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Neurergus kaiseri.

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Amphibian & Reptile Conservation 6(4): 1-8.

Sexual size dimorphism in Neurergus kaiseri (Caudata:

Salamandridae) in south-western Zagros Mountains, Iran

^ozafar Sharifi, Hossein Farasat, and Somaye Vaissi

Rctzi University Center for Environmental Studies , Department of Biolog}’, Faculty of Science, Baghabrisham 67149, Kermanshah, IRAN

Abstract . — Using bivariate and multivariate techniques we evaluated sexual size dimorphism in 13

body-related and six head-related metrics from 99 live specimens of the Lorestan newt, Neurergus

kaiseri. Analyses of variance of 12 metrics showed that average sizes for all these characters in fe-

males are significantly (P< 0.05) greater than in males. However, one character (vent length) is larger

in males than females (P<0.001). Evaluation of 13 metrics showed that average size dimorphism is

apparent in 10 characters with nine characters showing these differences at P<0.01 and one char-

acter at P<0.05 confidence levels. Principal Components Analysis of external characters provided a

good separation of males and females. Although body measurements gave a clear pattern of differ-

ences between the sexes in N. kaiseri, head measurements showed no such distinctions.

Key words. Neurergus kaiseri , Principal Component Analysis (PC A), sexual size dimorphism, southwestern Iran,

cloaca

Citation: Sharifi M, Farasat H, Vaissi S. 2012. Sexual size dimorphism in Neurergus kaiseri (Caudata: Salamandridae) in south-western Zagros Moun-

tains, Iran. Amphibian & Reptile Conservation 6(4):1-8(e48).

Introduction

Sexual dimorphism shows widespread and recogniz-

able patterns in many species and has been studied for

more than a century (reviewed in Fairbairn et al. 2007).

Sexual size dimorphism is common in animal taxa, but

is highly variable in magnitude and direction (Anders-

son 1994; Fairbairn 1997; Brandt and Andrade 2007).

Sexually dimorphic traits have been surveyed in differ-

ent classes of vertebrates, including birds (Temeles 1985;

Temeles et al. 2000), primates (Crook 1972), amphibians

(Schauble 2004; Vargas-Salinas 2006; McGarrity and

Johnson 2008; Malmgren and Thollesson 1999; Kalezic

et al. 1992), lizards (Bruner et al. 2005; Kaliontzopou-

lou et al. 2007), and snakes (Feriche et al. 1993; Shine

et al. 1999). Amphibian females generally grow larger

than males and female body size is often correlated to

clutch size (Duellman and Trueb 1986; Rafinski and

Pecio 1989; Kalezic et al. 1992). In amphibians, the most

strikingly dimorphic sexual characteristics are seasonal;

however, most species also show permanent sexual dif-

ferences in morphometries and morphology (Malacarne

and Cortassa 1983).

Although mature female amphibians are generally

larger than males, and female body size is often corre-

lated to clutch size, there are examples where males are

the larger. This can be attributed to high degrees of ago-

nistic male behavior such as combat during the reproduc-

Correspondence. Email: 1 sharifimozafar2012@gmail.com

tive season. Several theories have been developed to ex-

plain ecological and evolutionary significance for sexual

size dimorphism (e.g., Slatkin 1984; Andersson 1994).

As stated by Daiwin (1871) sexual selection is likely the

most important single cause that generates dimorphism,

but other factors such as female reproductive strategy

and competition for food resources have been considered

to be significant (Duellman and Trueb 1986).

In the present paper, we explore and discuss sexual

size dimorphism in the Lorestan newt Neurergus kai-

seri in the southwestern mountains of Iran. The aim is

to describe the expression of intersexual differences in

this species to reveal sexually dimorphic traits that can be

important in systematic and evolutionary research.

Material and methods

We measured 99 live specimens of Neurergus kaiseri

found in the southern Zagros ranges. The average annual

precipitation in the southern Zagros ranges from 400 to

800 mm per year. The dominant vegetation cover around

streams is oak tree ( Quercus brantii ) open woodlands.

The active period of N. kaiseri in its aquatic environment

starts in March and ends in July, a period when tempera-

ture enables breeding and feeding. The N. kaiseri used in

the present study (58 males, 41 females) were all caught

in the daytime between the 7 th and 13 th April 2012. The

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Sharifi et al.

Figure 1 . Male Neurergus kaiseri have a fleshy protuberance at the base of the tail (A), whereas female has a prominent cloaca but

without the protuberance (B). Photos by Mozafar Sharifi.

method of capture was by hand, with individuals taken

from among or under stones in the shallow water at the

side of the stream. After measuring, the N. kaiseri were

released unhanned at the location of their capture. The

sex of each individual was assessed according to external

secondary sexual characters: males have a fleshy protu-

berance at the base of the tail, whereas females have a

prominent cloaca, but without the protuberance (Fig 1).

Juveniles are differentiated from mature adults in having

a smaller body length and lacking both the protuberance

and the prominent cloaca (Baran and Atatiir 1998).

Thirteen variables (Table 1) for all specimens were

measured with calipers to the nearest 0.1 mm. To test

significant differences of sexually dimorphic metrics,

Independent Sample /-test (2 -tailed) as well as Principal

Component Analysis (PCA: correlation matrix) at the

significance level of 0.01 were used. In multivariate anal-

yses the variables were carried out into two sets (body-

and head-related measurements) and were analyzed

separately using PCA based on Pearson’s correlation

coefficients. SPSS software version 16, Excel, and Past

software were used for running the statistical analyses.

Table 1 . Definitions of the morphometric character set and abbreviations used for body- and head-related metrics.

Abbreviations

Body measurements

SVL

LFL

LHL

FHL

TLL

Head measurements

IOD

Variable definition

Weight

Snout to vent length, tip of snout to anterior margin of cloacal lips

Tail length, posterior margin of cloacal lips to tip of tail

Length of fore limb, anterior margin of front leg to tip of the longest finger

Length of hind limb, anterior margin of hind leg to tip of the longest toe

Forelimb to hindlimb length, posterior margin of front leg (axilla) to anterior margin of hind leg (groin)

Vent length, anterior margin of cloacal lips to posterior margin of cloacal lips

Total length, tip of snout to tip of tail (SVL + VL + TL)

Head length, tip of snout to posterior region of neck

Head width, largest width of head, in line with the comer of the mouth

Height of head, margin of lower jaw to upper of eye, in line with the eyes

Interorbital distance, shortest distance between eyes

Distance of nostrils, from one nostril to the other

Length of wrinkles under throat, tip of snout to posterior margin of wrinkles under throat

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Sexual size dimorphism in Neurergus kaiseri

Results

The results of the Independent Sample t-test (2 -tailed)

show that in N. kaiseri most characters differed signifi-

cantly between sexes (P<0.01), so that in each variable

females are larger than males, excluding vent length (Ta-

ble 2). In N. kaiseri, 89% of body related metrics were

significantly sexually dimorphic (Table 2). In contrast,

there were fewer such sex related differences (50%) in

measurements related to head morphology. The mean

male to female Snout to Vent Length (SVL) ratio was

0.86 for N. kaiseri (Table 2). In Bivariate Analyses,

SVL in relation to the Total Length (TL; measured from

tip-of-snout to tip-of-tail), was dimorphic in N. kaiseri

(males 46.59% ± 0.004 SE, females 49.36% ± 0.004 SE;

P <0.001). The relation between Tail Length (TL) to the

Total Length and Lorelimb to Hindlimb Length (LHL) to

SVL were not significantly sexually dimorphic in N. kai-

seri. Males of N. kaiseri had the shorter tail (males 56.76

± 0.93 SE, females 63.20 ± 0.92; P <0.001).

Analysis of metrics indicated general trends in varia-

tion. Loadings for the first two components are given in

Table 2, and the individual specimens are projected onto

these components in Ligure 3. In each PC A there were

high positive loadings for all characters on PCI. This

axis is therefore interpreted as a general size measure.

Contrasting positive and negative loadings were found

on PC2, indicating general shape measures as important

for this separation.

Body variables gave a clear pattern of differences be-

tween the sexes in N. kaiseri, while head measurements

showed no such distinctions (Pigs. 1 and 2). Lactor load-

ings for principal components (Table 3) revealed that a

total of 75.9% and 58.3% of the variability for N. kaiseri

could be explained by the first two components (PCI and

PC2) for body- and head-related traits, respectively. The

first component, which explained 62.1% and the second

component, which explained 13.7% of the total character

variation for body characters, provided complete separa-

tion between males and females (Pigs. 3, 4, and 5). The

first component, which explained 39% and the second

component, which explained 19.3% of the total character

variation for head measurements, do not prove complete

separation between males and females (Pigs. 3, 4, and

5). The remaining components (PC3 ± PC9) individually

explained < 12% of the total variation for this species on

body related traits, and did not reveal any readily inter-

pretable patterns. Lactor loadings for discriminant Hot-

teling’s T 2 revealed that with using body measurements,

males and females were well separated (Hotteling’s

T 2 : 1307.9, P: 175.28, PO.OOl), but with using head

variables the sexes were not separated (Hotteling’s T 2 :

29.351, P: 5.63, P0.001), and revealed these measure-

ments unsuitable for determination of sexual dimorphism

in N. kaiseri ( Pig. 2).

Table 2. Descriptive statistics (mean, standard error of mean, and range) of 13 external characteristics (mm) in males and females of

Neurergus kaiseri ; n: number; SE: standard error of mean. Morphometric Abbreviations: W (Weight), SVL (Snout- Vent Length), TL

(Tail Length), HH (Height of Head), LFL (Length of Forelimb), LHL (Length of Hindlimb), FHL (Forelimb to Hindlimb Length),

VL (Cloacal Length), IOD (Interorbital Distance), DN (Distance of Nostrils).

Variable

Males (n =

Mean ± SE

58)

Range

Females ( n

Mean ± SE

= 41)

Range

Body measurements

6.2 ± 0.2

3 . 2 - 9 . 8

7.2 ± 0.3

3 . 8 - 11.4

0.0

SVL

54.8 ± 0.5

47 . 9 - 61.8

63.6 ± 0.8

54.1 - 78.9

0.0

56.8 ± 0.9

33 . 5 - 72.8

63.3 ± 0.9

52 . 6 - 75.9

0.0

LFL

20.1 ± 0.2

16 . 3 - 22.3

20.5 ± 0.2

16 . 9 - 23.1

0.05

LHL

21.6 ± 0.2

17 . 2 - 24.6

22.4 ± 0.3

19 . 2 - 26.0

0.0

FHL

29.4 ± 0.4

18 . 0 - 35.8

35.0 ± 0.6

26 . 9 - 41.6

0.0

13.8 ± 0.2

11.1 - 16.7

14.4 ± 0.4

6 . 2 - 18.9

0.1

6.2 ± 0.2

4 . 5 - 7.9

2.1 ± 0.4

1 . 4 - 2.5

0.0

TLL

117.8 ± 1.4

100.1 - 137.3

128.9 ± 1.4

111 . 8 - 146.5

0.0

Head measurements

13.5 ± 0.1

10 . 7 - 16.0

13.6 ± 0.1

12.1 - 15.0

0.2

U . 0 ± 0.1

9 . 5 - 13.4

11.1 ± 0.2

5 . 7 - 12.5

0.7

5.6 ± 0.1

4 . 9 - 7.4

6.0 ± 0.1

5 . 3 - 7.2

0.0

IOD

7.1 ± 0.1

L/<

7.4 ± 0.1

6 . 2 - 8.8

0.0

3.8 ± 0.1

1 . 2 - 4.6

4.0 ± 0.0

3 . 5 - 4.7

0.01

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Sharifi et al.

Figure 2. Discriminant Hotelling’s T 2 for separation of male and female Neurergus kaiseri. (A) Body-related characters; (B) Head-

related variables. Note that on base head-related variables male and female aren’t well separated.

Figure 3. Principal Component Analysis (PCA) on sexual dimorphism in Neurergus kaiseri. Scatter plots of principal component

scores for the first two principal axes, with convex polygons for males and females. Loadings are shown in Table 3. (A) Body-

related characters; (B) Head-related variables, significant sex differences are noted on neither PCI, nor PC2.

PCI ( 55.82 %)

Figure 4. Principal Component Analysis (PCA) on seasonal

sexual dimorphism in Neurergus kaiseri. Scatter plots of prin-

cipal component scores for the first two principal axes, with

convex polygons for males and females. Loadings are shown

in Table 3.

Discussion

The Lorestan newt Neurergus kaiseri was shown not

to exhibit sexually dimorphism in head-related metrics.

This is in agreement with other studies on head morphol-

ogy in newts (Malmgren and Thollesson 1999; Rafinski

and Pecio 1989; Kalezic et al. 1992). These results do

not support the ecological model that N. kaiseri has de-

veloped intersexual differences in feeding strategies

along a niche divergence process (Slatkin 1984; Ander-

sson 1994) driven by the two factors, the rate of feed-

ing and type of food consumed (Shine 1989). The first

factor considers that substantial intersexual difference

in body size lead to differences in feeding rates between

the sexes. The second factor comprises species where the

sexes diverge in trophic morphology as a result of inter-

sexual differences in dietary preferences. Both male and

female newts experience high energetic costs during the

reproductive season (Halliday and Arano 1991; Griffiths

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Sexual size dimorphism in Neurergus kaiseri

SVL

7.50

7.00

6.50

^ 6.00

5.50

5.00

4.50

Figure 5. Bivariate scatterplots of variables on sexual dimorphism with convex polygons for males and females in Neurergus kai-

seri. (A and B) Body-related characters (C and D) Head-related variables. Body measurements gave a clear pattern of differences

between the sexes in N. kaiseri , while head measurements showed no such distinctions. All values in mm.

1996) and both spend considerable time feeding when

not involved in courtship. This indicates that feeding

rates between males and females might be similar within

species, even during the breeding period, suggesting that

sexual dimorphism resulting from feeding rates and diet

may be negligible.

The separation of sexes in statistical analyses was

high in N. kaiseri. Sexual dimorphism was attributed to

females showing large values for dimensions related to

fecundity, such as SVL and distance of FHL, contrasted

with large values for cloaca in males. In all analyses the

female SVL and FHL metrics were highly significant in

the observed patterns, contrasting against the male CL.

These results can be interpreted as primarily concordant

with the fecundity model. Previous studies on amphib-

ians have shown that females are generally larger than

males in body size (Duellman and Trueb 1986), possibly

because fecundity increases with increasing female body

size. Males, however, can often increase their lifetime re-

productive success through other life history traits in spe-

cies with little or no agonistic behavior; for example by

maturing at an early age. Moreover, Kalezic et al. (1992),

showed that the trunk length (corresponding to FHL) is

directly correlated to the length of the pleuroperitoneal

cavity in Triturus newts to which Neurergus is a closely

related.

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Sharifi et al.

Table 3. Factor loadings for the first two principal components (eigenvectors) for Neurergus kaiseri from multivariate

analyses (Principal Components Analysis, PC A) on body- and head-related variables.

Neurergus kaiseri

Variable

PCI

PC2

PC3

Body measurements

SVL

0.848

0.124

- 0.304

0.755

- 0.570

0.293

LFL

0.668

0.470

0.447

LHL

0.734

0.420

0.041

FHL

0.762

- 0.025

- 0.534

TLL

0.934

- 0.298

0.123

Eigenvalue

3.726

0.827

0.680

% of variability

62.099

13.776

11.328

Cumulated %

62.099

75.874

87.202

Head measurements

0.484

0.794

0.049

0.631

- 0.540

- 0.003

IOD

0.654

0.140

- 0.482

Eigenvalue

1.699

0.985

0.887

% of variability

39.011

19.328

17.216

Cumulated %

39.011

58.339

75.555

Male N. kaiseri could be distinguished from females

in having a larger cloaca (Fig. 1). The cloacal swelling in

male newts is most notable laterally and ventrally com-

pared to females, and may be an important factor in male

mating success. Most of the cloacal volume is occupied

by glands secreting substances fonning the spermato-

phore, although tubules emanating from the pheromone-

producing dorsal gland are present — especially in the

caudal region of the cloaca (Sever et al. 1990). The dor-

sal gland itself, which is known to be greatly enlarged

during the breeding season in some newts, lies anterior

to the pelvic girdle. As proposed by Sever et al. (1990),

it is quite likely that both the rate of spennatophore pro-

duction and the synthesis of courtship pheromones — fac-

tors contributing to male mating success — are under the

influence of sexual selection, thus increasing the size and

volume of structures in the cloacal region.

