The phenology of a rare salamander (Salamandra infra- immaculata) in a population breeding under unpredictable ambient conditions: a 25 year study Michael R. Warburg Deparment of Biology, Technion-Israel Institute of Technology, Haifa 32000, Israel. E-mail: warburg@ tx.technion.ac.il Abstract. This is a long-term study (1974-1999) on the phenology of the rare, xer- ic-inhabiting salamander Salamandra infraimmaculata in a small isolated population during the breeding season near the breeding ponds on Mt. Carmel. This is a fringe area of the genus’ south-easternmost Palaearctic distribution. Salamanders were cap- tured during the 25 year long study. The first years up to the 1980s the total number of salamanders increased but during the last years there seems to have been a decline. Although this could be a phase in normal population cyclic oscillations nevertheless when compared with long-term data on a European Salamandra it does not seem so. The interpretation of the species’ status is dependent on numbers of salamanders captured as well as on the duration of the study. These subjects are reviewed and dis- cussed in this paper. Keywords. Salamandra, Amphibia, Urodela, phenology, long-term study, unpredict- able climate, population decline. INTRODUCTION The adult population of Salamandra infraimmaculata was studied at the breeding sites on Mt Carmel during 25 years 1974-1998 (except 1990). This relict population inhabits a fringe habitat on Mt Carmel at the south-eastern edge of the genus’ range. In Israel this salamander is a rare and protected species and lives in only three disjunct northern are- as of the Country. The main population is located in the mountains of the Western and Central Galilee (Degani and Warburg, 1978). In addition, two other smaller populations inhabit two disjunct areas: one about 50 km to the north-east (Degani and Mendelssohn, 1980), and the second about the same distance to the southwest, in the northern portion of Mt Carmel (Warburg, 1986a, 1986b, 1992, 1994). This last population is estimated to be much smaller than that in the Galilee mountains (Warburg, 1992, 1997). There is no Acta Herpetologica 2(2): 147-157, 2007 ISSN 1827-9643 (online) © 2007 Firenze University Press 148 M.R. Warburg apparent reason why salamanders had not extended their distribution into other moun- tain ranges in the Mediterranean region of central Israel such as Samaria and Judea: they are never found there, although Palaearctic species of animals (and plants) have succeeded in colonizing this area (Yom-Tov and Tchernov, 1988). The fact that the salamanders are not found south of Mt Carmel is of interest, and provided the main stimulus for studying this isolated population over such a long period. Since it is a fringe population inhabiting an area where conditions are suboptimal to the animals for part of the time, it exhibits special adaptations that are not found in other species in this genus (Sharon et al., 1996; Warburg, 1997). Adult S. infraimmaculata are terrestrial, and only females return to water when mature at the age of 3-4 years, and only for the time needed to lay larvae (see Warburg et al., 1978-1979). Males usually remain outside the ponds. The objectives of this study were to survey the phenology of a single salamander pop- ulation over a long period (25 years) in order to assess its status as an endangered species. Since it is extremely difficult to make a definite statement about causes that might endan- ger a species, long-term studies as this are much better qualified to make any suggestions than a 3-4 year standard length study. Among several long-term studies (43 research papers) 29 of which concerning urodele species, are listed in Appendix 1. There are several advantages in long-term studies. Firstly, an entirely different out- look emerges as the research unfolds, and secondly, changes in populations can be fol- lowed over a long period enabling a different aspect in evaluating oscillations in popula- tion cycles of a long-living urodele. MATERIALS AND METHODS The study was carried out south to Haifa, at the top of Mt Carmel located towards its western slopes, about 20 km south of the urban area. The area contains four rock-pools which are important breeding sites for the salamanders in this region. During the 25 years of the study, annual rainfall ranged between 397-1161 mm, being on average 690 mm (Table 1); 460 mm (66.6%) fell during the breeding season, in September-Janu- ary, while 230 mm during the rest of the rainy season. Rain during the remainder of winter (end of February) is not of great significance to the breeding pattern of the adults, but for the survival of the larvae, since the larvae need at least 6-8 weeks to metamorphose and they might not be able to com- plete metamorphosis once the pond water warms up (see Cohen et al., 2005, 2006). Adult salamanders were captured on stormy winter nights throughout the entire breeding season, i.e. about 10-12 weeks from mid-October to the beginning of January. They were collected, sexed by cloacal examination (Warburg et al., 1978, 1979), weighed (Mettler balance at + 0.1 g accu- racy), measured (to the nearest mm) and photographed, for individual recognition on the basis of dorsal patterns (see Warburg, 2006 for details). They were then released to their original collect- ing site either during the same or on the following night. The number of salamanders active each year during the breeding season at the study site was rather small (< 30) compared to most of other salamander species as well as to numbers of Salamandra spp in Europe (Feldmann, 1987; Klewen, 1985). In order to investigate if the numbers of salamanders varied over years or accordingly with yearly rainfall, we used t-test and regression analyses. In this last case, we performed linear, polyno- mial, and exponential models and we used that with the higher value of R2. 