Italian Journal of Zoology Body size, population ...

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Body size, population structure and fecundity traits of a Salamandra atra atra (Amphibia, Urodela, Salamandridae) population from the northeastern Italian Alps L. Luiselli , F. Andreone , D. Capizzi & C. Anibaldi Published online: 28 Jan 2009.

To cite this article: L. Luiselli , F. Andreone , D. Capizzi & C. Anibaldi (2001) Body size, population structure and fecundity traits of a Salamandra atra atra (Amphibia, Urodela, Salamandridae) population from the northeastern Italian Alps, Italian Journal of Zoology, 68:2, 125-130, DOI: 10.1080/11250000109356396 To link to this article: http://dx.doi.org/10.1080/11250000109356396

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126

L. LUISELLI, F. ANDREONE, D. CAPIZZI, C. ANIBALDI

dents' holes. They were located at sight and caught by hand. Each individual was subsequently sexed and snout-vent length (SVL), tail length (TaL) and total length (TL) were measured with a dial calliper to the nearest 0.1 mm. Individual marking was applied by cutting a combination of one or two toes (Twitty, 1966; Donnelly et al., 1994). Sex was determined by analysis of external secondary sexual characters (SSC): adult males have a prominent, swollen, cloaca, and are more slender than females, which (especially when pregnant) are more corpulent than males. Furthermore, 'adults' were distinguished from 'juveniles', according to Klewen (1986) and Bonato (1998, unpubl. Thesis, Padova Univ.), with the latter group including individuals without evident external SSC, and usually with a total size smaller than 90 mm.

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Fecundity and offspring parameters Apparently-non-gravid females were indicated as 'non-pregnant females', while evidently-gravid females, probably at a late stage of gestation, were named 'pregnant females'. Pregnancy was established by gentle palpation of the females' belly: the presence of intrauterine larvae at the end of their development can usually be detected with this method, which has already been applied to S. lanzai (Andreone et al, 1996, 1999a, b). To obtain data about the number of newborns per female and to test the efficacy of belly pressing, 16 females were kept in captivity; these were judged as pregnant in the field, and captured (in the period 22-29 July 1996) at a locality situated approximately 1500 m from the study site and at the same altitude. They were subsequently maintained in terraria, each one being 40 x 40 cm and housing a single female; these were stored in the garden of the private house of one of us (DC). The terraria were provided with an articulated system of refuges which gave the salamanders the possibility to hide during the cold season. The ambient temperature of the terraria fell well under 0° C during the winter, and in fact the locality used for housing them (L'Aquila, Central Italy) is covered in snow for long periods from November to March. Salamanders were measured and fed ad libitum with several preys, such as earthworms, caterpillars, slugs and larvae of different insects. Water was vaporized to guarantee the right degree of humidity. When salamanderlets were born, they were measured for TL and SVL. Post-partum females were then kept in captivity for a subsequent 15-day period to check for a possible delayed parturition, and were released later at the place of capture together with their newborns. Data analysis Data were analysed with the statistical software package STATISTICA, with alpha set at 5%, applying parametric and non-parametric tests. Two population ratios were estimated: the operational sex ratio (SR = no. of males : no. of females), and juvenile ratio (JR = no. of juveniles : no. of adults).

18 Days

19

20

21

Fig. 1 - Day-by-day secondary sex-ratio variations in the studied Salamandra a. atra population at Sella Nevea (Tarvisio, NE Italy) from the beginning until the end of the study period (14-21 July

1996).

the study, to 0.27 at the sixth day, and to a final value of 0.25. The overall adult population was constituted by 118 animals, while juveniles were 30, thus accounting for 20.3% of the number marked. Body size and sexual dimorphism Male TL ranged from 87.0 to 140.0 mm (x ± SD: 117.3 ± 13.1 mm), and female TL averaged 117.9 ± 11.8 mm (91.0-143.0 mm). Snout-vent length was 74.9 ± 7.5 mm in males and 76.0 ± 7.7 mm in females. Neither of these measurements proved to be significantly different between sexes (TL: t = -0.27, df = 127, P = 0.79; SVL: t = -0.81, df = 127, P = 0.42). As expected, tail length was positively correlated to SVL both in males (r = 0.84, r2 = 0.70, n = 61; ANOVA: F, 59 = 140.85, P < 0.001) and females (r = 0.67, r2 = 0.44, n = 57; ANOVA: F1>55 = 43.68, P < 0.001). Although TaL/SVL ratio values were not significantly different between sexes (males = 0.92 ± 0.28; females= 0.88 ± 0.33; t = 0.11 P = 0.89), at the identical body

200

-r 0.40

T

RESULTS

Population structure

In the overall study period, 148 salamanders were captured and marked. Males accounted for 51.7% of the adult population, and females for 48.3 %. Throughout the eight capture occasions the SR shifted from 0.13 of the first day (with eight females and one male) to the final 1.07 ratio, with a total of 6l males and 57 females (Fig. 1). These numbers are not different from the expected 1:1 ratio (x2 = 0.076, P > 0.05). The ratio between juveniles and adults was more regular (Fig. 2): JR passed from 0.22 at the beginning of

0 +—Hr^™r™^r^^r^"r^^r^"f^^- 0.00 16

17 18 19 20 21 Days Fig. 2 - Juvenile ratio variations in the studied Salamandra a. atra population from the beginning until the end of the study period.