Acknowledgments. — We thank Nate Nelson for pro-

viding funding for this project through the conservation

breeding program for N. kaiseri at Sedgewick County

Zoo, Wichita, Kansas, USA. We are also grateful to Razi

University which provides funding to the postgraduate

students involved in present study.

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a general size measure. On PC2 positive loadings (characters

above the abscissa) are contrasted with negative loadings (be-

low), and the component is interpreted as a measure of shape

that discriminates between males and females (Figs. 4 and 5).

Abbreviations as in Table 1 .

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Received: 11 May 2012

Accepted: 07 June 2012

Published: 12 July 2012

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Mozafar Sharifi is a senior lecturer in ecology at Department of Biology, Razi University, Kerman-

shah, Iran. He is also director of Razi University Center for Environmental Studies. In recent years his

main research interest focuses on conservation biology of chiroptera and amphibians. He has contribu-

tion to the processes involving conservation assessment of chiroptera and two species the genus Neu-

rergus in collaboration with the IUCN.

Hossain Farasat is currently a Ph.D. candidate at Department of Biology, Razi University, Kerman-

shah, Iran. He earned his M.Sc. from Razi University. His present research focuses on the ecology

and genetic diversity of fragmented populations of Neurergus kaiseri. His main interest is to examine

whether these fragmented populations are structured by a metapopulation. He is also keen to apply his

finding in conservation of this critically endangered and endemic species of Iran.

Somaye Vaissi is a M.Sc. student in systematic zoology at Department of Biology, Razi University,

Iran. She has earned her B.Sc. in animal biology from the same department. She is currently the curator

of a Captive Breeding Facility for Neurergus microspilotus at Razi University funded by the Mohamed

bin Zayed Species Conservation Fund. Her current research activities with two species of Neurergus

involve several topics associated with husbandry and health of the newts in captivity. These include

nutrition, growth, development and their health. She has contribution in detecting chytrid fimgus and

other diseases such as red-leg syndrome and rickettsial inclusions in the newts.

amphibian-reptile-conservation.org

008

July 2012 | Volume 6 | Number 4 | e48

mons Attribution-NonCommercial-NoDerivs 3.0 Unported License, which permits unrestricted use for non-com-

mercial and education purposes only provided the original author and source are credited.

Amphibian & Reptile Conservation 6(4):9-29.

Conservation biology, husbandry, and captive breeding of

the endemic Anatolia newt, Neurergus strauchii Steindachner

(1887) (Amphibia: Caudata: Salamandridae)

^erge Bogaerts, 2 Henry Janssen, Jennifer Macke, 4 Gunter Schultschik, 5 Kristina Ernst,

6 Frangois Maillet, 7 Christoph Bork, 8 Frank Pasmans, and Patrick Wisniewski

Hupinelaan 25, NL-5582CG Waalre, THE NETHERLANDS 2 Calvariebergstraat 6, B-8000 Brugge, BELGIUM 3 675 Totavi Street, Los Alamos,

New Mexico 87544, USA 4 Sachsenweg 6, Haus 12, A-2391 Kaltenleutgeben, AUSTRIA 5 Waldgartenstrasse 26, D-81377 Miinchen, GERMANY *24

Rue du Bondar, F-95740 Frepillon, FRANCE D-44359 Dortmund, GERMANY ^Laboratory of Veterinary’ Bacteriology and Mycology Faculty of

Veterinary Medicine, Ghent University ’, Salisburylaan 133, B-9820, Merelbelce, BELGIUM

Abstract. — The long-term experiences of different private breeders on husbandry and breeding of

the Anatolia newt, Neurergus strauchii are presented. This information is introduced and discussed

in respect to the ecology, systematics, and conservation of N. strauchii. Our knowledge and data of

husbandry and captive breeding is collated and compared with the literature. We present our experi-

ences to provide information and advice for the successful long-term keeping, breeding, and raising

of N. strauchii and also an example and model that may be used for privates’ contribution to Conser-

vation Breeding Programs for endangered Neurergus species and other semi-aquatic salamanders.

Neurergus strauchii has proved relatively easy to keep in captivity under a range of aquatic and

terrestrial housing and with adequate diet. However, although breeding is successful under a vari-

ety of conditions survival from egg to adult is low. Cold husbandry temperatures in winter increase

reproduction. Eggs are laid very irregularly in time and number, and oviposition may depend on the

condition of the female, particularly her nutritional condition through diet. There may be up to 285

eggs per female. The best temperature for egg laying is about 14.5 °C. Hatching success of eggs can

vary enormously from 0% to 80%. Most larvae hatch from 11.5 to 14.5 mm. Larvae are easy to raise,

with low mortality over a wide range of temperatures, and metamorphose in three to seven months,

mostly from 55 to 63 mm and about 0.6 g. Several diseases are known to affect these newts and high

temperature stress may exacerbate pathology.

Key words. Neurergus strauchii, breeding, husbandry, ecology, conservation, private breeders, long-term mainte-

nance, diseases, international cooperation

Citation: Bogaerts S, Janssen H, Macke J, Schultschik G, Ernst K, Maillet F, Bork C, Pasmans F, Wisniewski P. 2012. Conservation biology, husbandry,

and captive breeding of the endemic Anatolia newt, Neurergus strauchii Steindachner (1887) (Amphibia: Caudata: Salamandridae). Amphibian & Rep-

tile Conservation 6(4):9-29(e53).

Introduction

Since its description by Steindachner (1887), relatively

little information has been collected on the Anatolia

newt, Neurergus strauchii. Schmidtler and Schmidtler

(1970) were the first to collect substantial information

on this species. In 1982, the first captive breeding expe-

riences were published by Fleck (1982). Haker (1985)

described breeding an F2 generation and the appearance

of a color mutant, later known as the “gold-dust” variety.

Although Fleck and Haker both mentioned that it was

not difficult to keep and breed N. strauchii, it is still rela-

tively rare to find N. strauchii in captivity. Little informa-

tion on the husbandry of N. strauchii has been published,

perhaps due to a lack of husbandry and breeding success.

Steinfartz (1995) was the first to report detailed informa-

tion on the keeping and breeding of the subspecies N. s.

barani, which had been described just two years prior

(Oz 1994).

Inspired by the aquatic versus terrestrial rearing ex-

periments on juvenile N. s. strauchii of Jennifer Macke

(Macke 2006), the scattered Internet data sheets (see for

instance Schultschik 2010; Sparreboom 2009), and the

fact that Kristina Ernst is running a Studbook for this

species for the AG Urodela, Serge Bogaerts started col-

lecting data and experiences from active and long-term

breeders in order to establish some guidelines for suc-

cessful husbandry of this species. In 2007, our common

project was presented at the meeting of the Arbeitsgruppe

Correspondence. Email: 2 hemy.janssen@skynet.be, fpmacke@gmail. com, Hnfo@salamanderland.at, -tina.ernst@yahoo.de,

f ug.maillet@free.fi: 1 christoph.bork@t-online.de, frank.pasmans@ugent.be, 1 s-bogaerts@hetnet.nl (corresponding author).

1 We dedicate this paper to a passionate and experienced amphibian keeper and breeder, Patrick Wisniewski, who sadly passed away

during the time of writing.

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Bogaerts et al.

Figure 1. Captive bred adult female of Neurergus s. strauchii. Photo by Serge Bogaerts.

Figure 2. Adult female of Neurergus strauchii barani photographed at Kubbe mountain, Malatya. Photo by Serge Bogaerts.

Urodela of the Deutsche Gesellschaft fur Herpetologie

und Terrarieukunde (DGHT) in Gersfeld, Germany (Bo-

gaerts 2007). Not all authors have collected similar data

for example, Henry Janssen has put an extraordinary ef-

fort in collecting data on reproduction between 1991 and

1997. However, through collating all husbandry knowl-

edge and data, we can draw some general guidelines for

successfully keeping and breeding N. strauchii. We will

combine the infonnation from both subspecies, as there

appears to be few differences in their maintenance.

Distribution, description, and habitat

Neurergus strauchii is endemic to mountainous areas in

eastern Turkey, roughly from Malatya to Lake Van. The

subspecies N. s. barani is found only in the mountains

southeast of Malatya. Neurergus s. strauchii has a wider

distribution and is found east from the river Euphrates

amphibian-reptile-conservation.org

up onto the Lake Van area. Although there is a relatively

high level of genetic differentiation at both the mitochon-

drial (12S and 16S rRNA) and nuclear levels between the

subspecies (Steinfartz et al. 2002; Pasmans et al. 2006),

it is not very easy to distinguish individuals of each sub-

species, particularly as juveniles. Ozdemir et al. (2009)

found that N. s. barani is not strongly differentiated from

N. s. strauchii, suggesting their distributions are either

connected, or have been separated only recently.

The most obvious visual difference between N. s.

strauchii and N. s. barani is the difference in the num-

ber and size of yellow spots on adults (Figs. 1 and 2).

The main phenotypic difference between the subspecies

is that the number of spots greatly increases during matu-

ration in N. s. strauchii, but increases veiy little in N. s.

barani. The N. s. barani subspecies keeps approximately

its juvenile pattern of small spots in two rows dorsally,

September 2012 | Volume 6 | Number 4 | e53

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Conservation, husbandry, and captive breeding of the Anatolia newt, Neurergus strauchii

Figure 3. Cloaca’s of male (left) and female (right) of N. s. bamni during breeding. Photo by Serge Bogaerts.

whereas the number of spots on N. s. strauchii increases

as it matures. Although this difference is very pronounced

between the eastern populations of N. s. strauchii and N.

s. barani, the westernmost N. s. strauchii are virtually in-

distinguishable from N. s. barani in this respect. Pasmans

et al. (2006) found a geographically correlated increase

in the number of spots on adult newts towards the eastern

part of their distribution.

Neurergus strauchii are relatively large newts, mea-

suring up to 19 cm (Steindachner 1887). Mean lengths

in the wild are 14.3 cm for adult males and 15.2 cm for

adult females (Table 1). The largest total length docu-

mented in the field was 18.1 cm for a female (n = 42)

and 17.6 cm for a male (n = 21) (Pasmans et al. 2006).

Males can be recognized by their slender body, shorter

tale, larger cloaca, and the bluish-white colorations on

the lateral sides of the tail, which can run through to the

lateral sides of the body. These breeding colorations are

often already visible in autumn. Females have an orange

cloaca, relatively longer tails, and shorter legs, and ap-

pear more robust than males (Fig. 3).

Neurergus strauchii lives roughly between 1,000 and

1 ,900 m. above sea level. Its breeding habitats are moun-

tain brooks, preferably with large, deep, slow running

pools. A typical habitat is shown in Figure 4. Terrestrial

habitats are often very bare, without much vegetation (Bo-

gaerts et al. 2006). Water temperatures vary considerably

seasonally and with stream length from springs. Pasmans

et al. (2006) recorded water temperatures in breeding

streams from 10.9 to 17.3 °C, although Schmidtler and

Schmidtler (1970) recorded temperatures of 9 to 10 °C

in a flowing spring in which they found adults. Schnei-

der and Schneider (2010) found water temperatures up to

21.9 °C, at the end of breeding season (June). Bogaerts et

al. (2010) report of a temperature drop of 2.5 °C from 8.3

°C to 5.8 °C within one week at the start of the breeding

season in April, which did not seem to change the breed-

ing activity. From a spring, the water temperature was

only 8.9 °C, but after flowing through a completely de-

forested and heavily grazed valley, the temperature rose

about 2 °C per 100 meters up to 19 °C. Nevertheless, this

wide temperature range is tolerated by N. strauchii, with

Table 1. Mean lengths and weights of adult N. strauchii (Adapted from Pasmans et al. 2006). Data were collected in the breeding

season. There is no significant difference between the subspecies or males and females between the subspecies (/-test).

Subspecies

Sex and number

Mean total

length (mm)

Min - max total

length (mm)

Snout vent

length (mm)

Tail length (mm)

Mean weight

(g)

barani

Males (n = 11)

143

132-153

11.2

barani

Females ( n = 25)

154

134-174

14.0

strauchii

Males (n = 10)

143

131-176

10.3

strauchii

Females (n= 17)

150

129-181

12.7

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Bogaerts et al.

Figure 4. Habitat of N. s. strauchii near Bitlis. Photo by Serge Bogaerts.

the wanner areas probably only increasing the develop-

ment rate of larvae and shortening or shifting the aquatic

phase in the adults. The streams in which the newts were

found by Pasmans et al. (2006) were all slightly alkaline

(pH 7-9) and soft to moderately hard, but these values

can be strongly influenced by heavy rains or periods of

prolonged drought.

Nenrergus strauchii has been found overwintering on

land, not far from streams (Schmidler and Sclnnidtler

1970). Adults, subadults, and juveniles have also occa-

sionally been found under stones on land in April (Pas-

mans et al. 2006). As streams probably partly diy, it

seems likely that N. strauchii spends most of the year on

land under stones or underground, protected from high

temperatures and arid summer conditions. Breeding ani-

mals in streams and pools are found during a relatively

short period in spring from April to June (Steinfartz and

Schultschik 1997; Bogaerts et al. 2010; Schneider and

Schneider 2010).

Protection

Neurergus strauchii is a strictly protected species (Ap-

pendix II) by the Convention on the Conservation of Eu-

ropean Wildlife and Natural Habitats (also known as the

Bern Convention), which was ratified by Turkey in 1984.

In Resolution No. 6 (1998) of the Standing Commit-

tee, N. strauchii is listed as a species requiring specific

habitat conservation measures. The status of N. strauchii

in Turkey is not clear, although the IUCN lists them as

Vulnerable Blab (iii) (Papenfuss et al. 2009). Their cur-

rently known distribution is much larger than previously

thought, but the fact that they live in a habitat that is

sensitive to human influences, and particularly climate

change, makes them vulnerable. Habitat changes and

destruction including overgrazing, pollution of breeding

waters, cutting of trees, appear to currently be the ma-

jor threats to the species (Bogaerts et al. 2006; Schneider

and Schneider 2010).

Materials and methods

Origin of N. s. strauchii

The origin of the N. s. strauchii being kept by the authors

has an interesting history, as it involves extensive co-op-

eration between privates and the N. s. strauchii originat-

ed from a very small gene pool. Henry Janssen was one

of the first people who succeeded in breeding F3 and F4

animals from captive breeding groups started by Fleck

(FI) and Haker (F2) originating from Bitlis, near Fake

Van, Turkey. These were distributed among other private

breeders, including all authors on this article. Gunter

Schultschik had several successful breedings (2000,

2001), and in 2003 Gunter bred a large group of offspring

many of which were distributed within Europe, with a

group being exported to the United States of America.

All N. s. strauchii we have kept are direct descendants of

the first breedings by Fleck. So we conclude that all ani-

mals of this subspecies kept by the authors originate from

the same very small gene pool and we have bred to at

least the F5 generation. Most N. s. barani that are in cap-

tivity originated from small private importations in 1997

and 1998, and two larger importations in 2002 and 2003.

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Conservation, husbandry, and captive breeding of the Anatolia newt, Neurergus strauchii

Housing for adults in captivity

Adults may be housed under a wide variety of condi-

tions. The first main variation in housing is whether they

are kept in an aquatic habitat all year or kept terrestrially

for part of the year. Although in nature they will probably

spend the majority of the year on land away from the

breeding waters, some are kept aquatic for most of the

year, or permanently.

