 26% of the years were insufficient for egg incubation, in eastern Brandenburg 15%. In western and northern Brandenburg with a more Atlantic climate, the sunshine hours provided poorer incubation conditions (west: favourable 32%, medium to moderate 31%, insufficient 37%; north: favourable Fig. 4. Climatic incubation conditions for pond turtle clutches in western, northwestern, northern and eastern Brandenburg, based on sunshine hours ( ). 41%, medium to moderate 28%, insufficient 31%; Fig. 4). Temperatures during the temperature-sensitive period of sex determination Based on the correlation between temperature sums and embryonic stages, the sensitive periods for temperature dependent sex determination (TSD, PIEAU & DORIZZI, 1981) were determined for 12 clutches (SCHNEEWEISS, 2002). The temperature-sensitive period occurred generally during the warm mid-summer months July and August (Figs 5 6). In seven out of the 12 studied clutches 90% and in two clutches 87% of all recorded temperature values were below 28 C (20 measurements per day). For all 12 clutches, Fig. 5. Temperature gradient during the temperature-sensitive period for sex determination at a favourable nesting site in eastern Brandenburg during the warm and sunny summer 1995 (measured in 10 cm depth). 134
5 Fig. 6. Temperature gradient during the temperature-sensitive period for sex determination at a suboptimal nesting site in northwestern Brandenburg during the warm and sunny summer 1995 (measured in 10 cm depth). the average frequency distribution of temperature measurements is as follows: < 28 C: 87.8% C: 4.0% > 29 C: 8.2% According to these results it should be expected that only males hatched since the threshold for the production of females (PIEAU &DORIZZI, 1981) is only rarely exceeded. Unfortunately, it is impossible to determine the sex of hatchlings in Brandenburg, as it would be necessary to sacrifice them for dissecting. This conflicts with nature conservation. However, the sex ratio of adult individuals in Brandenburg does not support that under natural incubation conditions only males are produced (see Discussion). Discussion Incubation success depends at the northwestern border of the range of Emys orbicularis on favourable climatic conditions, particularly on sufficient sunshine periods (SCHNEEWEISS et al., 1998; SCHNEEWEISS & JABLONSKY, 2000; SCHNEEWEISS, 2002). However, the soil temperature sums corresponding to certain developmental embryonic stages or hatching success showed some variation (Figs 1 2). This suggests that further factors are involved. PAUKSTIS et al. (1984) found in Chrysemys picta (Schneider, 1783) that an increased substrate-humidity prolongs the embryonic development. Bad, cool and moist weather episodes are also known to delay embryonic development (EWERT, 1991). The nesting sites in Brandenburg are located on well-drained sandy and south facing slopes (SCHNEEWEISS, 2002). Thus, the influence of humidity is perhaps not too important. If data are combined for the whole area of Brandenburg, 45% of 40 years had favourable, 28% had medium to moderate, and 27% had insufficient incubation conditions according to sunshine hours. The temperature sums and sunshine durations increase from west to east Brandenburg, corresponding to an increasingly continental climate (SCHNEEWEISS, 2002). Hatchlings hibernate in Brandenburg generally in the nests and survive the winter only under favourable weather conditions (SCHNEEWEISS &JABLONSKY, 2000; SCHNEEWEISS, 2002). From 1994 to 2000, three out of six winters offered appropriate conditions (SCHNEEWEISS, 2002). But only in two out of six years this matched favourable incubation conditions during summer. Only the longevity of pond turtles, the regular annual clutch production and large clutch sizes (average: 12.6 eggs per clutch; maximum 21 eggs per clutch) compensate for climatic losses (SCHNEEWEISS, 2002). However, this complicated and delicate natural history makes the European pond turtle in Brandenburg extremely vulnerable against direct and indirect human pressure, which surely caused the collapse of the pond turtle populations within the past 200 years in this region. Under laboratory conditions with constant incubation temperatures, E. orbicularis embryos 135
6 develop male characteristics at temperatures below 28 C and female characteristics above 29.5 C (PIEAU, 1974a, b, 1975; PIEAU & DORIZZI, 1981). At intermediate temperatures, both sexes are produced. PIEAU et al. (1984) proposed that soil temperatures determine under natural conditions the sex during a temperature-sensitive period. During this phase, temperatures below Cwere thought to produce exclusively males (PIEAU, 1974b, 1982). Considering the recorded low soil temperatures in Brandenburg, a strongly male-skewed sex ratio should be expected. However, the opposite is true. Females clearly predominate in the small relict populations in Brandenburg (SCHNEEWEISS, 2002, 2004). This corroborates that a genotypical sex determination mechanism overrides the temperature-dependant sex determination under natural incubation conditions, as suggested by some recent investigations (GIRONDOT et al., 1994; GIRONDOT, 1997; GIRONDOT & PIEAU, 1997). Acknowledgements I wish to thank H. BECKMANN (Linum), N. JEN- DRETZKE (Zepernick), H. LOBERENZ (Marienwerder), R. PAUL (Hamburg), M. PLETZ (Hohen Neuendorf), J. PLÖTNER (Berlin), R. SCHULZE (Zepernick), C. STEINHAUER (Görne), I. TETZLAFF (Zepernick), and M. WOLF (Linum) for their assistance during my investigations. Many thanks to the Ministry of Environment Brandenburg (Ministerium für Umweltschutz, Naturschutz und Raumordnung) and to DGHT for financial support. References BROCKMÜLLER, H Die Schildkröte in Mecklenburg. Arch. Ver. Fr. Naturgesch. Mecklenburg 30: DEEMING, D.C.