Ecological and Biological Adaptations of Triturus vittatus vittatus (Urodela) to an Unstable Habitat

Introduction

The banded newt (Triturus vittatus) is one of seven newt species found in Israel. It is found at the southern border of their distribution, and is adapted to extremely unstable conditions [1, 2]. This unique species differs from the other six species in that at sexual maturity, it lives in two phases, terrestrial and aquatic [3]. The banded newt is distributed throughout Lebanon, Syria, Israel, and Iraq [4]. According to Litvinchuk et al. (2005) [4], the banded newt consists of two species, T. ophryticus and T. vittatus, based on trunk vertebra count, genome size and allozyme data. The northern taxon, T. ophryticus, is subdivided into two geographical fragments: “western group” populations from western Anatolian Turkey; and “eastern group” populations distributed in the remaining area of Turkey and Western Caucasus. The species T. vittatus is found in Israel [5]. The banded newt species or T. vittatus (the difference is not clear) is an endangered subspecies in Israel [5, 6], found at the southern limit of the species’ distribution. Adaptation of T. vittatus to the southern border of newt populations in Israel has been scarcely described [7]. On the other hand, many aspects of T. vittatus in Israel have been investigated: its life cycle [8, 9], ecological conditions during larval growth [10, 11, 12, 13, 14, 15], environmental hiding-place- seeking behavior after metamorphosis [10], and genetic differentiation of the larvae in various breeding places [16, 17, 18, 19]. The development of the newt Triturus carnifex, which is very similar to T. vittatus, has been described from egg deposition to hatch and illustrated with the use of photographs of living embryos by D’amen, et al. [20]. Embryogenesis is divided into five major phases (cleavage, gastrulation, neurulation, and organogenesis, the latter split into two phases—tail bud and ‘larva’) and into a sequence of 42 stages.

The life cycle of T. vittatus in Israel has been described in several studies [3]; in northern Israel and the Upper Galilee by Degani et al. [15] and in central Israel by Geffen et al. [8]. T. vittatus in the aquatic phase reproduces mainly in unpredictable habitats such as winter pools that generally contain water only until the beginning of the summer, although occasionally these pools contain water throughout the year.

Like other newts, T. vittatus requires a water body surrounded by an adequate terrestrial habitat to support both terrestrial and aquatic life phases. Terrestrial adult newts reach the pond area at the beginning of the rainy season, before the ponds fill up with water, and transition to the aquatic phase in the filled ponds. In the Upper Galilee, males inhabit the ponds from January to March, and leave them after mating. Females may remain in the water until May, when they deposit 18–68 eggs on plant or rock surfaces, and then transition to the terrestrial stage. The larvae hatch 19–29 days later, depending on water temperature [12]. Egg-laying by the adult newt on plants, hatching of the larvae from eggs, and larvae in their early stages of growth, have only been described in general terms in natural Israeli habitats. However, the development of embryos and of the larvae immediately after hatch has been described in other species of newts, for example, Triturus carnifex [20]. The growth and complete metamorphosis of tadpoles have been well-studied around water bodies [9, 15, 21]. The limnological conditions in the Israeli water ponds in which the tadpole newts grow and develop have been studied and described in detail [21]. Pond water temperatures range between 5 and 30ºC, pH varies from 6.5–10, and dissolved oxygen ranges between 2 and 27 mg/L, generally between 5 and 10 mg/L. Electrical conductivity varies from 150–800 μS, due to ammonia and nitrite.

The aims of this study were to expand our knowledge of the life cycle of T. vittatus, which is not described in detail in its unstable habitat at the southern border of its distribution, where the pond fills up about 1 month or more after the rains begin, and remains filled with water for only a relatively short time. Specific aims were to: (1) study the behavior of the adults when they arrive at the breeding area under unstable winter conditions, and determine their location in the pool area and the waiting time for the pool to fill with water; (2) study the period of spawning, embryo development and larval growth immediately after hatch; (3) examine the relationship between vegetative growth in the pond and egg-laying by the newts; (4) measure the time taken for the embryos to develop in this habitat, and the size of the larvae immediately after hatch in the wild. None of these variables have been described in detail in this unpredictable habitat [15].

Results

The terrestrial newts moved to the pond area in November and were found in the pond in December (Figure 1). The first rains did not fill the pond, and annual vegetation covered the pond area. The newts found hiding places in the center (deep part) of the pond. The newts were found for about 1 month (December) in the dry pond and did not transition to the aquatic phase. The transition from the terrestrial phase to the aquatic phase occurred only after the pool had been filled with water, and the newts were then found in the water (Figure 2).