149The phenology of Salamandra infraimmaculata RESULTS A total of 363 different individual salamanders were hand-captured during 310 visits to the breeding ponds over a period of 25 years, when one year (1990) was not studied Table 1. Average annual rainfall and number of salamanders captured during the breeding season: Sep- tember to January. Year Rainfall (Av. Ann.) (%) Total Captured no. visits Capts/Visits 1974 586 72.5 808 10 5 2 1975 383 59.0 649 7 5 1.4 1976 550 63.1 872 3 3 1 1977 600 82.8 724 8 10 0.8 1978 398 74.2 536 7 21 0.33 1979 642 69.5 923 5 13 0.38 1980 439 70.5 623 11 6 1.83 1981 211 47.8 441 17 14 1.21 1982 600 68.8 872 21 23 0.91 1983 317 61.8 513 21 33 0.63 1984 342 56.1 609 19 17 1.12 1985 369 63.0 586 26 17 1.53 1986 622 79.4 783 29 22 1.32 1987 654 68.8 951 16 9 1.78 1988 339 71.1 477 33 13 2.54 1989 444 60.2 737 21 18 1.17 1990 216 43.6 495 (*) (*) (*) 1991 843 72.6 1161 14 9 1.56 1992 533 72.1 739 10 12 0.83 1993 310 51.5 602 10 4 2.5 1994 611 75.3 811 19 26 0.73 1995 412 66.4 620 8 6 1.33 1996 295 47.9 616 18 8 2.25 1997 477 64.0 745 17 8 2.12 1998 303 76.3 397 13 8 1.62 Av 460 66.6% 690 1.23 Total 363 (*) courtesy of the Israel Meteorological Services Beth Dagan. In bold: highest and lowest values 150 M.R. Warburg (Table 1). The average number of visits to the pond in one year (excluding 1990) is 13.4, ranging between 3 and 33 (there was no correlation between the number of visits and the number of salamanders collected: R2 = 0.34 best fit polynomial regression), and salaman- ders were captured in 160 visits (51.4 %). Altogether the mean number of salamanders captured per visit was 1.23 (Table 1). Most salamanders were captured between 1983 and 1989, and following 1989 there has been a gradual decline (though non significant R2 = 0.34) in the numbers of salamanders captured (Table 1). The highest number of salaman- ders captured in one visit was 32 specimens in 1988. The captures of salamanders were then calculated for 4-year periods (Table 2). The rea- son for this was in order to compare with the extent of the usual research projects which last up to four years (Alford and Richards, 1999) although some lasted longer. Six such periods fit into the 24 years studied (Fig. 1a), most of them differing significantly from each other (Table 2). During the first four years (1974-1977), 29 salamanders were captured, while the next four years (1978-1981) 58 salamanders followed by 147 salamanders in the next four years (1982-1985). The last four years of study (1994-1998) 95 salamanders were captured (Fig. 1a). After grouping, there appears to be a definite and statistically significant (R2 = 0.85 best fit polynomial regression) decline in numbers of salamanders frequenting this breeding site on Mt Carmel (Fig. 1a). No such difference could be seen in the rainfall pattern when this was arranged for 4-year periods (R2 = 0.04 best fit power regression). If the study would have lasted four years (which is longer than a 3-year average fund- ed research project) e.g. from 1974 to 1976 it could be concluded that the population of adult salamanders is small and declining (Table 1). A fourth year did show an increase but the population size never reached its 1974 peak until six years later (1980). From that year onwards the population size increased, reaching a maximum of 32 in 1988 (Table 1). In the next 4-year period (1978-1981) the population reached a plateau thereafter start- ing to increase almost continuously till 1986 when it peaked. If we would have studied this population for a period of three years between 1980-1986 we would conclude that the population is increasing. Nevertheless, there does not seem to be a statistically significant relationship between the duration of study and the number of salamanders captured (R2 = 0.34) nor in the rainfall pattern over the study period (R2 = 0.04 best fit power regression). There is no indication that there was indeed any change in the rainfall pattern (Table 1), in the hydro period of the ponds, the quality of air, water or soil. Moreover, there was no significant relationship between rain and the number of salamanders captured (R2 = 0.0038 best fit power regression). Table 2. Differences between 4-year periods (t-tests with 6 df ) in captures. 