Different types of tanks are used for housing and rela-

tively small: 30 x 40 cm to 50 x 120 cm. Individual carers

use different furnishings for their terrariums. Terrestrial

enclosures are often typical naturalistic terrariums with,

for instance, a well-drained forest soil or loam and pieces

of bark, moss, and plants to create shelter. Gunter Schul-

tschik keeps his animals in a more sterile enclosure, on a

five cm layer of synthetic foam, with shelters made out

of pieces of bark. In this case, each tank is connected to

a water system that drips cold water into the tank slowly,

and seeps through the foam, running out again through a

drain. This system works well in a warm and dry envi-

ronment, but not in a relatively cold moist cellar or base-

ment. When kept terrestrially, in a naturalistic enclosure,

a water bowl is always present, and a gradation of humid-

ity is offered so animals can choose from slightly humid

to dry parts of the habitat.

When kept all year round in an aquarium or aqua-

terrarium, all carers provide the newts with an oppor-

tunity to climb to a dry area, which usually consists

of stone plates that are above the water level (Fig. 5).

These stones are often covered with cork bark or some-

times moss for hiding opportunities. The newts usually

don’t remain in the dry region for long periods, only for

a few hours or occasionally for a few days, except when

temperatures rise above 20-22 °C, then they escape the

water. Henry Janssen notes that in colder periods, with

temperatures below 10 °C, the newts spend most of their

time on land. Temperatures can drop in winter to close

to zero and in summer can rise up to 30 °C. Animals that

are kept aquatic during summer will typically stay in the

water until the temperature of the water exceeds 20-22

°C. Incidental high temperatures of up to 30 °C do not

directly harm the newts, as long as the newts are healthy

and can stay on land.

For lighting, natural light or fluorescent lamps are

used. Temperatures in the tanks usually follow the sea-

son in order to mimic the animals’ natural enviro nm ent

(Table 2). Neurergus strauchii are very good at escape

and will soon notice any chance to escape and take it.

Therefore, it is necessary to cover the aquarium or ter-

rarium with a secure, well- ventilated cover.

Temperature cycling

A cold period occurs in nature from autumn to spring, in

the snow covered mountain areas where these newts live.

In captivity, this cold period is simulated using different

methods as part of the natural reproductive cycle. Half

of the current authors hibernate their animals in a refrig-

erator, approximately from mid-December to the end of

February, at temperatures from 2 to 5 °C or at a constant

4.5 °C. Newts are kept in small boxes with wet paper

towel(s) and bark with the sexes separated. The other

half of the current authors keep newts under a regional

temperature cycle at temperatures varying between 0-10

Figure 5. Aquarium constructed for N. s. strauchii. Photo by Jennifer Macke.

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Bogaerts et al.

Table 2. Mean temperature ranges in the adult environment through the seasons and aquatic (a), aqua-terrestrial (a-t) or terrestrial

(t) set up of the tank.

Keeper

Spring

Summer

Autumn

Winter

Steinfartz (1995)

14 °C (a)

Up to 23 °C (a)

10-14 °C (t)

Henry Janssen

10-17 °C (a)

up to 25 °C (a-t)

10-17 °C (a-t)

7-13 °C (a-t)

Jennifer Macke

16-17 °C (a)

18-22 °C (a)

16-17 °C (a)

2-12 °C (a)

Gunter Schultschik

16-17 °C (a)

up to 30 °C (t)

16 (t)

4.5 °C (t)

Kristina Ernst

12-18 °C (a)

18-27 °C (t)

8-18 °C (t) and more humidity

2-5 °C (t and a)

Frangois Maillet

12-14 °C (a)

17-20 °C (a)

12-16 °C (a)

6-10 °C (t)

Christoph Bork

12-16 °C (a)

17-21 °C (a), max. 25

16-19 °C (a)

< 10 °C (t, for 2 months)

Serge Bogaerts

12-16 °C (a)

Up to 30 °C (a-t)

15-20 °C (t)

5-10 °C in a refrigerator (t)

Patrick Wisniewski

10-15 °C (a)

15-25 °C (a)

15-20 °C (t)

10-15 °C (t)

°C in garages, basements, or garden sheds for one to

three months. Fleck (1982), Haker (1986), and Steinfartz

(1995) all kept these newts in an unheated room where

temperatures could drop as well. This is either done in

terrestrial or aquatic conditions, and both sexes are usu-

ally kept together. Newts can be transferred into another

tank or stay in the same tank. Newts are mostly not fed

during the cold period; only Jennifer Macke feeds them

twice per week throughout the cold period and finds that

they eat well, and are active even when their temperature

is as low as 2 °C.

Diet and nutrition

Adult newts eat many types of living and non-living

food. On land we offer them a wide variety of insects,

including young crickets ( Acheata domesticus or Gryllus

sp.), mealworms ( Tenebrio molitor), fungus beetle lar-

vae ( Alphitobius laevigatas), and larvae of wax moths;

both the lesser ( Achroia grisella ) and greater ( Galleria

mellonella). We also feed earthworms ( Lumbricus sp.),

maggots, firebrats/silverfish ( Thermobia sp.), and slugs.

In water they are fed earthworms, black worms (Lum-

briculus variegatus), Tubifex sp., bloodworms ( Chironi -

mas sp.), Daphnia sp., Gammarus sp., Hyalella azteca,

white worms (Enchytraeus albidus), woodlice ( Asellus

sp.), etc. Amphibian eggs and larvae ( Rana sp.) are eat-

en. Henry Janssen also saw them eat small fish (Gup-

pies, Poecilia reticulata) at night when the guppies were

sleeping. Non-living prey is accepted. Fleck (1982) fed

them slices of liver, and Christoph Bork fed them, with

tweezers, octopus that was cut into small worm-like

strips.

Kristina Ernst reports that keeping females on land

makes it easier to give high calorie food like wax worms,

which seems to yield more eggs the next breeding peri-

od. Henry Janssen has noted that, with equal amounts of

food offered, juveniles grow faster and adults gain more

volume at lower temperatures (10-17 °C) than at higher

temperatures (18-25 °C). Neurergus strauchii is not as

voracious a feeder as, for instance, newts of the genus

Triturus. Neurergus strauchii may be rather slow to catch

prey. Neurergus s. barani seem to be more greedy for

food and eat everything in greater portions, compared to

N. s. strauchii in our experience; it is one of the few sig-

nificant differences between keeping N. s. strauchii and

N. s. barani. We find that feeding plenty of (high calorie)

food during the breeding period is essential for females

to produce many eggs.

Food items offered on land are typically dusted with

a calcium vitamin powder. We have used, for example,

Korvimin ZVT, Amivit A, Nutrobal Vitamin/Mineral

powder, and ZooMed Calcium. Gut loading crickets with

calcium rich plants, like dandelion, or nettles will en-

rich their food quality. Feeding crickets at temperatures

below 10 °C is difficult as most crickets die. Individual

newts can have very different preferences for food items.

Results

Breeding

For breeding purposes, the newts are placed into an

aquarium. The tanks are furnished in various ways. Most

of us use a layer of gravel on the tank floor, and various

types of stones are placed on top of each other to provide

places for hiding and egg deposition. Jennifer Macke

uses turned over non-glazed ceramic flower pots with

a cut out entrance, used by the females to deposit their

eggs, which can easily be taken out with the eggs and

replaced. Some of us have used no substrate or just a few

flat stone plates, covering only part of the tank bottom.

Tables 3 and 4 report the periods, temperatures, and other

characteristics of the various breeding tanks.

Development of enlarged cloacas and the whitish-blue

colorations on tails of males can already be observed in

autumn. The smallest male in captivity bred measured

11.5 cm total length (TL) and 6.2 cm snout-vent length

(SVL); the smallest female measured 12.8 cm TL and

6.5 cm SVL. Thus, animals start breeding at total lengths

of around 12 cm TL. Breeding occurs within a water

temperature range of 9-17 °C (mean 10-14 °C) and this

seems to be independent of the time of the year (Table

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Conservation, husbandry, and captive breeding of the Anatolia newt, Neurergus strauchii

Table 3. Aquarium conditions when breeding started. Included are only those years in which fertile eggs were deposited.

Keeper

Subspecies

Year

Starting

Temperature start

breeding (°C)

Water level

(cm)

Water circulation

and/or air pump

Fleck (1982)

strauchii

1981

March

yes

Steinfartz (1995)

barani

1993-1994

Feb-March

yes

Jennifer Macke

strauchii

2005-2009

2011-2012

Dec-Jan

9-12

yes

Gunter Schultschik

strauchii & barani

2003-2004

Jan-Feb

16-17

yes

2004

May

April

Kristina Ernst

strauchii & barani

2005

2011

11-12

yes

2012

Feb

10-12

Francois Maillet

barani

2005

March-

April

12-14

12/15

yes and air pump

Christoph Bork

strauchii & barani

2001

2003

2005

Feb

13-15

24-28

yes

Patrick Wisniewski

strauchii

1996 1997

Feb-March

10-12

strong air pump only

Serge Bogaerts

strauchii

2006

Feb

12-14

yes

3). Newts were bred in winter, early spring or even to

the end of spring. The water level does not seem to be

important. As these newts are stream dwellers, most of

us have simulated this by using water circulation, some-

times with the addition of an air pump.

Breeding starts with male activity, typically at water

temperatures of 10 °C. Males and females can be put in

the water at the same time, but some of us prefer to intro-

duce females to the water a few days or weeks later. Af-

ter entering the water, males have been observed to start

performing courtship the same evening. Within the court-

ship period, it is best to try and keep water temperatures

below 14 °C. At 14 °C females start oviposition (Table 4

and Fig. 6).

Figure 6 shows oviposition in three of the most suc-

cessful breeding years, in relation to the water tempera-

ture. Oviposition may take place during both day and

night and may continue until water temperatures reach

about 20 °C. Eggs are laid very irregularly in time and

number, and oviposition may depend on the condition of

the female, particularly her nutritional condition through

diet. Occasional egg laying (one per day or less) can

continue for up to two months after the main period of

oviposition.

Henry Janssen measured the water temperatures at

which oviposition took place for 1,225 eggs from dif-

ferent breedings over the years 1991-1997. He also

noted which of these eggs hatched. Of all eggs, only six

(0.48%) were laid at water temperatures below 14 °C.

Most eggs (77.3%) were deposited at temperatures of

15-19 °C. Above 20 °C, production of eggs rapidly de-

creases. Figure 1 shows a dip at 16-17 °C, but we think

this is an artifact of the combination of data from differ-

ent years. Another finding of Henry Janssen is that of all

eggs that were deposited, the ones laid between 14-16 °C

had the best hatching rate (62.4% between 14-15 °C and

Figure 6. Oviposition (n = 760 eggs) in three successful breed-

ing years in relation to water temperature. Data by Henry Jans-

sen.

28.5% between 15-16 °C). There are several possible in-

terpretations for these data. First, it may be related to the

fecundity of the females; the first eggs laid are often of a

higher quality than later eggs. Second, it could be related

to the fertility of the males, which seem to be more active

at lower temperatures. Jennifer Macke has also noted that

egg fertility consistently decreases over time during the

egg laying period (data not shown). Henry Janssen noted

from the 1995 breeding season that when he separated

females from males, after he discovered that males were

eating some of the first eggs, most eggs laid afterwards

were not fertilized. This seems to indicate that regular

uptakes of spermatophores by the female, during the

breeding period, are necessary for her to continue pro-

ducing fertile eggs.

Table 4 records the aquarium conditions when fe-

males started oviposition — the number of eggs per fe-

male, and the percent of hatched eggs. As can be seen,

large variations were found in number of eggs per female

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Bogaerts et al.

Table 4. Conditions in the aquarium when females started oviposition, number of eggs per female (~ when more females are kept to-

gether), time to metamorphosis, and percent hatched. - No data available. # Average over the whole oviposition period. *Ten of these

are 14 months old but still have not completed metamorphosis; they show no differences in length compared with their siblings.

Number of

Time to meta-

Keeper

Subspecies

Year

Starting

T°C

eggs per

morphosis

Hatched

female

(months)

Fleck (1982)

strauchii

1981

April

~ 75

4.5

Haker (1986)

strauchii

1985

June

Steinfartz (1995)

barani

80-90

2005

Feb 16

152

-50%

2006

Feb 19

150

-50%

2007

Feb 27

104

Jennifer Macke

strauchii

2008

March 4

246

2009

Feb 27

285

2011

Feb 26

238

mean 41% #

2012

March 8

195

mean 78% #

2004

May

Gunter Schultsckik

strauchii

2005

2011

May

April

11-12

yes

2012

Feb

10-12

barani

2004

June

-200

5-8

- 50%

barani

2005

May

20-21

- 100

4-7

- 25%

strauchii

2005

May

17-19

- 150

4-7

98%

Kristina Ernst

barani

2006

May

-250

- 75%

strauchii

2006

May

-200

97%

strauchii

2011

April

- 150

4-7*

88%

strauchii

2012

March

- 100

80%

barani

2012

April

- 100

90%

Christoph Bork

strauchii &

barani

2001

2003

2005

March

14-16

- 4

No counts, but

never 100%

strauchii

1992

Mar-April

14-17

129

4-8

45%

Henry Janssen

strauchii

1995

April-May

16-19

4-8

strauchii

1996

April

16-17

-85

4-8

25%

Patrick Wisniewski

strauchii

1996

March

10-15

5-6

45%

strauchii

1997

February

10-15

5-6

50%

Serge Bogaerts

strauchii

2006

March

14-16

-40

5-10

70%

and hatching rates. However, the temperature conditions

in which oviposition occurred were roughly the same for

all of us, for both subspecies.

Eggs

Eggs are mostly attached to the underside of stones (Fig.

7), but they can be laid almost anywhere, including on

the filter, aquarium walls, and plants (Fig. 8), or specially

prepared flower pots. Eggs may be found loose on the

bottom of the tank, but this mainly occurs when there is

too little space on the favorable places and, or eggs are

not well attached. During oviposition the female lies on

her back, often sandwiched between two layers of flat

rock, depositing eggs on the underside of the upper rock.

It is important that the habitat has enough space between

the stone plates for the females to move around. Henry

Janssen noted that out of a total of 560 eggs, 237 were

deposited on the glass, 199 on stones, 83 loose on the

substrate, 37 on plants, three on the filter system, and one

was stuck to the hind leg of a female. No negative effects

from exposure of developing eggs to indirect sunlight or

artificial light could be observed when compared to eggs

that developed under darker conditions.

In general, eggs were removed from the breeding

tank, as the adults sometimes eat the eggs. Eggs were

typically removed every few days. Some of us moved the

eggs together with the stones they were attached to, oth-

ers cut the eggs gently loose from the rocks with a razor

blade or fingernail. There was no difference observed in

the development of eggs that were cut loose versus eggs

that were left on the stones they were laid upon.

Water parameters of the tank, where the eggs are put

to hatch, do not seem to matter. Even an air stone is not

really necessary for the development of the eggs. If the

water is refreshed once a week this seems to be enough.

It is, however, also possible to leave the eggs in the tank

until they hatch, which some of us prefer.

In all our breedings, no clutch of eggs was 100%

fertile. Unfertilized eggs and eggs that have died off,

shrink in size and start decaying, resulting in the clear

layers around the zygote becoming cloudy, starting with

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Conservation, husbandry, and captive breeding of the Anatolia newt, Neurergus strauchii

Figure 7. Female N. s. strauchii depositing eggs. Photo by Christoph Bork.

the innermost layer and continuing outwards, followed

by mould — growth on the outer surface (observations

Henry Janssen; Fig. 9). It seems that a developing egg,

attached to a moulding egg, can be infected with fungus

too. Therefore, it is best to separate moulding eggs from

developing eggs. Eggs can be eaten by the usual preda-

tors like snails and flat worms ( Planaria sp.). Hatching

success of eggs can vary enormously (Table 4). Jennifer

Macke noted that in 2005 about 50% of eggs were fertile,

and 10% began to develop but died as embryos. In 2006

about 80% were fertile and about 10% began to develop

but died as embryos. Malformations seem to occur in

all breedings. Kristina Ernst states that through feeding

the females more often, more eggs are produced and in

shorter periods. She observed up to about 15 eggs per day

per female.

In 2005 Jennifer Macke had eggs laid from February

until the beginning of March. After that animals were

transferred to another location and they continued to lay

eggs (about one a day), but all eggs produced in April

and May were infertile. In 2009 Jennifer counted a total

of 570 eggs from two females during the entire egg lay-

ing period (February- June). Henry Janssen measured the

hatching success of all eggs deposited between 1991 and

1997, each year breeding occurred. Of the total of 1,413

eggs, 348 hatched (24, 62%).