&FERGUSON, M. W. J Physiological effects of incubation temperature on embryonic development in reptiles and birds, pp In: DEEMING, D.C.&FERGUSON, M.W.J. (eds) Egg incubation: Its Effects on Embryonic Developments in Birds and Reptiles, Cambridge Univ. Press, Cambridge. DENT, D. R Quantifying insect populations: estimates and parameters, pp In: DENT, D. R. & WALTON, M. P. (eds) Methods in Ecological and Agricultural Entomology, CAB International, Wallingford. EWERT, M. A Embryology of turtles, pp In: GANS, C.,BILLET, F.&MADERSON, P. F. A. (eds) Biology of the Reptilia, Vol. 14, Development A, Wiley, New York. EWERT, M. A Cold torpor, diapause, delayed hatching and aestivation in reptiles and birds. Egg incubation: its effects on embryonic developments in birds and reptiles, pp In: DEEMING,D. C. & FERGUSON, M.W.J.(eds)EggIncubation: Its Effects on Embryonic Developments in Birds and Reptiles, Cambridge Univ. Press, Cambridge. GIRONDOT, M Evolution of temperature-dependent sex determination, p. 79. In: Herpetology 97. Abstracts of the Third World Congress of Herpetology 2 10 August 1997, Praha. GIRONDOT, M.,ZABORSKY, P.,SERVAN, J.&PIEAU, C Genetic contribution to sex determination in turtles with environmental sex determination. Genet. Res. 63: GIRONDOT, M.& PIEAU, C Does Emys orbicularis have sex chromosomes? p. 79. In: Herpetology 97. Abstracts of the Third World Congress of Herpetology 2 10 August 1997, Praha. KINZELBACH, R Die Europäische Sumpfschildkröte (Emys orbicularis) im Einzugsgebiet des Rheins. Zeitschr. Angew. Zool. 75: KURCK, C Den forntida utbredningen af kärrsköldpaddan, Emys orbicularis (Lin.), i Sverige, Danmark och angränsande länder. Lunds Univ. Årsskrift, N. F., Avd. 2, 13: MAHMOUD,I.Y.,HESS,G.L.&KLICKA, J Normal embryonic stages of western painted turtles, Crysemys picta bellii. J.Morph.141: MOLL, E.O.&LEGLER, J. M The life history of a neotropical slider turtle, Pseudemys scripta (Schoepff) in Panama. Bull. Los Angeles Co. Mus. Nat. Hist. (Sci.) 11: PAUKSTIS, G.L.,GUTZKE, W.H.N.&PACKARD, G. C Effects of substrate water potential and fluctuating temperatures on sex ratios of hatchling painted turtles (Chrysemys picta). Can. J. Zool. 62: PIEAU, C. 1974a. Différentiation du sexe en fonction de la température chez les embryons d Emys orbicularis L., (Chelonien); effets des hormones sexuelles. Ann. Embryol. Morphog. 7: PIEAU, C. 1974b. Sur la différentiation sexuelle chez des embryons d Emys orbicularis L. (Chélonien) issus d œufs incubés dans le sol au cours de l été Bull. Soc. Zool. Fr. 99: PIEAU, C Temperature and sex differentiation in embryos of two chelonians, Emys orbicularis L. and Testudo graeca L, pp In: REINBOTH, R. (ed.) Intersexuality in the Animal Kingdom, Springer, Berlin, Heidelberg, and New York. PIEAU, C Modalities of the action of temperature of sexual differentiation in field-developing embryos of the European pond turtle Emys orbicularis. J. Exp. Zool. 220: PIEAU, C., RIMBLOT, F.& LESCURE, J Influence de la température d incubation des œufs sur la différentiation sexuelle des tortues. Son importance dans l élevage des tortues. Acta Zool. Pathol. Antverp. 78:
7 PIEAU, C.& DORIZZI, M Determination of temperature sensitive stages for sexual differentiation of the gonads in embryos of the turtle, Emys orbicularis. J. Morphol. 170: SCHNEEWEISS, N Demographie und ökologische Situation der Arealrand-Populationen der Europäischen Sumpfschildkröte Emys orbicularis (Linnaeus, 1758) in Brandenburg. PhD Thesis, Humboldt Universität, Berlin, 166 pp. SCHNEEWEISS, N Age structure of relict populations of the European pond turtle (Emys orbicularis) at the northwestern boundary of its range. Biologia 59, Suppl. 14: SCHNEEWEISS, N.,ANDREAS, B.&JENDRETZKE, N Reproductive ecology data of the European pond turtle (Emys o. orbicularis) in Brandenburg, Northeast Germany, pp In: FRITZ, U., JOGER, U.,PODLOUCKY, R.&SERVAN, J.(eds) Proceedings of the EMYS Symposium Dresden 96, Mertensiella 10. SCHNEEWEISS, N.&JABLONSKY, A The reproduction of Emys orbicularis in relation to climatic factors in Northeast Germany and Eastern Poland, pp In: Proceedings of the 2 nd International Symposium on Emys orbicularis, Chelonii 2. VASSE, J Transplantation of turtle embryonic thymus into quail embryo: colonization by quail cells. J. Embr. Exp. Morph. 77: YNTEMA, C. L A series of stages in the embryonic development of Chelydra serpentina. J.Morphol. 125:
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