1974-77 1978-81 1982-85 1986-89 1991-94 1978-81 0.329 1982-85 0.001 0.011 1986-89 0.003 0.014 0.531 1991-94 0.014 0.014 0.091 0.072 1995-99 0.041 0.328 0.003 0.036 0.512 151The phenology of Salamandra infraimmaculata It would not have been possible to reach the conclusion that there are natural popula- tion oscillations unrelated to the amount of annual rainfall unless these long-term obser- vations became available in spite of the fact that no statistically significant relationship could be demonstrated between the duration of the research and the number of salaman- ders captured. DISCUSSION The chances of capturing salamanders increase greatly with the duration of the study period since salamanders are known to return to the breeding sites even after long inter- vals (Warburg, 2006). The reasons why both capture and duration are important for such study are: (i) a specimen may be missed by a few minutes consequently it is not certain Fig. 1. Phenology of (a) S. infraimmaculata arranged in 4-year periods, and (b) S. terrestris over 21 years study and arranged in 4-year periods; data from Feldmann (1987) by permission. 152 M.R. Warburg that the salamander did not visit; (ii) if the study would have been shorter, there was the risk to miss salamanders that do not visit the pond every year. S. salamandra in particu- lar seems to be a favorite object for these studies (14 studies see Appendix 1). Perhaps because they are remarkable in their site fidelity both to the breeding ponds as well as to their winter or summer refuges (Feldmann, 1987; Warburg, 1996, 2006) and because they are such long-lived animals (see Warburg, 2007). Thus, many salamanders (50% Feld- mann, 1971, 63.1% in Feldmann, 1978, 70% in the present study and 84% in Feldmann and Klewen, 1981) returned to their winter refuges for at least six years. The most important point in this study is how to interpret the apparent decline in number of salamanders visiting the ponds on Mt Carmel. Although of statistical signifi- cance when analyzed for 4-year periods, this decline could also indicate a low point in long-term population oscillation. Similar long-term phenological studies on other urode- les show a variety of patterns: Thus, a 6-year study on Notophthalmus perstriatus (Dodd, 1993), a 7-year study on Triturus cristatus (Kupfer and Kneitz, 2000), and a 16-year study on Ambystoma tigrinum, all show a decline in numbers. Nevertheless, all these studies may have in fact described a phase in normal population oscillations taking place in urodeles. However, long-term data (21 years) on a S. terrestris population in Central Europe did not reveal a significant change over the years (Feldmann’s data, see Fig. 1b). So, we are left with one possibility: a definite decline in numbers of S. infraimmaculata. Could such a decline endanger S. infraimmaculata population on Mt Carmel and cause its extinction? In my opinion it is unlikely since this single population studied here is only one of Mt Carmel’s salamanders metapopulation which consists of a few, isolat- ed, patch-like populations. 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Long-term studies on some urodeles (> 5 Yrs) Species Years Source Cryptobranchus alleganiensis 20 Wheeler et al. (2003) Ambystoma talpoideum 6 Semlitsch (1987) A. talpoiderum 8 Semlitsch et al. (1988) A. talpoideum 9 Pechmann et al. (2001) A. talpoiderum 12 Semlitsch et al. (1993) A. talpoideum 16 Semlitsch et al. (1996) A. opacum 16 Semlitsch et al. (1996) A. opacum 12 Pechmann et al. (1991) A. tigrinum 9 Pechmann et al. (2001) A. tigrinum 16 Semlitsch et al. (1996) A. maculatum 5 Husting (1965) A. maculatum 6 Blackwell et al. (2004) A. maculatum 12 Brodman (2002) A. jeffersonianum 12 Brodman (2002) A. californiense 7 Trenham et al. (2000) Hynobius nebulosus tokyoensis 7 Kusano (1982) Desmognathus ochrophaeus 7 Tilley (1980) D. quadramaculatus 6 Dodd and Dorazio (2004) Plethodon kentucki 7 Marvin (2001) P. jordani 6 Dodd and Dorazio (2004) P. jordani 7 Hairston (1983) P. glutinosus 5 Hairston (1983) P. ornata 12 Pechmann et al. (1991) P. cinereus 14 Jaeger (1980) P. shenandoah 14 Jaeger (1980) Eurycea quadridigitata 16 Semlitsch et al. (1996) E. quadridigittata 6 Dodd (1992) E. quadridigittata 9 Pechmann et al. (2001) Triturus marmoratus 6 Diaz-Paniagua et al. (1996) T. marmoratus 5 Martinez-Solano et al. (2003) T. cristatus 6 Arntzen and Teunis (1993) T. cristatus 6 Arntzen (2000) T. cristatus 7 Kupfer and Kneitz (2000) T. cristatus 20 Beebee (1997) T. vulgaris 20 Beebee (1997) 157The phenology of Salamandra infraimmaculata Species Years Source T. vulgaris 11 Gressler et al. (1997) T. helveticus 20 Beebee (1997) T. alpestris 5 Martinez-Solano et al. (2003) T. dobrogicus 11 Gressler et al. (1997) T. dobrogicus 5 Jehle and Hödl (1998) Salamandra salamandra 5 Martinez-Solano et al. (2003) S. salamandra 6 Rebelo and Leclair (2003) S. salamandra 10 Kästle (1986) S. salamandra 20 Schmidt et al. (2005) S. terrestris 7 Feldmann (1971) S. terrestris 13 Feldmann (1978) S. terrestris 21 Feldmann (1987) S. terrestris 17 Feldmann and Klewen (1981) S. terrestris 5 Klewen (1985) S. terrestris 6 Klewen (1986) S. infraimmaculata 10 Warburg (1986a) S. infraimmaculata 11 Warburg (1986b) S. infraimmaculata 18 Warburg (1994) S. infraimmaculata 25 Warburg (present study) Notophthalmus viridescens 16 Semlitsch et al. (1996) N. viridescens 9 Pechmann et al. (2001) N. perstriatus 6 Dodd (1992, 1993); Dodd and Cade (1998) Taricha rivularis 7 Twitty et al. (1967) Appendix 1. continued