Gunther Schultschik noted the exact water parameters

in his rearing tanks. Larvae were raised at a water tem-

perature of 16-19 °C, with no measurable organic ions in

the water (NH 3 , N0 2 , N0 3 ), maximum of oxygen, mini-

mum of CO,. Water was treated by UV lamp. PH was

7.2 to 7.5. Francis Maillet maintains a pH of 7-8 and

changed part of the water often to avoid nitrate develop-

ment.

Henry Janssen measured the length at hatching for

283 specimens (Figure 10). About 45% of the measured

larvae were between 12 to 14 mm at hatching. Fig. 11

shows a hatching larvae.

Henry Janssen measured the relationship between

days of incubation and total length at hatching for 249

larvae. The shortest time to hatch was 15 days and the

longest was 34 days. About 57.4% of all larvae hatch be-

tween 26 and 3 1 days after deposition. Consistent with

this, Jennifer Macke found that from the time the first

eggs were laid until the first larva hatched, exactly 30

days elapsed when the eggs were maintained at 16-17 °C.

The total length of the larvae becomes larger when

hatching is delayed. Thus, the moment of hatching is not

a fixed point in time. Moving the egg, for instance, can

cause the larva to leave the egg shortly thereafter, where-

as it would have stayed in place if the egg had been left

undisturbed.

Larval rearing

All authors raised their larvae in more or less the same

way, and all agreed it was not very difficult or problem-

atic. For the first few days after hatching, the larvae live

on their yolk. No food was added at this time, and some

f/i

J J i

f/M

Figure 8. Fresh laid N. s. strauchii egg. Photo by Henry Jans-

sen.

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Bogaerts et al.

Figure 9. Moulding unfertilized eggs of N. s. strauchii on mm

paper Photo by Serge Bogaerts.

Figure 10. Total length of larvae at hatching in mm. Data by

Henry Janssen, n = 283.

authors noted that micro-organisms, particularly water

mites ( Hydracarina sp.) and Cyclops sp. attacked new-

ly-hatched larvae. After a few days the larvae begin to

eat live food. Larvae are kept in tanks or tubs containing

three to 20 cm of water, an air stone, and some pebbles

and pots as hiding places. Aquatic plants are sometimes

included. Larvae are fed first with Artemia (only the first

one or two weeks), small live Daphnia sp., Tubifex/Lum-

briculus (initially chopped, later whole), red mosquito

larvae/bloodworms ( Chironimus sp.), and white worms

( Enchytraeus albidus ). Gunter Schultschik gave Artemia

until the larvae were 20 mm. When feeding Daphnia,

care must be taken to avoid feeding other less harmless

aquatic fauna. Water temperatures can range from 10 to

20 °C. Even if the temperature of the water rises up to

30 °C accidentally, it is not a serious problem, although

larvae stop eating and become less active.

The larvae are not as aggressive toward each other

as, for instance, Triturus larvae, but care must be taken

to avoid overcrowding. Kristina Ernst noted cannibalis-

tic behavior until the larvae were 1. 5-2.0 cm, at which

point the behavior disappeared. Several of us have never

observed cannibalism and even kept larvae of different

sizes together without a problem. Most of us have kept

the larvae in small groups (15-30 larvae) in, for instance,

plastic containers of various sizes with aquatic vegeta-

tion and shelters, like pieces of ceramic garden pots, as

these salamanders hide during the day. Water is refreshed

every week, or as often as required to avoid poor water

quality.

In some cases, malformed larvae hatch. These larvae

spin around when trying to swim, or are swollen. These

larvae often lag far behind their siblings in growth, and

euthanasia is the best option. Larvae of a few centime-

ters in size develop gold colored, shiny spots and dots

that seem similar to the lateral line sense organs in fish

used to detect movement and vibration in surrounding

water (Fig. 12), which stay visible until metamorphosis

(Fig. 13). After about three to four months the larvae de-

Figure 11. Hatching larvae of A. s. strauchii. Photo by Serge Bogaerts.

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Conservation, husbandry, and captive breeding of the Anatolia newt, Neurergus strauchii

Figure 12. Larva of N. s. strauchii few weeks old, the lateral line sense system visable in stripes on lateral sides and tail and in spots

behind the eye. Photo by Serge Bogaerts.

Figure 13. Larva of N. s. strauchii of approximately four months old. Photo by Serge Bogaerts.

velop yellow spots and later become darker and darker

developing their juvenile black pattern (Figs. 14, 15).

Another one to three months may elapse before the gills

are completely gone. Mortality of larvae is very low. Lar-

vae become lighter in color at night. Depending on the

water temperature and the amount of food, larvae meta-

morphosed in three to seven months, with a mean period

of about five months (Table 4).

The first shedding takes place at around the time of

metamorphosis, sometimes just before emergence from

the water. They leave the water mostly at night and

search for a hiding place, and if not provided, they try to

hide again in the water. The first few weeks after meta-

morphosis, the juveniles can be kept in an aqua-terrarium

with different hiding places from wet to dry, from which

they can choose. Metamorphosis in this newt seems to be

very gradual, such that juveniles continue to shift from

water to land during a period of several weeks.

After metamorphosis the juveniles resemble their par-

ents, although they have significantly fewer yellow spots,

and spots are confined to two rows along their backs. The

bellies are not completely black and show light-colored

parts. The orange-red stripe on the belly is rose-orange

and not as brilliant as in the adults. We are positive color

intensity in captive-raised adults depends on the amount

of carotenoid-rich food animals eat, like in the Japanese

fire belly newt, Cynops pyrrhogaster (see Matsui et al.

2003).

Henry Janssen measured the total length of 108 speci-

mens at the moment of metamorphosis (Figure 16). The

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Bogaerts et al.

Figure 14. Larva of N. s. strauchii change its coloration to juvenile pattern. Photo by Serge Bogaerts.

Figure 15. Larva of N. s. strauchii just before metamorphosis. Photo by Serge Bogaerts.

data include only larvae that metamorphosed within

the year eggs were laid. Metamorphosed N. s. strauchii

weigh about 0.60 g (n = 11, with mean total length of 55

mm; data Serge Bogaerts) which corresponds to Schult-

schik (data not shown) who gives 0.67 g for metamor-

phosed N. s. strauchii.

Henry Janssen measured the rate of metamorphosis

of all eggs deposited between 1991 and 1997 in which

breeding occurred each year. Of the total of 1,413 eggs,

only 138 specimens reached metamorphosis (9.8%) (see

Table 5).

Metamorphosis was considered as the moment the

gills disappear, the black and yellow coloration are vis-

ible, and juvenile newt(s) come onto land for the first

time. However, this is not a fixed moment. They can stay

in a semi-aquatic stage for a while, with very short gills

and full black and yellow coloration. The data of Hen-

ry Janssen show that there is a wide range of lengths at

which metamorphosis can take place (Fig. 16). All of the

measurements taken by other breeders have fallen within

these ranges (Table 6).

“Overwintering” larvae

In both N. s. strauchii and N. s. barani, overwintering

larvae are observed. Larvae that hatch later in the season,

or stay behind in development, will remain larvae dur-

ing the winter and metamorphose the next year. Fleck

(1982) and Haker (1986) describe N. s. strauchii still

found in larval fonn in January. Pasmans et al. (2006)

describe this phenomenon for N. s. barani. During a field

visit in May 2006, special attention was paid to this phe-

nomenon at the type locality of N. s. barani, and many

larvae that hatched in 2005 could be observed (S. Bo-

gaerts, pers. obs.). The larvae keep their gills and fins,

but develop characteristics of the juvenile coloration:

black background color and yellow spots. Overwintering

larvae seem to grow a bit larger than their siblings that

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Conservation, husbandry, and captive breeding of the Anatolia newt, Neurergus strauchii

Table 5. Survival rate from egg laying until metamorphosis over seven years of breeding. Data by Henry Janssen.

Year

Number of eggs

Hatched eggs

Metamorphosed

Success rate per year (%)

1991

1992

514

229

9.3

1993

28.2

1994

5.1

1995

476

6.3

1996

171

19.8

1997

Table 6. Lengths of larvae at metamorphosis.

Keeper

Subspecies

Length (mm)

Remarks

Schmidtler and Schmidtler 1970

strauchii

54-61

Fleck 1982

strauchii

54-55

Steinfartz 1995

barani

Henry Janssen

strauchii

47-75

Gunter Schultschik

strauchii

45-50

Kristina Ernst

barani & strauchii

40-60

Jennifer Macke

strauchii

60-65

Still with gills

Francois Maillet

barani

55-60

completed metamorphosis the previous year (up to 75, 25

Jennifer Macke tested the difference between terres-

mm; data Henry Janssen).

Raising juveniles

Fleck (1982) writes that raising juveniles is not problem-

atic, as they easily switch between aquatic and terrestrial

living, and can be kept and raised in an aqua-terrarium.

Most of us raise the juveniles terrestrially. This method

of rearing is most like their natural conditions, where ju-

veniles live terrestrially until reaching reproductive age.

A small terrarium (50 x 20 x 15 cm) is often used, with

a leaf litter soil (typically from beech or oak forest), or a

mixture of substrates (soil, coconut fibre, etc.) and some

pieces of bark, which the newts use as shelter. A more

sterile option with moist paper towel(s) and some pieces

of bark also works well, but needs cleaning at least once

a week. The juveniles are fed at a minimum of once a

week, or usually more (further details above under the

“Diet and nutrition” section on page 14). Tanks should

provide a range of dry and moist places (Fig. 17). Frank

Pasmans raised juveniles on wet Kleenex kitchen towel

paper, with pieces of ceramic roof tiles piled up, creating

gradients from moist to dry.

Foods are prepared similar as for the adults and are

typically small crickets, small wax wonns, slugs, fruit

flies {Drosophila sp.), woodlice {Asellus sp.), firebrats/

silverfishes ( Thermobia sp.), etc. Further, bloodworm

(Chironimus sp.), Tubifex sp., or chopped earthworms

and blackworms can be fed from a small bowl or on a wet

paper towel. They can be kept in the same temperature

ranges as adults. Our captive bred animals have reached

at least the age of 12 years.

trial and aquatic raising of juveniles. In March 2004, four

of the juveniles obtained in October 2003 were adapted

to water at a size of about 7-8 cm total length. This was

accomplished by placing them, one at a time, into an

1 8-liter (five gallon) tank containing two cm (one inch)

of water, a thick layer of aquatic plants, and an ample

supply of live blackwonns {Lumbriculus variegatus),

and chopped earthworms. Each animal adapted to hid-

ing beneath the plants within one day. Once adapted to

water, they were moved to a larger tank (60 x 30 x 30

cm) containing 25 cm of water, large river rocks, clay

pots, and a mini canister filter providing a bit of current.

Local tap water comes from ground water that is alkaline

and moderately hard (GH 70 ppm, KH 90 ppm, pH 8).

Both the aquatic and terrestrial animals appeared healthy

and grew well. Feeding regimens were, of necessity, dif-

Length at metamorphosis

a> 8

C 6

1111

. n

_.UL_D 0

<y* Gy 3 ^ Gy 5 <0^ <0^ Qy 3 <§* A*'' A^ A^ ^

length (mm)

Figure 16. Length at metamorphosis (n = 108; data by Henry

Janssen).

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Bogaerts et al.

Figure 17. Set up for raising juvenile N. s. strauchii. Photo by Jennifer Macke.

ferent for the two groups. The terrestrial group was fed

as described above, including live blackworms ad libi-

tum. The aquatic group was hand fed almost every day

with chopped earthworms and occasional fly larvae or

crickets. They were also given some live blackworms

during the first months. However, when a large popula-

tion of leeches was discovered in the tank (and one leech

was observed briefly attached to one of the newts), no

more blackwonns were given. By August 2004, the typi-

cal size of the terrestrial animals was 10 cm, while the

aquatic animals were approximately 12 cm and more

heavily spotted. The aquatic group mated and bred the

following winter, while the terrestrial animals showed no

sign of breeding readiness. By August 2005, the aquatic

animals were all 12-13 cm, while the terrestrial group

had reached 11-12 cm, and males of both groups had

enlarged cloacas and some white highlights on the tail.

Thus, it can take just two years between egg and breeding

adult (at least for males). In our experience, females need

one year more to become adult, and when raised more

slowly (given less food), they take three to four years to

mature.

Gold dust variety

Haker (1986) first bred some aberrant color morphs,

known as the “gold dust” variety — originated because of

their appearance of being sprinkled with gold dust and a

black line along the dorsal side (Fig. 18). This fonn oc-

casionally still occurs in breedings directly derived from

Haker through Henry Janssen. The number of individuals

is very low, noted Patrick Wisniewski. In the first breed-

ing of 35 metamorphs, two were “gold dust,” and in the

second batch of nine metamorphs, only one. This form

has not appeared since the breedings of Henry Janssen,

in any of the other breeding groups, that are involved in

this article.

Diseases

Very little is known regarding diseases occurring in newts

of the genus Neurergus. As in most urodelans, inadequate

husbandry (including poor water quality) and/or nutrition

are probably the most important predisposing factors for

disease. More specifically, for Neurergus , most disease

cases appear to occur during summer months, suggesting

this species to be sensitive to higher temperatures (>20

°C). A six week quarantine period is recommended when

having first obtained animal(s). During this period, the

newly acquired animal should be assessed by a qualified

veterinarian for the presence of infectious and non-infec-

tious diseases. We strongly recommend every newly ac-

quired animal to be tested for the presence of ranaviruses

and Batrachochvtrium dendrobatidis . The presence of

both agents can be assessed by detection of their respec-

tive DNA in skin swabs (less sensitive for the detection

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Conservation, husbandry, and captive breeding of the Anatolia newt, Neurergus strauchii

Figure 18. Adult of A. s. strauchii of “Gold-dust” form. Photo by Henry Janssen.

Figure 19. Metabolic bone disease in an adult female N. s.

strauchii. Note the malformation of the lower jaw. Photo by

Frank Pasmans.

of ranaviruses) or tail clips. Trade derived animals have

indeed been identified as important carriers of both infec-

tious agents and may spread diseases to native amphibian

populations. Both diseases have been listed by the Office

International des Epizooties or World Organisation for

Animal Health (OIE) as notifiable diseases since 2008.

The following disorders have been diagnosed in Neurer-

gus (in part by F. Pasmans, pers. observ.):

1) Metabolic bone disease (MBD, Fig. 19). MBD

comprises a number of metabolic disorders affecting

skeletal calcification. In urodelans, most cases of MBD

can probably be attributed to relative lack of calcium

and/or vitamin D in the feed, and would thus be more

appropriately named, nutritional secondary hyperpara-

thyroidism. Clinical signs are most obvious in young,

terrestrial specimens, and include backbone and head

malformations (e.g., shortening of the lower jaw), and

abnormal movements. MBD can be prevented by supply-

ing feed items (e.g., crickets) with extra calcium through

the insect diet (“gut loading”) and topically applying cal-

cium containing powder on the feed insects. However,

this is only applicable for juveniles raised on land and for

terrestrial adults. Feeding calcium supplementation for

aquatic newts is much more difficult to achieve and may

in part be met by providing calcium supplemented pellet

feed (e.g., turtle pellets, if accepted by the newt).

2) Ranavirosis. Recently, ranavirosis has been de-

scribed in N. crocatus, imported from Iraq (Stohr et al.,

in prep.). Clinical signs of this viral disease include red-

dening of the skin (erythema), skin ulceration, edema,

anorexia, and death. The course of a Ranavirus infection

may vary from subclinical (without clinical signs) to

mass mortality. This virus is one of two known infectious

threats to amphibian biodiversity worldwide. Prevention

consists of quarantine measures of newly acquired ani-

mals and preferably testing of a tail clip or skin swab for

the presence of the viral DNA. It is of utmost importance

to prevent any contact of Ranavirus -infected newts or

their enviromnent (e.g., aquarium water) with the envi-

ronment, to prevent spread of the virus to native amphib-

ian populations. Ranavirosis cannot be treated.