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Figure 1: Number of rainy days in the area of the winter pool and the three main seasonal changes in the pool. (A) Pool during the summer before the rains. (B) Pool when the rain starts; pool is still empty and only annual vegetation covers the area. (C) Pool full of water. The terrestrial newt stage is found in the pool in December and the aquatic newt stage in January and February.

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No difference was found between body measurements for the terrestrial phase and aquatic phase (Figures 3 & 4). In contrast, there was a large difference in body color for both males and females, with the largest difference for the male. In particular, variations were found in the dorsal fin along the male’s body and the tail between aquatic and terrestrial phases.

After 2 weeks, the pool was filled with water, and a large number of common water-crowfoot (Ranunculus peltatus) began to grow (Figure 5). Newt eggs appeared on the plants 2 weeks to 1 month after the pool had filled with water. Between February 15th and March 14th, eggs and embryos were found on the common water-crowfoot. In the first 2 weeks of March, freshly hatched newt larvae also began to appear. The embryos and larvae were seen attached to the plants on around March 14th (Figure 6). On March 21st, only small tadpoles, immediately post hatch, were found.

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The larval growth until metamorphosis is presented in Figure 7. Regression conducted on data of larval size that had been recorded for the winter pond was y = 3.5853e0.0352X, R2 = 0.9748. The duration of growth in the winter pond (Nahalit) was about 2.5 months. The SD of the larvae increased as the age of the tadpoles increased. The growth rate clearly shows an exponential curve.

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Discussion

Although many aspects of T. vittatus biology, ecology, systematics and behavior on the southern border of its distribution in Israel have been investigated [2, 3] the data collected in the present study have never been described. These data provide information on the newts’ adaptations to unstable habitats. The adult newts reach the pool area when the rains start, but the pool has yet to fill with water. Once the pool is filled, it takes time for sexual behavior, egg- laying and embryo development to hatch. To adapt to this situation, adult T. vittatus in their terrestrial stage migrate to the pool about a month before it fills with water. This environmental behavior and the factors influencing it, as described here in their habitat, were previously investigated under controlled conditions in the laboratory, where their selection of hiding places was shown to be driven by soil moisture and negative phototoxicity [22]. In the laboratory, significant differences were found in the newts' choice of hiding places between those covered with black paper and those covered with papers of different colors. Moreover, the response to moisture was stronger than that to light. Juvenile T. vittatus chose moist soil in hiding places [11] covered by black or transparent paper, and the difference between these choices and other combinations of light and moisture was significant [22]. In the present study, the adult newts were found hiding under the stones in the deepest places in the pond where the rains drained before the pond was filled. This supports results from other studies about their life cycle, but adds additional aspects that show their adaptability [9, 15, 17]. During the rainy season, before the pool fills with water, the newts move into the dry pool. Since in the rainy season, it will take a month or more until the pond fills up (Figure 1), the mature male and female gonads of T. vittatus in the terrestrial phase mainly contain mature sperm and oocytes [2, 23]. This long period—1 month—during which the terrestrial newts are found in dry ponds has not been described in the natural habitats at the southern border of their distribution. The pond filled with water at the end of January and on February 15th, newt eggs were found on the plants growing in the pond. Sexual behavior is initiated a short time after the pond fills with water and is immediately followed by egg-laying, which occurs over a short time. The whole process takes about 1 or 2 weeks under these conditions [17]. Sexual behaviors of these newts have been described in detail in the laboratory but not in their habitat [24]. The common water-crowfoot takes only a few weeks to reach a size that is suitable for egg-laying, in agreement with previous studies. However, this study is the first to describe embryo development. Between February 14th and March 15th, both embryos inside the eggs and hatched tadpoles could be found. After March 21st, only tadpoles and green toads were seen [25].

The period of tadpole growth in Nihalit winter pond has been described in previous studies but, with no description of the period between the territorial adult newts’ entry into the pond, initiation of sexual behavior, egg-laying, embryo development, and tadpole hatching. All of the measurements were performed only on tadpoles. Figure 8 summarizes the reproductive stages of T. vittatus in a semiarid habitat at the southern border of its distribution.

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Figure 8: Suggested qualitative model of T. vittatus reproduction based on the results of the present study and the literature. (A) With the onset of winter rains, the adult newts move to their breeding place (Degani and Mendelssohn, 1983). (B) The newts are in the dry pool, hiding under stones while they wait for the pool to fill up. (C) The pond fills with water, the newts transition to the aquatic phase, sexual behavior is initiated and the male transfers the spermatophores to the female (D'amen et al., 2006; Degani, 2019b). (D) Laying eggs on plants, (E) embryos and tadpoles develop in a pond.