POPULATION ECOLOGY OF SALAMANDRA ATRA

127

length males had TaL longer than females (single factor ANCOVA, with sex as the factor and SVL as the covariate: F2.n1 = 47 -39, P < 0.0001; see Fig. 3). Juveniles ranged in SVL from 27.8 to 56.2 mm (43.7 ± 7.92 mm) and in total length from 45.0 to 85.0 mm (67.4 ± 12.4 mm).


Pregnancy and offspring parameters Throughout the field study, a total of 57 females was collected. Of these, 31 were judged to be pregnant and 26 non-pregnant. These values are not statistically different (x 2 = 0.034, P > 0.05). However, there was a statistically significant difference between the two samples in terms of body size: pregnant females averaged 78.0 + 7.2 mm, and non-pregnant females averaged 73-9 ± 8.0 mm (t = 2.02, df = 55, P = 0.048). The 16 captive females ranged from 52.3 to 88.4 mm in SVL (72.8 ± 10.3 mm on average) (Table I). Of these, four (25% of the sample) proved to be 'non-pregnant' (i.e., not giving birth to any young). All the other females gave birth to a single young. The period from capture to date of birth ranged from 196 to 267 days (224.5 + 22.6 days) SVL of salamanderlets ranged from 25.3 to 30.9 mm (28.5 ± 1.9 mm). The twelve pregnant females averaged

E £

SVL (mm) Fig. 3 - Relationship between snout-vent length (SVL) and tail length (TaL) in adult males (filled dot, unbroken line) and females (open dots, broken line) Salamandra a. atra from the studied population.

TABLE I - Summary of the data on a selected sample (ySalamandra a. atra females (from Sella Nevea, NE Italy) taken in captivity.

Females

Pregnant

Capture date

20/07/96 22/07/96 22/07/96 23/07/96 24/07/96 24/07/96 26/07/96 26/07/96 26/07/96 27/07/96 28/07/96 29/07/96

Birth date

08/03/97 19/03/97 19/03/97 08/03/97 26/02/97 22/04/97 13/02/97 19/03/99 08/03/97 19/03/99 22/04/97 13/02/97

x ± SD Non pregnant

22/07/96 24/07/96 25/07/96 26/07/96

x ± SD t-test

t P

-

Pregnancy duration (days)

Mother SVL (mm)

Newbo.rn SVL

230 239 239 227 244 240 201 207 196 206 267 198

71.9 68.7 67.5 78.6 75.2 58.1 62.9 69.7 77.4 80.9 87.4 85.3

29.8 25.3 26.4 28.6 30.9 28.6 28.8 28.6 29.8 25.3 26.7 30.9

224.5 ± 22.6

76.6 ± 8.8

28.4 ± 1.9

-

65.5 88.4 52.3 75.3

-

-

70.3 ± 15.3

-

-

0.54 0.59

-

(mm)

Pregnant, females which gave birth to one young; Non pregnant, females which did not give birth to any young; Pregnancy duration, date of birth minus date of capture (in days).

128

L. LUISELLI, F. ANDREONE, D. CAPIZZI, C. ANIBALDI

73-6 ± 8.8 mm SVL, and the four 'non-pregnant' ones averaged 70.3 ± 15.3 mm SVL (range: 52.3-88.4 mm). The difference between these two female samples was not statistically significant (Mann-Whitney U-test = 78.58, P = 0.44). Maternal SVL and offspring SVL were not significantly correlated (Spearman's r2 = 0.043, P = 0.52; Fig. 4), which means that the hypothesis that a longer female would have given birth to a longer newborn was not confirmed. SVL-Mother


DISCUSSION

(mm)

Population structure

Fig. 4 - Relationship between maternal and newborn snout-vent length (SVL) in Salamandra a. atra from the studied population.

The analysis of the SR trend in Figure 1 shows that the two sexes were not equally active during the studied period. Until the 5 th day the females were more abundant than males, and only during the three last days were males a little more frequently encountered. At all events, the curve reached a plateau, showing therefore that the final SR was likely coincident with the population operational SR. A comparison with SR of other populations, sites and localities cannot give definitive information, since it is possible that ratios skewed from one year to another and depend on several factors, including local climatic conditions. The largest data set was provided by Klewen (1986), who reported information about the number of males and females in some populations of S. a. atra in Germany, the total number being 676 and 436 respectively (SR = 1.55). Concerning S. a. aurorae, Bonato (1998, unpubl. Thesis, Padova Univ.) reported data for two subpopula-

tions, and found a SR of 0.70 and 1.18 respectively (Table II). Sex-ratio was very variable between populations also in S. lanzai: according to Andreone et al. (1999a, b) and unpublished information for this species, values are usually close to the expected 1:1 ratio (1.45 in the Upper Germanasca Valley, Province of Turin, 1.33 in the Upper Pellice Valley, Province of Turin, and 0.76 in the Upper Po Valley, Province of Cuneo). In the studied S. atra population the juveniles accounted for 20.27%. As shown in Figure 2, JR was almost constant over all the studied period, showing that the epigean activity of juveniles is not biased as observed for the male-female ratio. In all the S. a. atra populations analysed by Klewen (1986), the mean juvenile percentage was about 12%. In two populations of S. a. prenjensis the value was 5.5%, while in S. a. auro-

TABLE II - Number of males, female, juveniles, and relative ratios in some Alpine salamander populations.