3) Chytridiomycosis. This fungal disease is caused

by Batrachochytrium dendrobatidis and is considered the

most important infectious driver of worldwide amphib-

ian declines. For this reason, it is of utmost importance

that (as for ranavirosis), captive populations of Neurer-

gus are negative for the fungus. It is at present not clear

whether this fungus causes clinical problems in newts of

the genus Neurergus. In other amphibians, the course of a

B. dendrobatidis infection may vary from asymptomatic

to apathy, skin disorders, and death. Recently, B. dendro-

batidis infection was demonstrated in N. kaiseri (Spitzen

van der Sluijs et al. 2011) but no clinical signs of disease

were noticed. As a preventative measure, all newly ac-

quired Neurergus should be tested for the presence of the

fungus using a skin swab. If positive, infected animals

and their captive environment should be treated appro-

priately. Neurergus kaiseri was treated successfully us-

ing voriconazole (F. Pasmans, pers. observ.; Martel et al.

2011). As for ranaviruses, all contact of B. dendrobatidis

infected animals and their captive environment with the

outside environment should be strictly prevented.

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Bogaerts et al.

Figure 20. Ascites (“bloating”) in an adult female N. s. strauchii with a severe enteritis, associated with high numbers of flagellates.

Photo by Frank Pas mans.

4) Chlamydiosis. For more than a decade, enigmatic

mortality in captive N. crocatus and N. strauchii newts

was observed by several breeders. This mortality even

impaired the establishment of successful breeding pro-

grams in for example N. crocatus. In the nineties of the

past century, entire captive breeding groups of this newt

were lost. Keepers reported non healing wounds on the

tail. Recently, the cause for this mortality was suggested

to be a bacterium: Candidatus Amphibiichlamydia sal-

amandrae (Martel et al. 2012). The disease presents as

anorexia, lethargy, edema, markedly abnormal gait, and

death. Secondary bacterial or mycotic infections (e.g.,

with Aeromonas sp. or Mucor sp.) appear to be common.

Urodelans can be very probably latent carriers of Chla-

mydia bacteria, with possible reactivation of the infection

during stress periods. Indeed, Chlamydia infections are

probably widely spread in urodelan collections and clini-

cal signs are possibly provoked by suboptimal condi-

tions, for example, elevated temperatures during summer

months. Until now, clinically infected animals invariably

die but therapy may consist of the use of, for example,

tetracyclines to cure the infection. Preventative measures

consist solely of quarantine measures and optimal hus-

bandry (including temperatures <20 °C).

5) Intestinal parasitosis (Fig. 20). As in all amphib-

ians, intestinal parasitosis may occur in Neurergus newts

and appears to be mostly provoked by suboptimal hus-

bandry. Several cases of severe enteritis, coinciding with

very high numbers of flagellate protozoa were diagnosed

in N. strauchii and N. crocatus. Clinical signs were an-

orexia, loss of condition to cachexia, and in some cases

ascites (bloating). Treatment using metronidazole and

optimizing husbandry was successful in cases with an

early diagnosis.

Conclusions

In addition to their beauty, N. strauchii are interesting

newts in captivity. Although our data are still scattered

and incomplete, the results of this project presents good

indications for long-tenn captive maintenance and gives

direction for further studies especially, when our experi-

ences differ, or have revealed new topics to study.

Our main goal in keeping this newt has been its suc-

cessful breeding. We vary in our opinions about the

importance of a terrestrial period as part of the yearly

breeding cycle. Although, it is in their natural cycle to

have a terrestrial period both Fleck (1982) and Steinfartz

(1995) write that a terrestrial phase is necessary to initi-

ate breeding. Fleck kept his animals from 1975 to 1979

in an aquatic enclosure, but males and females were not

synchronized in their breeding behavior. He gave three

animals a terrestrial phase in 1980 and then both sexes

got into breeding condition at the same time. However,

Jennifer Macke has bred the same group of animals for

eight years without any terrestrial periods, while most of

us experienced that animals were less willing to breed

when they were not given a terrestrial period.

Thus, if keeping adults aquatic or not, the whole year

round is not of major importance in breeding these ani-

mals, we show that a dramatic change in temperature,

often combined with an abrupt shift from land to water

is probably more important. Steinfartz (1995) reported

that in his opinion it is not a low temperature in win-

ter that is necessary for successful breeding, but a strong

temperature difference between summer and winter pe-

riod. However, our findings indicate a strong correlation

between specific temperatures and the specific phases of

reproduction. A period with temperatures below 10 °C

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Conservation, husbandry, and captive breeding of the Anatolia newt, Neurergus strauchii

Figure 21. Proposed yearly temperature-curve for the captive breeding of Neurergus strauchii.

prior to the breeding season proves essential to realize

the temperature curve that stimulates breeding (Fig 21).

Hence, a terrestrial period may help to synchronize the

sexes and breeding behavior. Adults can be kept all year

round aquatic and will still breed, but need to at least

undergo a change in temperatures. Keeping animals in a

terrestrial phase makes it easier to change temperatures

by, for instance, placing them in a refrigerator or out-

doors. Another advantage of a terrestrial period is that

one can provide more differentiation in food items (e.g.,

crickets, wax worms, and other insects) which increased

diet quality.

It seems that changing the newts between enclosures

is not a drawback. When animals are kept the whole year

in the same tank, with just gradual changes of temper-

ature, they will not breed, but if they have a dramatic

change of environment (or change of temperature), they

are likely to initiate breeding behavior. We all agree that

giving the newts a cold winter period is the best way to

have a successful breeding.

Although Sparreboom et al. (2000) noted interfer-

ing males when a couple is mating, it does not seem to

decrease the success rate of breeding, but if undisturbed

breeding is the goal, one should keep one male together

with one or more females during the breeding period.

For successful initiation of oviposition, it seems that

a shift in temperature from 12-14 °C (courtship behavior

and development of eggs) to 16-18 °C is important. A

temperature stable environment where the tank is placed

(basement) or refreshing the water can help provide this.

The period of egg laying seems to depend on the gradual

rising of temperature. If temperature rises quickly this

can reduce, or even eliminate, the period of egg laying.

Henry Janssen noted such negative influences on his

breeding results, caused by rapid and unwanted tem-

perature changes, typical for the sea climate where he

lives. It seems therefore important for the breeder to have

some control over water temperature. In nature, depend-

ing on the weather, mating season starts approximately

at the end of April to beginning of May for both sub-

species (Bogaerts et al. 2006) and continues into June

(Schmidtler 1994). In captivity, temperature is of more

influence than the time of the year and newts are prepar-

ing to breed when temperatures rise above 10 °C.

Although eggs are mostly “spawned” on the under-

side of stones, they can be laid anywhere, as described.

Bogaerts et al. (2006) found some eggs of A. v. barani on

tree branches and at the bottom of water bodies, but con-

cluded it was an artifact due to the lack of other suitable

sites. This might also be true for captive populations.

Eggs laid or kept in lighter enviromnents develop in the

same manner, and we have not found any differences in

development. Development of eggs does not seem to be

influenced by taking them out of the breeding tank or

cutting them loose from stones. The eggs are not deli-

cate. One can choose the way that suits the breeder best.

Taking the eggs out of the tank gives the breeder more

control.

Our data show total number of eggs per female can

be much higher, up to 285, than previously reported

(Schmidtler and Schmidtler 1970; Fleck 1982; Stein-

fartz 1995). It seems likely the amount of food given to

females adds to production of more eggs. Even young

females can lay many eggs, thus size of the female does

not seem to be a major factor determining the amount

of eggs laid, but the amount of food given probably is

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Bogaerts et al.

a contributing factor as well; however, we do not have

enough data to support this claim. There doesn’t seem to

be a difference between the two subspecies in the number

of eggs.

Steinfartz (1995) stated that in his opinion the lar-

vae of N. s. barani are more pond-type, in comparison

to stream-type larvae of N. s. strauchii, based on minor

differences. In the experience of the authors that have

kept both subspecies, it is impossible to tell larvae apart.

However, perhaps N. s. barani grows a little larger and

more robust before metamorphosis. But we do not have

data to support this.

Rearing of the larvae and juveniles was relatively

unproblematic in all cases, as long as water quality is

checked regularly. Raising juveniles can be done in a ter-

restrial environment or in an aqua-terrarium. In nature,

juveniles certainly grow up terrestrial, as aquatic juve-

niles have never been observed in the field. Raising them

in an aqua-terrarium gives the opportunity to feed them

more varied types of food. The newts are able to switch

easily from land to water and vice versa, and they adapt

quickly to water without skin problems. Jennifer Macke

showed a slightly faster growth of aquatically-raised

animals. But as the number of animals is very small and

because the feeding regime and types of food differed,

it is not possible to draw straightforward conclusions. It

seems likely that growth depends more on quality and

availability of food and temperature, than on the type

of housing. In the past, whole groups of captive bred N.

strauchii have collapsed; also among the authors. Sev-

eral possible and proven candidates have been described

above. We strongly advise to avoid stress (e.g, high tem-

peratures >20 °C) and provide optimal husbandry and

feeding.

We hope our successful long-term keeping, breeding,

and raising of N. strauchii is an example and model that

may be used for private contributions to conservation

breeding programs, for endangered Neurergus species

and other semi-aquatic salamanders. Future studies on

captive specimens will provide more data on the cap-

tive breeding of this, and other newts. According to the

Studbook (Molch-Register) by Kristina Ernst it seems

this species is still available in good numbers, but con-

sistent breeding every year is still rare, even among the

authors. Hopefully, this paper can contribute to greater

captive breeding efforts and to a better understanding of

the ecology of this fascinating newt but also can be seen

as a valuable example of privates’ contribution to con-

servation breeding programs for endangered Neurergus

species and other semi-aquatic salamanders.

Acknowledgments. — Henk Wallays is thanked for his

support and encouragement in the early part of the proj-

ect. We thank the AG Urodela (www.ag-urodela.de) and

the Salamander Society (www.salamanders.nl) for their

support.

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Martel A, Adriaensen C, Bogaerts S, Ducatelle R, Hae-

sebrouck F, Pasmans F. 2012. Novel Chlamydiaceae

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Martel A, Van Rooij P, Vercauteren G, Baert K, Van

Waeyenberghe L, Debacker P, Gamer TW, Woeltjes T,

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Ozdemir N, Uzurn N, Avci A, Olgun K. 2009. Phylog-

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Turkey based on morphological and molecular data.

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Papenfuss T, Sparreboom M, Tok V, Ugurtas IH, Seville

M, Kuzmin S, Anderson S, Eken G, Kilic T, Gem E.

2009. Neurergus strauchii. In: IUCN 2011. IUCN Red

List of Threatened Species. Version 2011.2. [Online].

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Pasmans F, Bogaerts S, Woeltjes T, Carranza S. 2006.

Biogeography of Neurergus strauchii barani Oz, 1994

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Steinfartz S, Schutlschik G. 1997. Die Gattung Neurer-

gus. Reptilia (Munster) 8:43-48.

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prep.). Ranavirus infection in a group of wild-caught

Lake Urmia newts {Neurergus crocatus ) imported

into Gennany from Iraq.

Received: 14 June 2012

Accepted: 01 July 2012

Published: 22 September 2012

Serge Bogaerts has been fascinated by salamanders and newts since the age of seven. He studied biol-

ogy at Raboud University Nijmegen, specializing in herpetology and animal ecology. He works as advi-

sor on ecology and nature law for infrastructure projects for the Ministry of Infrastructure and Environ-

ment, while he continues herpetological studies as a hobby. Both through field work and captive care,

he is striving to leam more about the ecology and behavior of newts and salamanders, particularly those

of the Mediterranean and Middle East, and he publishes the results of these studies whenever possible.

Henry Janssen started out as a turtle enthusiast in the early 1970s. Gradually his interest shifted to

newts, in particular to the genus Paramesotriton. Over the years he was able to build up a significant

collection of Paramesotriton and other newt species, and has bred and raised at least one generation of

most of these. By keeping detailed records of his observations and through the systematic gathering of

data, he has acquired a thorough knowledge about the species he works with.

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Bogaerts et al.

Jennifer Macke has had a life-long fascination with animals. Her interest in newts began with an un-

dergraduate research project on limb regeneration, and she has kept and bred caudates ever since. She

is particularly interested in newts of the genera Cynops and Neurergus. She is currently employed as

a molecular biologist and also volunteers her time to manage the care of the reptiles, amphibians, and

invertebrates at a local nature center.

Gunter Schultschik started keeping newts and salamanders as a boy and still considers himself just an

enthusiast. After getting in contact with AG-Urodela of DGHT in 1989, his collection grew rapidly. J.

F. Schmidtler (Munich) was his teacher when he began to travel through Anatolia and the Middle East

searching for amphibians and reptiles. As a member of the Austrian Herpetological Society, he founded

“Urodela-Austria” a working group which has a meeting once a year, the “Molchlertag.” After some

publications together with W. Grosse, they started a project called “Captive Care Management” for

threatened species of tailed amphibians, which will be published soon in the DGHT series Mertensiella.

Kristina Ernst has been interested in all kinds of animals since she was a small child. Her fascination

for newts and salamanders started in 1 993 with her first newts of the genus Cynops. In 2000 she became

a member of AG-Urodela of the DGHT and discovered, and developed a special interest in the genus

Neurergus. Since then, she has focused on this genus and is responsible for the studbook of Neurergus

strauchii at AG-Urodela.

Francois Maillet has been keeping and breeding salamanders and newts as long as he can remember.

Together with Jean Raffaelli and Amaud Jamin, he forms the core of the French Urodela Group (FUG),

whose goals are to bring together knowledge and experience regarding captive bred animals, and to

keep stable long-term populations of many species of newts and salamanders in captivity.

Christoph Bork has been interested in amphibians since he was six years old. He especially loves

newts and salamanders, which he has kept seriously for at least 25 years now. He got his start with

Triturus species, and mainly keeps Neurergus species nowadays. As a hobby newt enthusiast he has

been a member of the AG Urodela for many years. Additionally he is fascinated by poison dart frogs.

Several of these species decorate his living room.

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Conservation, husbandry, and captive breeding of the Anatolia newt, Neurergus strauchii

Frank Pasmans has been fascinated by urodelans since he was a young boy, and he has kept and bred

several species. As a veterinarian, he is currently head of a research group that studies amphibian dis-

eases at Ghent University, Belgium.

Patrick (Pat) Wisniewski (1954-2008) was an all-

round natural historian and the longest serving cu-

rator of Martin Mere in Lancashire, one of the nine

UK Wildfowl & Wetland Trusts centres. He was

“the newt man’s newt man,” said to be ahead of

his time in amphibian husbandry. He kept and bred

a great range of amphibians, especially newts and

salamanders — mainly European and Asian species.

A vast collection of captive animals covered every

inch of several rooms and part of the garden. Pat

wrote the booklet “Newts of the British Isles” pub-

lished in 1989.

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ative Commons Attribution-NonCommercial-NoDerivs 3.0 Unported License, which permits unrestricted use for

non-commercial and education purposes only provided the original author and source are credited.

Amphibian & Reptile Conservation 6(4):30-35.

Ecology of Kurdistan newt ( Neurergus microspilotus :

Salamandridae): Population and conservation with an

appraisal of the potential impact of urbanization

1>2 Nasrullah Rastegar-Pouyani, 1 2 Mohsen Takesh, 1>2 Akbar Fattahi, 3 Marzieh Sadeghi, 3 Fatemeh

Khorshidi, and 4 Robert Browne

1 Department of Biology, Faculty of Science, Rail University, 6714967346 Kertnanshah, IRAN 2 Iranian Plateau Herpetology Research Group

(IPHRG), Faculty of Science, Razi University, 6714967346 Kermanshah, IRAN * Faculty of Chemistry, Razi University, Kertnanshah, Iran 4 Royal

Zoological Society of Antwerp, Koningin, Astridplein 26, 2018, Antwerp, BELGIUM

Abstract. — The Kurdistan newt, Neurergus microspilotus Nesterov, 1916, inhabits springs, ponds,

brooks, streams, and wet caves in the western Iranian Plateau in both Iran and Iraq. The Iranian

distribution of N. microspilotus is limited to Kurdistan and Kermanshah Provinces. Several major

populations of N. microspilotus are threatened by urban development. We gathered autecologi-

cal data of N. microspilotus and evaluated factors that may affect the distribution and abundance

of this species. We conducted visual surveys for N. microspilotus at twelve localities across the

north-western regions of Kermanshah Province from February to July 2012. The survey sites were

classified as undeveloped or developed based on their proximity to urban or rural landscapes,

and other anthropogenic disturbance and structures. We analyzed the effect of ecological factors,

including water pH and specific conductance, temperature, peak of mating behavior, and the time

of egg-laying. The daily air temperature of the study sites was provided by the weather bureau of

Kermanshah Province. We investigated the correlation between daily maximum air temperature and

N. microspilotus population density using Pearson Correlation Analysis, and analyzed the impact

of urbanization on specific conductance and pH of habitat water and numbers of N. microspilotus

according to Independent-Samples f-test. The densities of N. microspilotus across sites were posi-

tively correlated with increased water and daily maximum air temperatures. In addition, we found

that densities of N. microspilotus at undeveloped sites were significantly higher than those of de-

veloped sites, whereas no relationship was recorded between specific conductance and pH of the

water and urbanization.

Key words. Kurdistan newt, Neurergus microspilotus, ecology, conservation, urbanization

Citation: Rastegar-Pouyani N, Takesh M, Fattahi A, Sadeghi MS, Khorshidi F, Browne R. 2013. Ecology of Kurdistan newt (Neurergus microspilotus: Sal-

amandridae): Population and conservation with an appraisal of the potential impact of urbanization. Amphibian & Reptile Conservation 6(4):30-35(e58).

Introduction

Many species of amphibians globally have declined in

abundance and range over recent decades (Collins and

Storfer 2003; Stuart and Chanson 2004; Beebee and

Griffiths 2005) and 30% of species are now threatened

with extinction (IUCN 2010). Related causes of these de-

clines and extinctions are habitat loss and fragmentation,

unsustainable harvesting, environmental contaminants,

increasing UV radiation, climate change, introduced

predators, and emerging diseases (Young et al. 2001;

Collins and Storfer 2003; Baillie et al. 2004). Urbaniza-

tion is a substantial cause of habitat loss and fragmenta-

tion (McKinney 2002, 2006). Urbanization is a complex

process characterized by increasing in human popula-

tion density, which generates significant changes in the

chemical, physical, and ecological conditions of affected

Correspondence. Email: 1 nasrullah.r@gmail.com

areas, and specifically results in the creation of new as-

semblages of plants and animals, and possible alteration

of the types and frequency of disturbance regimes (Mc-

Donnell and Pickett 1993; Kinzig and Grove 2001).

Urbanization alters hydrology through water extrac-

tion, the construction of impervious surface and increased

runoff, increase sedimentation, and pollution of hydro-

logical systems (Paul and Meyer 2001; Miltner et al.

2004), and through modifying soils (Effland and Pouyat

1997). Urbanization may also result in an increase in in-

vasive plants and animals (Pickett et al. 2001; McKinney

2006), different climates between urban and surrounding

rural areas (Grimm et al. 2008). Urbanization is therefore

currently one of the most pervasive causes of natural eco-

system modification globally, and thus presents a major

threat to biodiversity conservation (Czech et al. 2000;

Miller and Hobbs 2002).

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Rastegar-Pouyani et al.

Previous investigations indicated that the distribution

of the Kurdistan newt, Neurergus microspilotus, is in the

mid-Zagros range at the bordering regions of Iran and

Iraq (Nesterov 1917; Schmidtler and Schmidtler 1975).

Najafimajd and Kaya (2010) reported the first observa-

tion of N. microspilotus in west-Azarbaijan, Iran, how-

ever, molecular studies were not conducted on these

specimens to confirm their claimed status. Major locali-

ties of N. microspilotus are found in both urban and rural

areas some of which are centers for tourism (Sharifi et

al. 2004; Rastegar-Pouyani et al. 2005; Rastegar-Pouyani

2006). In the present study, we investigated the relation-

ships between presence and density of N. microspilotus,

and the degree of urbanization, and analyzed factors that

may affect this relationship including autecological data

and water temperature.

Materials and methods

Study sites and survey techniques

The survey area is located in north-western regions of

Kermanshah Province, western Iran, and surveys were

conducted from February to July 2012. Twelve sites in-

cluding a range of ponds, pools, brooks, and streams were

selected for surveys. The selection of sites was based on

our previous knowledge of these sites providing a consis-

tent occurrence of N. microspilotus.

Sites investigated were Darian (35°08' N 46° 19' E),

Darre-Najjar (35°06' N 46°19' E), Deshe (35°04' N 46°16'

E), Dorisan (35°1E N 46°23' E), Hajij (35°09' N 46°19'

E), Kavat (34°53' N 46°3E E), Lashgargah (35°01' N

46°08' E), Nilan (35°09' N 46°12' E), Nodeshe (35°1E N

46° 14' E), Noseme (35W N 46°22' E), Qholani (34°54'

N 46°27' E), and Qhuri-Qhala (34°2E N 46°30' E) (See

Table 1).

We categorized study sites into two categories; 1)

Developed-sites placed at the center or vicinity of urban,

rural, or tourism areas, and 2) Undeveloped-sites remote

from urbanization with limited ecological change such

as grazing.

The counting of N. microspilotus in the Kavat and

Dorisan habitats begun on 08 March 2012 and, with

weekly intervals, ended on 05 July 2012. Neurergus mi-

crospilotus were surveyed and counted through stream

bank observation without substrate disturbance. The

peak of mating behavior was recorded as the maximum

amount of courting behavior, and the time of egg-laying

through the observation of eggs in the water for the first

time during the season.

Collection of habitat data

To assay the specific conductance and pH of water, wa-

ter-sampling was performed on a 50 ml water sample

from each site. A Jenway 3345 Ion Meter was used for

determination of conductivity measurements. The pH

of water was calculated via pH meter model Metrohm

827 pH lab equipped with a combined glass electrode,

calibrated against two standard buffer solutions at pH 4.0

and 7.0 and used for monitoring of the pH values. The

daily maximum air temperature of the study sites, over

the period of the study, was provided by the weather bu-

reau of Kermanshah Province (Table 3).

Statistical analysis

To statistically analyze the effect of urbanization on spe-

cific conductance and pH of water, and the population

density of N. microspilotus, we subjected the data to

Independent-Sample /-tests. To analyze the relationship

between daily maximum air temperature and increas-

ing populations of A. microspilotus subjected the data to

Table 1 . Study site names and coordinates (North, East), N. microspilotus numbers (no.), water specific conductance (SC; pS cm 1 ),

and pH, natural (normal font) or developed (italic font) sites, and threats.

Sites

Coordinates

No.

Threats from development

Kavat

34°53'N46°31'E

750

0.3

8.2

—

Qholani

34°54' N 46°27' E

0.4

7.8

—

Darre-Najjar

35°06'N46°19'E

0.4

7.6

—

Darian

35°08'N46°19'E

0.2

7.8

Fish aquaculture and gardening

Nilan

35°09'N46°12'E

0.3

7.6

Gardeners in this suburban development, clearing the bottom of the pools

of aquatic plants that provide shelter for eggs, larvae, juveniles, and adults

Hajij

35°09'N46°19'E

0.3

7.4

Dam-construction in the Sirvan River, ecotourism, gardening

Noseme

35°00' N 46°22' E

0.3

7.2

Habitat degradation or loss through irrigation and domestic water usage,

accumulation of rubbish in water, and home-construction in the village

Deshe

35°04'N46°16'E

0.3

7.3

Dorisan

35°01'N46°23'E

0.3

7.3

Nodeshe

35°11' N 46°14' E

0.3

7.5

Organic-pollution of water and gardening

Qhuri-Qhala

34°21' N 46°30' E

0.4

7.4

Major tourist destination. Accumulation of rubbish in the water and the ma-

nipulation of habitat through sanitation processes and cleaners in streams

Lashkargah

35°01' N 46°08' E

0.46

7.6

Many N. microspilotus are road fatalities

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Ecology of Neurergus microspilotus

Table 2. Statistical analysis of the effect of urbanization on the specific conductance and pH of water and the number of

N. microspilotus .

Variable

Developed habitats ( n = 9)

Mean ± SD

Undeveloped habitats ( n = 3)

Mean ± SD

p-value

Specific conductance

0.3 ± 0.1

0.48 ± 0.1

1.1

0.32

7.5 ± 0.2

7.9 ± 0.3

2.9

0.02

Number

20.1 ± 21.3

299.7 ± 393.9

2.4

0.04

Pearson Correlation Analysis using the program SPSS

(version 16 for Windows; SPSS Inc. Chicago, Illinois,

USA). Data were considered statistically different at P

<0.05.

Results and discussion

for the reproduction of N. microspilotus within the Ka-

vat and Dorisan habitats, as well as on Shahoo Mountain

(northwestern Kermanshah Province), gradually reaches

an optimum with the onset of increased moisture (from

melting snow and spring rain) and temperature, with a

peak in mid- June and early July (Fig. la, b).

Our results suggest that nine out of 12 localities of N.

microspilotus from the populations were lowered by ur-

banization. These localities are Darian, Deshe, Dorisan,

Hajij, Lashgargah, Nilan, Nodeshe, Noseme, and Qhuri-

Qhala.

The Independent-Samples /-test revealed that devel-

oped/undeveloped sites do not have any difference in

specific conductance (p = 0.31), but do in the water pH

and number of newts (p = 0.04). Bowles et al. (2006)

used specific conductance to investigate the effect of

urbanization on water of habitats in Eurvcea tonkawae,

but our results indicate that specific conductance could

not be used as a separator tool to measure the impact of

urbanization on N. microspilotus. The resulting data of

the specific conductance indicates that there is not much

overlap between developed (0.22 < X < 0.46) and un-

developed sites (0.27 < X < 0.44). Instead, the analysis

suggests that the pH is a better indicator (p = 0.02) of the

effects of urbanization on N. microspilotus (in our stud-

ied populations) (Table 2).

The resulting data on the counting of the newt in the

Kavat and Dorisan habitats, the temperature of the two

synoptic stations, dates of observations and statistical as-

sessment of correlation between maximum daily air tem-

perature, and the number of N. microspilotus are present-

ed in Table 3. The Pearson Correlation Analysis revealed

that there is a strong association between the temperature

and presence of individuals of two populations in Kavat

and Dorisan (/7-value = 0.919, r = 0.000; /7-value = 0.812,

r = 0.000, respectively).

According to the data, N. microspilotus adjusts its

transition from torpor, and presence in the environment

and mating behavior, at a time when food availability of

insects and other invertebrates is maximum and the thick-

ness of the forest canopy and leaves on the water surface

provides the maximum shelter from predators (Table

3; Fig. la, b). At this time a maximal cover of aquatic

vegetation provides the best environment for reproduc-

tive activities, the deposition of sperm, and egg attach-

ment. In March and early April, the vegetative cover of

the Kavat and Dorisan habitats is low. Habitat suitability

Acknowledgments. — We wish to thank the Mohamed

Ben Zayed Foundation, and the European Association of

Zoos and Aquaria for supporting of this project through

grants. Support was also provided by core funding from

the Royal Zoological Society of Antwerp. We also thank

the weather bureau of Kermanshah Province, especial-

ly Mr. Shaygan for providing weather data, the driver,

Sabzali Rasooli, who helped us very much during field

work in western Iran, and Mohammad Reza Ashrafi

Kooshk and Dariush Naderi for their help in preparation

of the manuscript.

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Rastegar-Pouyani et al

^1"

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«T)

0 —

3 O

■P o_

2 03

m 0

Q.~

E -Q

■S -

S «

re >

0 re

5 v-

s£>

■'t

iri

</>

0 -K

o re

c s

= J 2

3 re

o —

3 +-

2 2

0 !5

a. re

E ■=

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+* re

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s a

■* — numb ers of n ew t

-* — weather temperature

&.■

i—i

4 ■

Figure la, b. The graphs of weather temperature (red) and number of newts (blue) in the Kavat

(a) and Dorisan (b) habitats.

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Received: 22 October 2012

Accepted: 29 December 2012

Published: 14 March 2013

Nasrullah Rastegar-Pouyani earned his B.S. in zoology from Razi University Kermanshah, Iran, in 1986 and

his M.S. in zoology from Tehran University, Tehran, Iran, in 1991, where he studied herpetology with the aga-

mids as the central object. He started his Ph.D. in Gothenburg University, Sweden, in 1 994 under the advisement

I of Professor Goran Nilson and graduated in 1999, working on taxonomy and biogeography of Iranian Plateau

agamids, with Trapelus as the main objective. He is a professor and head of the biology department at Razi

University. His research interests include taxonomy and biogeography of the Iranian Plateau, the Middle East,

ar| d central Asian herpetofauna.

Mohsen Takesh earned his B.S. in animal biology from Urmia University, Urmia, Iran, in 2009 and his M.S.

in animal biosystematic from Razi University, Kermanshah, Iran, in 2012 under Professors Mozafar Sharifi and

Nasrullah Rastegar-Pouyani. His M.S. thesis was on ecology and distribution of Kurdistan newt, Neurergus

microspilotus , in its Iranian distribution range. His research interests include ecological, phylogeographical, and

phylogenetic investigations of amphibians and reptiles.

Akbar Fattahi earned his B.S. from Urmia University, Urmia, Iran, in 1993 and his M.S. in animal biosyste-

matic from Razi University, Kermanshah, Iran, in 2012 under the supervision of Professor Nasrullah Rastegar-

Pouyani. His M.S. thesis was on ecology and systematics of the Kurdistan newt, Neurergus microspilotus , in its

Iranian distribution range and the tree-frog, Hyla savignyi, in Kermanshah Province, western Iran. His research

interests include ecological and taxonomic investigations on amphibians and reptiles.

amphibian-reptile-conservation.org

034

March 2013 | Volume 6 | Number 4 | e58

Rastegar-Pouyani et al.

Marzieh Sadeghi earned her B.S. in applied chemistry from Razi University Kermanshah, Iran, in 2003 and

her M.S. in analytical chemistry from Shiraz University, Shiraz, Iran, in 2005, where she studied construction of

optical sensor for pH and metal ions under the advisement of Professor Afsaneh Safavi. She started her Ph.D. in

Razi University, Kermanshah, Iran, in 2005 under the advisement of Professor Mojtaba Shamsipur and gradu-

ated in 2010, working on optical and electrochemical sensor for metal ions and pharmaceutical compounds

as the main object. Her research interests include optical sensor and liquid phase microextraction, solid phase

extraction, and removal of toxic compound from aqueous environment using nanomaterial compound.

Fatemeh Khorshidi earned her B.S. in applied chemistry from Razi University Kermanshah, Iran, 2006 and her

M.S. in analytical chemistry from Razi University, Kermanshah, Iran, in 2012, where she studied the removal of

arsenic from aqueous environment using metallic nanocomposite under the advisement of Dr. Marzieh Sadeghi.

Her research interests include removal of toxic elements from aqueous environments, nano-drug and medical

nano technology.

Robert Browne is co-editor of the journal Amphibian and Reptile Conservation. He has a wide range of aca-

demic and practical experience in many research fields supporting herpetological conservation and environmen-

tal sustainability. Currently he works for “Sustainability America” www.SustainabilityAmerica.org (Belize).

amphibian-reptile-conservation.org

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March 2013 | Volume 6 | Number 4 | e58

ative Commons Attribution-NonConunercial-NoDerivs 3.0 Unported License, which permits unrestricted use for

non-commercial and education purposes only provided the original author and source are credited.

Amphibian & Reptile Conservation 6(4):36-41.