Subspecies

Locality

Salamandra a. atra

Dorfwald Schwarzenburg Scheidwald/Troli Hundshorn Burgholz Schachen Schmirntal Total Sella Nevea

Salamandra a. aurorae

st

Asiago (1 population) Asiago (2 nd population) Asiago (total)

Juv.

JR

271

36

453 33 45 293

0.13 0.38 0.18 0.07 0.09 0.06 0.20

Klewen Klewen Klewen Klewen Klewen Klewen

1112

153 6 3 26 1 225

1.07

118

30

0.25

This study

0.70 1.18 0.98

_ -

_ 49

-

Females

SR

175

96

1.82

246

207 13

1.19 1.54

676

16 97 7 436

1.81 2.02 1.43 1.55

61

57

21

30

13 42

11

Males

20

29 196 10

43

Adults

17

85

0.58

Reference

(1986) (1986) (1986) (1986) (1986) (1986)

Bonato (1998)* Bonato (1998)* Bonato (1998)

Sex-ratio (SR) was calculated dividing the number of adult males by the number of adult females, while juvenile ratio 0R) was estimated dividing the number of juveniles (individuals without evident external secondary sexual characters and with a TL usually < 90 mm) by the number of adults. , unpubl. Thesis, Padova Univ.

POPULATION ECOLOGY OF SALAMANDRA ATRA

rae, Bonato (1998, unpubl. Thesis, Padova Univ.) found a much higher juvenile value, corresponding to 36.6%. This was similar to that observed for S. lanzai in the Upper Pellice Valley, for which a percentage of 35.6% was found. It is not unlikely, in fact, that the existence of a complex system of crevices and cavities may afford better retreats for juveniles, which do not have an evident epigeous life. In places where this possibility is precluded, juveniles may be relatively more visible and mobile then at surface. In any case, it should be noted that young S. a. atra from the study area did not appear above ground earlier than June (Luiselli et al., unpubl. obs.), thus suggesting that their activity is reduced in comparison with that of the adults.

129 Data about fecundity suggest a low number of newborn per female. However, it is not clear how long the gestation period is in this population. Usually, for the Alpine salamanders it is given as 2-4 years (Wunderer, 1909, 1910; Vilter & Vilter, 1963). On average, the mean time from capture to birth of the young was about 7.5 months. Taking into account the ratio between gravid and non-gravid females, and that this time might have been considerably shorter than in nature (where temperatures are likely lower, and animals are not stressed), and that pregnant females with embryos were probably in an advanced stage, it may be hypothesized that the gestation time of the studied population should not be less than 2-3 years.


Fecundity and pregnancy duration Considering that 25% of the females thought to be pregnant in the field (and thus subsequently kept in captivity) in fact did not give birth to any young, it may be supposed that at least 8 of the 31 females captured in the field and considered pregnant were presumably non-gravid, or gravid at a preliminary stage. Based on these tentative estimates, it may be hypothesized that only about 23 of the 57 wild females were pregnant at a final stage, thus giving the ratio of one pregnant female every 2.5 females. Concerning fecundity, it should be stressed that all the pregnant females gave birth to a single salamanderlet only. Since we did not subsequently analyse (by dissection or X-ray screening) the same specimens, it cannot be totally excluded that the same females would have given birth to a second newborn after a certain delay. However, this hypothesis may be excluded, for the following reasons: (i) females were held in captivity for at least 15 days after parturition, and (ii) all the salamanders gave birth to a single salamanderlet. Thus, it appears that, at least for the S. a. atra studied at Sella Nevea, the number of newborn per female is definitely one (or rather that one is the rule for the majority of females). Thus, this seems to be a good case of invariant clutch size in a live-bearing salamander. Indeed this observation deserves attention, since until now S. atra was said to give birth normally to two young. For instance, Wunderer (1909, 1910), who analysed a large number of Alpine salamanders, in nearly all cases found two newborns. The same number was also quoted for S. a. aurorae by Franzen & Nicolai (1987). According to Guex & Greven (1994) the internal fertilized eggs are retained within the caudal portion of the oviduct ('uterus'). Fully metamorphosed juveniles are born in Mertensiella luschani, S. atra, and S. lanzai as well as in some subspecies of S. salamandra (Ozeti, 1979; Griffiths, 1996). The female S. atra ovulates over 100 eggs, 40 to 60 for each uterus (Czermak, 1843, Wunderer, 1909, 1910, Hafeli, 1971), but generally only one egg in each uterus becomes enveloped by a full set of jelly layers (named the 'embryonic egg' by Czermak, 1843) and develops into a larva.

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