Rediscovery of the Lake Urmia newt, Neurergus crocatus

Cope, 1862 (Caudata: Salamandridae) in northwestern Iran

after 1 50 years

^Inaz Najafi-Majd and 2 Ugur Kaya

Ege University, Faculty of Science, Department of Biology’, Section of Zoology, Bornova, izmir/ 35100, TURKEY

Abstract . — We report on the rediscovery of the Lake Urmia newt, Neurergus crocatus in Iran, 150

years after its original description and last report by Cope 1862. The Lake Urmia newt is classified as

Vulnerable by the IUCN Red List of Threatened Species. Some specimens, both adult and larvae, of

N. crocatus were found in Iran during two field surveys near the Iran-lraq border (south west of West

Azerbaijan Province, surrounding the type locality “Urmia,” at 1786-1823 m above sea level [a.s.l.]

elevation). Water samples were taken from two breeding habitats, as preliminary data, and were ana-

lyzed for 13 chemical variables to determine the characteristics of water chemistry. The morphologi-

cal comparison of the new specimens with the original description and data from Schmidtler and

Schmidtler (1975) did not reveal any distinct morphological differences. Previous to our study there

was no information regarding the exact locality of N. crocatus and its population status in Iran. Our

confirmation of N. crocatus in northwestern Iran indicates that protection is needed if this species

is to persist in Iran. In addition, water chemistry analysis of the two new habitat records showed that

in this area N. crocatus inhabits two streams with good water quality.

Key words. Neurergus crocatus , rediscovery, conservation, Iran

Citation: Najafi-Majd E, Kaya U. 2013. Rediscovery of the Lake Urmia newt, Neurergus crocatus Cope, 1862 (Caudata: Salamandridae) in northwestern

Iran after 150 years. Amphibian & Reptile Conservation 6(4):36-41(e59).

Introduction

Newts of the genus Neurergus (Salamandridae) are con-

fined to Turkey, Iran, and Iraq. Neurergus was originally

categorized as a member of the family Salamandridae and

the subfamily Tritoninae, subsequently it was changed

to Pleurodelinae (Cope, 1862). Four species of Neurer-

gus have been described (Schmidtler 1975; Leviton et

al. 1992; Sparreboom et al. 2000): Neurergus crocatus

Cope, 1862 from northwest of Iran, northern Iraq, and

southeast of Turkey; Neurergus strauchii (Steindacliner

1887) from the western side of Van Lake to Malatya in

eastern (Anatolian) Turkey; Neurergus microspilotus

(Nesterov 1916) from the west and northwest of Iran and

east of Iraq; and Neurergus kaiseri Schmidt 1952 from

the surroundings of Shah-Bazan of Luristan Province,

Iran. All known species of Neurergus can easily be dis-

tinguished by their morphological characters (Schmidtler

and Schmidtler 1970, 1975; Schmidtler 1994; Najafimajd

and Kaya 2010; Schneider and Schneider 2011). At pres-

ent, the taxonomic relations of the closely related taxa N.

microspilotus and A. derjugini (Nesterov 1916) from the

Iraq and Iran borders are still debatable (Schneider and

Schneider 2011).

The genus Neurergus is represented by three species

in Iran, N. crocatus Cope, 1862, N. microspilotus (Nest-

erov 1916), and N. kaiseri Schmidt, 1952 (Balouch and

Kami 1995). According to IUCN, N. crocatus has one of

the largest distribution ranges among all Neurergus spe-

cies; though there is almost no data about its biology and

exact distribution (Steinfartz et al. 2008). As stated by

Sparreboom (2009) this insufficient data may be ascribed

primarily to geographic inaccessibility, as well as long

term ethnic tensions, and a long and continuing history

of military conflicts. Neurergus crocatus has been known

from several localities in Turkey since 1986 (Baran and

Oz 1986; Baran and Atatur 1997; Ozdemir et al. 2009).

This striking coloration of these N. crocatus attracted the

attention of local people and non-herpetologists subse-

quently misidentified them as N. strauchii (Kemal 2008).

Very recently in 2010 a new locality for N. crocatus, in-

cluding two neighboring streams close to the §emdinli,

Turkey, was published (Schneider and Schneider 2010).

Neurergus crocatus has been reported from eight lo-

calities in Iraq: Agrah (Schmidt 1939), Shiwolak and

Tajeka villages in the northeastern (Khalaf 1961; Nader

1969), and five recent localities from Barzan, Girbish,

Roste, Smilan, and Nawanda in 2010 (Schneider and

Schneider 2011).

Correspondence. Email: 2 ugurkaya@ege. edu.tr (corresponding author); 1 elnaz.najafi.majd@gmail.com

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April 2013 | Volume 6 | Number 4 | e59

Najafi-Majd and Kaya

There is limited information regarding the exact local-

ity and the distribution of N. crocatus and its population

status in Iran. Only one historic record by Cope (1862) is

noted from northwestern Iran but the exact type locality

is unknown, however Fowler and Dunn (1917) reported

the type locality as “Ooremiah, Persia.”

Within the Salamandridae, newts of the genus Neu-

rergus are basically known as stream inhabiting species

that leave streams during dry periods or during winter

(Schmidtler and Schmidtler 1970, 1975; Schmidtler

1994). The Lake Urmia newt, N. crocatus is quite close-

ly related in an ecological aspect to Calotriton species

which have similar habitats (Steinfartz et al. 2002). Neu-

rergus crocatus is a montane species and lives in cool

and well-oxygenated streams (Ozeti and Yilmaz 1994;

Baran and Atatiir 1998), where it breeds. There is no

published information about the terrestrial component of

their life history. It is presumed that the adults hibernate

under rocks and other cover during the winter (Papen-

fuss et al. 2009). There is almost no information on its

life cycle, but eggs and larvae of different lengths were

observed at the end of May and June. The seasonality of

the breeding season is dependent upon elevation (Ozeti

and Yilmaz 1994).

According to the IUCN, there is a continuing decline

in the extent and quality of the habitat of N. crocatus in

Turkey, Iran, and Iraq (Papenfuss et al. 2009). However,

there is no published information about the size and rate

of this decline. Neurergus crocatus is categorized as a

Vulnerable species [VU B2ab (iii)] in the IUCN Red List

of Threatened Animals. Despite the significance of its

conservation, nothing is known about the life history of

N. crocatus , e.g., individual growth, longevity, and other

demographic parameters, or its ecology including critical

habitat components such as water quality and tempera-

ture, breeding, oviposition, or hibernation sites.

One hundred and fifty years after the original descrip-

tion of N. crocatus (Cope 1 862) we verify the existence

of N. crocatus in northwest Iran. We also provide infor-

mation on the characteristics of water chemistry in the

aquatic breeding habitat of N. crocatus.

Materials and methods

To assess the presence of N. crocatus in north-west Iran,

we conducted two surveys during the field seasons of

2009 and 2010 of the northern Zagros Mountains in the

west of Lake Urmia, from Sero (the area between Lake

Table 1 . Morphological characteristics of the closely related species Neurergus microspilotus and N. crocatus (Schmidtler and

Schmidtler 1975) in comparison with our specimens from Oshnaviyeh.

Characteristics

Neurergus crocatus

Neurergus microspilotus

Specimens from Oshnayiyeh

Adult

1. Maximum total length

of $/c?

16 / 18 cm

15 / 17 cm

16.8 cm $ (Mean)

2. The form of cloacae in

mating season in $

Lips approximately 1-2 mm

protruding

Not sharp conical, lips 3 mm

protruding

Lips approximately 1-2 mm pro-

truding

3. Design of backside

(spots small 0.2 mm, large

0.4 mm)

Large and small yellow spots

Small yellow spots

Large and small yellow spots

4. Design of throat

Unicolored orange

Orange, mostly with black spots

Unicolored orange

5.Design of belly

Unicolored yellow to reddish

orange

Lateral black coloration con-

fines orange middle parts

Unicolored yellow to reddish

orange

6. Design of underside of

extremities

Unicolored orange

Orange, mostly black spotted

Unicolored orange

7. Design of tail laterals

Large yellow spots

Small yellow spots

Large yellow spots

Larvae

8. Total length

35-70 mm

58 mm

9. Relation dorsal fin-

1 . 0 - 1.1

Protrudes from the back center

significantly

0.7-0. 9

1 . 0 - 1. 1

Protrudes from the back center

significantly

length / interaxial length

Protrudes from the back center

10. Dorsal design of older

larvae (about 50 mm total

length)

Bright spots irregularly and big;

partly fussed

Clearly long bright stains

toward two lines along center

of the back

Big, irregular bright spots; partly

fussed

1 1 . Design of belly of older

larvae (about 50 mm total

length)

Almost unicolored bright

Tow imperfect dark spot lines

along edges of belly

Almost unicolored bright

12. Design of tail sides

More or less clearly dark pig-

mented

Clearly blackish brown

"clouded"

More or less clearly dark pigmented

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Rediscovery of the Lake Urmia newt

Urmia and Iran-Turkey border) and continued the search

to the south up to Piranshahr, in the West Azerbaijan

Province near the Iran-Iraq border (between 37° 42’ 36”

and 36° 40’ 33” latitudes).

We investigated all potential and accessible habitats

of N. crocatus in this area, including streams, springs,

and ponds. Searches were undertaken between 9.30 am

and 6.30 pm. Local people were interviewed in order to

obtain more information on N. crocatus.

Geographic positions of study sites were recorded

with a GPS receiver (Garmin eTrex® 30). Total lengths

of adult females were measured with calipers in the field

and given in millimeters (mm). Collected specimens

were compared morphologically with the description

given in Cope (1863) and Schmidtler and Schmidtler’s

(1975) table (Table 1).

Water samples were collected from the breeding habi-

tat to determine parameters of the salamander’s breeding

water conditions. Water conductivity, pH, dissolved oxy-

gen (DO), and salinity were measured in the field using a

Hach Portable pH/conductivity/dissolved oxygen meter,

and water temperature was measured with a thermome-

ter. Some water chemistry parameters such as iron, man-

ganese, chloride, ammonium, sulfide, potassium, nitrate,

ammonia, and hardness (calcium and magnesium) were

measured in the laboratory using a DR 2800 VIS Spec-

trophotometer, following the manufacturer’s procedures.

Results and discussion

There was no evidence of the species hi the 2009 field

survey but in 2010, on June 4 th , seven adult specimens

(?) were discovered and collected from a Margo Ziyarat

Region spring near Oshnaviye, at the border in the west

of West Azerbaijan Province, north-Zagros Mountains.

In the last conducted survey of the same locality on July

30, 2010 morning, two adults in the spring and eight lar-

vae were found in a small stream and six larvae were

collected from the stream; elevation of the location was

1786-1823 ma.s.l.

Neurergus crocatus was previously known from 11

locations in Iran, Iraq, and Turkey (Cope 1863; Schmidt

1939; Khalaf 1961; Nader 1969; Baran and Oz 1986;

Schneider and Schneider 2010, 2011). This species is

present in the vicinity of Beytu§§ebap and Semdinli,

south-east Anatolia, Turkey and in eight localities in the

northeastern region of northern Iraq. For the Iranian re-

cord, Cope (1862) did not designate the exact type lo-

cality of N. crocatus ; however subsequently Flower and

Dunn (1917) determined the type locality as “Ooremi-

ah, Persia” which corresponds to Lake Urmia. Freytag

(1956: pi. 4) has at first depicted the type specimen with

the labels. We discovered N. crocatus in the west of West

Azerbaijan Province near the Iran-Iraq border in a natural

spring and a small stream. The investigated locality and

previously known localities are shown in Fig. 1.

In the north west of Iran in the Mergo Ziyarat region

near Oshnaviyeh, we found a total of 17 newts (nine

adult females and eight larvae); adults from a spring and

larvae from a stream. Adult specimens were discovered

in Arabe Spring (37° 2.59’ N; 44° 56.72’ E), west of Os-

hnaviyeh. Six larvae were collected from Gurgu Stream

(37° 2.78’ N, 44° 56.80’ E), approximately 100 m north

of the spring at 1786-1799 m a.s.l. (Fig 2: A, B). Females

were hiding between vegetation in the spring and larvae

were found in streams with fast running water, in a small

puddle behind stones.

Morphological characters

Collected specimens were compared morphologically as

well as in coloration with the description of Cope 1862

and Table 1 in Schmidtler and Schmidtler (1975). Neu-

rergus crocatus is characterized and readily identified by

yellowish color spots on their flattened black body. Dor-

sal blotches are yellow and small in midline and larger

with light yellow coloration in the lateral position; ven-

tral surface orange-red in males, yellowish in females;

limbs overlap when laid against the body, broadly. Males

have white colored spots along the tail (Schneider and

Schneider 2010). Tail fins on dorsal and ventral sides de-

veloped; dorsal tail fin a little higher, especially in the

breeding season (Fig 2: C, D).

Our specimens represent the typical characteristics of

N. crocatus given in the literature (Table 1 ; Schmidtler

and Schmidtler 1975). The species dorsal coloration

varies from dark brown to black with numerous yellow

round or elongated spots. The yellow spots were a little

smaller than in the type specimen (Freytag 1956: pi. 4).

The coloration of trunk and tail venter is yellowish or-

ange with infrequent small black spots overlaying the

abdomen.

Ecological habitat characteristics

Generally, salamanders are found only in or near running

water such as mountain brooks and streams and their sur-

vival and distribution can be strongly limited by water

quality (Saynn et al. 2009). Moreover, salamanders have

highly permeable skin and their larvae may be particu-

larly susceptible to water quality parameters (Duellman

and Trueb 1994). Some chemicals such as nitrates and

chlorides could influence salamander distribution, abun-

dance, and the selection of breeding sites (Odum and

Zippel 2008).

Neurergus crocatus is a montane species that lives

and breeds in cool and continuously flowing streams

and springs in hillsides and mountainous areas. Habitat

substrate is composed of small stones and sands. Typical

of the environment of N. crocatus are Water cress (Nas-

turtium officinale), Oregano ( Origanum vulgare), and

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Najafi-Majd and Kaya

Figure 1. Anew locality, Oshnaviyeh (11) and other known localities of Neurergus crocatus : 1) Beytii^ebap, 2) Semdinli, 3) Agrah,

4) Shiwolak, 5) Tajeka, 6) Barzan, 7) Girbish, 8) Roste, 9) Smilan, 10) Nawanda. The hatched part shows our studied area, which

also covers the unknown exact location of Cope’s original “terra typica.”

Figure 2. A) Arabe Spring. B) Gurgu Stream. C and D) Neurergus crocatus adult female.

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Rediscovery of the Lake Urmia newt

Table 2. Values of some water chemistry variables in breeding habitats of Neurergus croccitus.

Habitat

TEM

CON

SAL

NO,

NH,

Hardness

(C°)

mg/I

Ms/cm

mg/I

mg/l

mg/i

Mg(mg/I)

Ca (mg/l)

Arabeh

7.69

6.78

228

0.11

0.03

0.2

0.9

0.7

1.2

0.01

2.43

0.01

Gurgu

8.45

7.64

301

0.14

0.00

0.2

0.9

0.5

1.2

0.02

2.00

0.13

Stinging nettle ( Urticci dioica ). According to Baran and

Atatiir (1998) N. crocatus spend the winter months on

land under stones or in burrows.

Analysis results of some water chemistry parameters

in breeding habitats such as iron, manganese, chloride,

potassium, nitrate, ammonia, and hardness (calcium and

magnesium) are given in Table 2.

Mean values of some water chemistry parameters of

breeding habitats was found to be as follows: Fe = 0.015

mg/1, Mn = 0.2 mg/1, Cl- = 0.9 mg/1, K = 0.6 mg/L, NCk =

1.2 mg/L, NFL, = 0.015 mg/L, hardness Ca = 0.07 mg/L,

and hardness Mg = 2.215 mg/L. Therefore, in these in-

habited waters toxic parameters (chloride, nitrate, and

ammonia), hardness (Mg and Ca), dissolved oxygen, and

pH are all in acceptable range (Odum and Zippel 2008).

Amphibians, especially salamanders, are excellent

indicators of local conditions because they have perme-

able skins and fairly limited home ranges (Blaustein and

Wake 1995). After obtaining similar information from

known breeding habitats and comparing these with habi-

tats that are not used for breeding, it will be possible to

assess the water quality requirements for breeding of N.

crocatus. This information can be combined with infor-

mation of other habitat variables to assess the broader

habitat requirements of N. crocatus.

Threats and conservation of N. crocatus

Currently, N. crocatus is considered Vulnerable by the

IUCN Red List due to its restricted range and potential

habitat destruction. Neurergus crocatus has not been ob-

served since its original description from Iran by Cope

in 1862. Our new record verifies its existence after 150

years from its original description and adds to the broad-

er distributional knowledge of the species. The species

is susceptible to habitat change, habitat loses, pollution,

drought, and over harvesting (Papenfuss et al. 2009), but

these factors have not been determined.

There is a continuing decline in the extent and quality

of its habitat. The distribution of this species in Turkey

is expected to undergo significant change due to various

human activities such as the construction of several dams

within the range of N. crocatus over the next 10 years

(Papenfuss et al. 2009). During summer and fall over

grazing and pollution of streams by sheep and goats dam-

age the habitat of N. crocatus. Some N. crocatus were

reported killed by local people that use these springs as

drinking water resource, as they think these newts are

poisonous.

To assure the sustainable management of N. crocatus

it is imperative to assess its habitat needs and conser-

vation status over its range and distribution surveys. Of

particular importance are how aquatic habitat variables

influence the choice and success of breeding sites.

Acknowledgments. — This study was a part of the first

author’s Ph.D. thesis. We want to thank Jahanbakhsh

Najafi-Majd who companies us in all field studies. This

work was supported by Ege University (BAP, Project

No. 2012/FEN/004).

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phibians and reptiles). Republic of Turkey, Ministry

of Environment, Ankara, Turkey 16 (214 p.).

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crocatus and Neurergus strauchii in Southeast Ana-

tolia. Zoology in the Middle East (Heidelberg) 1:96-

104.

Biricik M. 2009. The re-determination of the Neurergus

(Salamandridae, Caudata) specimens recently record-

ed in $irvan. Cesa News (Centre for Entomological

Studies, Ankara) 46(1 901): 1-5, 6-10.

Blaustein AR, Wake DB. 1995. The puzzle of declin-

ing amphibian populations. Scientific American

272(4):52-57.

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World. Proceedings of the Academy of Natural Sci-

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can Museum of Natural History, New York, New

York, USA. [Online]. Available (electronic database):

http://research.amnh.org/vz/herpetology/amphibia/

[Accessed: 31 January 2011].

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(Baghdad) 4:3-12.

Najafimajd E, Kaya U. 2010. A newly found locality

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Approach to an essential environmental parameter. In-

ternational Zoo Yearbook 42:40-52.

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ani N, Kuzmin S, Anderson S, Eken G, KiliQ T, Gem

E, Kaya U. 2009. Neurergus crocatus. In: IUCN Red

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2012 ].

Saynn F, Ba§kale E, Tarkhnishvili D, Kaya U. 2009.

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tats of the Caucasian salamander, Mertensiella cauca-

sica in the Western Lesser Caucasus. Comptes Rendus

Biologies 332:464-469.

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western Asia. Field Museum of Natural History, Zoo-

logical Series 24:49-92.

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17:193-198.

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Schneider C, Schneider W. 2010. Fieldnotes on the ecol-

ogy and distribution of Neurergus crocatus COPE,

1862 and Neurergus strauchii strauchii (STEIN-

DACHNER, 1887) in Turkey. Herpetozoa (Wien)

23(l/2):59-69.

Schneider C, Schneider W. 2011. Die Bergbachmolche

der Gattung Neurergus im Irak (Caudata: Salamandri-

dae). Herpetozoa (Wien) 23(3/4):3-20

Sharifi M, Assadian S. 2004. Distribution and conserva-

tion status of Neurergus microspilotus (Caudata: Sala-

mandridae) in western Iran. Asiatic Herpetologica!

Research 10:224-229.

Sparreboom M, Steinfartz S, Schultschik G. 2000. Court-

ship behavior of Neurergus (Caudata: Salamandri-

dae). Amphibia-Reptilia (Leiden) 21(1): 1-11.

Steinfartz S, Hwang UW, Tautz D, Oz M, Veith M.

2002. Molecular phylogeny of the salamandrid ge-

nus Neurergus : evidence for an intrageneric switch

of reproductive biology. Amphibia-Reptilia (Leiden)

23(4):4 19-431.

Rastegar-Pouyani N. 2006. Conservation and distribu-

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dridae) in Zagros Mountains, Kermanshah Province,

western Iran. 13th Congress of the Societas Europaea

Herpetologica. 115-116.

Received: 19 October 2012

Accepted: 26 December 2012

Published: 05 April 2013

Elnaz Najafi-Majd is originally from the Islamic Republic of Iran. She is currently a Ph.D. student at the Zo-

ology Section, Biology Department at Ege University in Turkey. She focuses her studies on the conservation,

ecology, and distribution of the Lake Urmia newt (Azerbayjan newt; Neurergus crocatus) and the Kurdistan

newt ( Neurergus microspilotus).

Ugur Kaya is professor at Ege University and curator of the zoology department Ege University (ZDEU) col-

lection. His main research fields are taxonomy, ecology, and bioacoustics behavior of amphibians. Recently, his

main research interests have focused on the conservation and ecology of amphibians. To help protect amphib-

ians species, he monitors various endangered populations and also uses bioacoustics to monitor other anuran

populations.

amphibian-reptile-conservation.org

041

April 2013 | Volume 6 | Number 4 | e59

Commons Attribution-NonCommercial-NoDerivs 3.0 Unported License, which permits unrestricted use for non-

commercial and education purposes only provided the original author and source are credited.

Amphibian and Reptile Conservation 6(4): 42-48.

New localities of the Kurdistan newt Neurergus

microspilotus and Lake Urmia newt Neurergus crocatus

(Caudata: Salamandridae) in Iraq

^mar Fadhil Al-Sheikhly, 2 lyad A. Nader, 3 Nasrullah Rastegar-Pouyani, and 4 Robert K. Browne

1 Omar Fadhil Al-Sheikhly, Department of Biology’ - University of Baghdad, IRAQ 2 P.O. Box 2491, Riyadh, SAUDI ARABIA D

Faculty of Science, Razi University, 67 14967346 Kermanshah, IRAN 4 Royal Zoological Society of Antwerp, Antwerp, BELGU

for Sarteneja, BELIZE

Ipf Biolog y,

inability

Abstract. — Little is known about the distribution and current conservationftatul^rfthe two M pe-

des of mountain dwelling newts of the genus Neurergus found in the Zacu4s Mounn^in nopnern

and northeastern Iraq: the Critically Endangered Kurdistan newt Neurerc s micrr oilotu (Nesterov

1916), and the vulnerable Lake Urmia newt Neurergus crocatus (Cop^u62)^Surveys irvlrie Kurd-

istan region of northeastern Iraq from 2007 to 2012 resulted in the liscc rj Jf N. m^ospilotus at

seven new localities distributed in the Zagros Mountain of Sulayjj^miya Pr^whpe. "Hie new locations

provide a major range extension of N. microspilotus. In additipn, tour new I^^M^ of N. crocatus

were located between 2007 and 2013. In addition to Neurergus ne^keurveys, imerviews with local

people were also conducted through the use of photographs. Severnkought during recent years

as well as anthropogenic habitat destruction and pollwc^rcive been considered as main threats to

the survival of both species in northern Iraq. Here twaescribe ngw geographical distributions and

the conservation status of both Neurergus species Bund in Iraq:

Key words. Kurdistan newt, Lake Uremia newt, Nmner gus micl

tan region, Iraq

Iptus^xeu rergus crocatus , salamanders, Kurdis-

Citation: Al-Sheikhly OF, Nader IA, Rastegar-Pouyani N, Browne RK. ^13.

newt Neurergus crocatus (Caudata: Salamandridae) if^^^Amphibil

lo c a rngp of the Kurdistan newt Neurergus microspilotus and Lake Urmia

Reptile Conservation 6(4): 42-48 (e68).

Introduction

The Kurdistan newts we sun

description by Nesterov ( ]

triton derjugini and R..

ons, Neurergus d. clerjTtgini (1

;d cor^Bfided to then

under the^knes Rhithro-

(crospilotu^mhQSQ tax-

ov 1916) and N. d.

microspilotus (NjBProv 1916), ar^™rently considered

a single speci^Pyn. Nm rergus mi^^pilotus [Nester-

ov 1916]) a^^vere ^^^recorded in Iraq by Schneider

and Schneide^k&ll), in the d^e vicinity of their type

1 ocaltfBB^I ram^Ee sur^pFmade by Schneider and

Sd^lider^k 11) irn^ysBmstan region of northern Iraq

_reportecWe Critically Endangered (IUCN

icrospilotus from seven localities

situa|Bcrm the northeastern mountains along the Iraq-

Iran bnkr. Leviton et al. (1992) described the range of

the Vuln^^le (IUCN Red List 2013) Lake Urmia newt

(TV crocatus ; Cope 1862) from northeastern Iraq, eastern

Turkey, northwestern Iran, and the Zagros Mountains of

Luristan.

Neurergus crocatus was found in Iraq by Allouse

(1955) and Khalaf (1959), with a subsequent review of

the range and distribution of N crocatus in Iraq by Nader

(1969). Al-Adhami and Hameed (1988) carried out a

comprehensive study on the histology of the TV. c. cro-

catus (Schmidt 1939) combined with description of the

sampling locations. Mahdi and George (1969) listed both

TV. microspilotus and TV. crocatus in the herpetofauna of

Iraq without providing their range or distribution. Both

species were shown to have a restricted range in Iraq

and to be allopatric (Najafimajd and Kaya 2010). From

2007 to 2013 we conducted intensive field work to de-

termine the range, distribution, and conservation status

of Neurergus newts in the Kurdistan region of northern

Iraq. Here we describe a new geographical distribution

for both species in Iraq and assesses their conservation

status.

Material and Methods

We surveyed suitable habitats from 2006 to 2012 for Neu-

rergus in the three Iraqi provinces of Kurdistan region in

Northern Iraq (Sulaymaniyah, Erbil, and Duhok provinc-

es; Table 1); additional field observations were made dur-

ing a short survey in 2013. In mountainous landscapes

(elevation of ca. 1200-1 600 m) consisting of fresh water

springs, streams, ponds, and waterfalls, we conducted

surveys in order to locate Neurergus eggs, larvae, and

Correspondence. Email: 1 alsheikhlyomar@gmail.com (corresponding author).

amphibian-reptile-conservation.org

042

July 201 3 | Volume 6 | Number 4 | e68

Al-Sheikhly et al.

Barzan

Smilan A (

Nawanda A

Shiwalok l

Halsho o

Awdalan JJ

Sulav

Ashawa

Duhok

Iran

Smaquli Area

< t « i

Erbil

N. microspilotus (2007-2013)

0 N. crocatus (2007-2013)

/ N. microspilotus Schneider & Schneider (2011)

A* crocatus Schneider & Schneider V 1111

V’^Sulaymaniyah

Ahmad AwaX

Sargate

Fig. 1 . Google Earth map of northern ^^LtKurdi

2013 for Neurergns microspilotus^^

sll^Vs new localities we discovered during our surveys from 2007 to

scribed by Schneider and Schneider (2011).

adults. Adults and larvaey^re photogra^^toi and some

collected for morphoh^^u^kmnination; e^wfially A.

crocatus , with focu^olrthe dimfc^es between the col-

oration pattern A. derjugin^^dcrospilotus taxon

and those of N^^catus Canon E^^Eanon EOS 40D

camera bod^EquipP^P^ith Canon EF 75-300 mm (f

4-5.6) and cSfc^^Ro-400jgjpi (f 4) lens was used to

take onl^t to con»n field identifications. We

in eir^M^a^^roof Hiking GPS device to

>ns (longl^e, latitude, and elevation). Lo-

dewed and shown photographs in

orcn^^further identify locations where Neurergus spp.

have observed. An IUCN threat assessment score

was then^pculated to identify the main threats to both

Neurergus spp.

Results

Kurdistan newt (Neurergus microspilotus)

Neurergus microspilotus is mainly found at an eleva-

tion of about 1200-1600 m in the fresh water springs,

streams, ponds, and waterfalls of the Zagros Mountain

Forest Steppe Ecoregion in northeastern Iraq. These

water bodies are primarily found on hillsides or in deep

wooded valleys. The 2012 surveys located populations

of A. microspilotus (18 individuals: 12 males; 6 females;

442 larvae) at seven new locations along the Iraq-Iran

northern border (Table 1, Fig. 1). The previously recog-

nized populations of N microspilotus in Iraq are mainly

restricted to the mountains of northeastern districts of

Sulaymaniyah province. We found six new localities for

N microspilotus in the Halabja and Pshdar districts of

Sulaymaniyah province.

On 10 July 2007 an adult male N microspilotus was

found in a shallow mountain pond with a maximum

depth of 7.3 cm. The pond (elevation 1307 m) branched

from a running stream within a valley near Isawa village,

Mawat Mountain, Sharbazher district (to the north of Su-

laymaniyah City). Furthermore, additional new localities

for N microspilotus were discovered during extensive

field surveys in northern Iraq (in Iraqi Kurdistan) per-

formed during May and June 2012. At the Isawa site on

13 May 2012 we failed to locate any adult A. microspilo-

tus but found hundreds of eggs and larvae in early meta-

morphosis stages. We also surveyed many suitable habi-

tats in the Pshdar district on 15 May 2012 which resulted

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July 201 3 | Volume 6 | Number 4 | e68

New localities of the Kurdistan and Lake Urmia newts

Table 1. List of the New localities for N. microspilotus and N. crocatus in Northern Iraq (Kurdistan Region); M = male; F =female;

L =larva; *= unknown count.

Province

District

Site

Coordinates

Neurergus species

Sulaymaniya Sharbazher Mawat - Isawa village

Sulaymaniya Halabja Sargate

Sulaymaniya Halabja Ahmad Awa Area

Sulaymaniya Halabja Byara

Sulaymaniya Pshdar Qara and Abubakra Area

Sulaymaniya Pshdar Halsho

Sulaymaniya Pshdar Hero

N35°56'E45°23'

N35°17'E46° 6'

N35°18'E46° 5'

N35°13'E46° 7

N 36°24' E 45° 3'

N36°12'E45°16'

N 36° 7E45°17

microspilotus

Total

Erbil

Shaqlawa

Dob Smaquli Area

N36°21'E44°19'

crocatus

Erbil

Choman

Grtk

N 36°46’ E 44°52'

crocatus

Duhok

Duhok Area

Ashawa - Sarsank

N37°0'E43°17'

crocatA

Duhok

Amedi

Sulav

N 37° 5’ E 43°27'

cv^mtus

Total

in three new locations for N. microspilotus. Adult males

and females were located in a small gravel pool branch-

ing from a running mountain stream at elevation ca. 1309

m in the Hero area (to the southeast of the Qaladza town-

ship). Searches along the edge of the pool resulted in

identifying 17 larvae in different metamorphosis stages.

Both adults and larvae were carefully examined andjaho

tographed (Figs. 2a and b).

We located a breeding site for N. microspilotus

elevation of ca.1342 m in a mountain poncHo the

of Hero in the Halsho area to the nordB^^BQalad'

(ca. 10 km). A total of 23 larvae wem^Rind buBo

were found (Fig. 3a). On 9 Jun^E012 t

AbubakrJBfeas ^Bkyisited. ATfbr interviewing many

Wak wp wprp able^klocate adult males and females

w^n ar vae m cimerent metamorphic stages in a

all mountainstream at an elevation of ca. 1300 m in

Qara mounBn (Fig. 3b). In June 2012, our surveys

eurergus Bre extended throughout suitable habi-

tatS^^neHjBja district. In addition to the Schneider

Scnneiaier (2011) sites, we located three new locali-

r . microspilotus in Halabja.

dult male along with 3 1 larvae were found in a

mountain pond (elevation ca. 1400 m) in Ahmad Awa on

4 June 2012. Additionally, 11 individuals (seven males

and four females) with 208 larvae in early metamorphic

* M

V, >*l’

Figs. 2a and 2b. Neurergus microspilotus (a): adult male; (b): larva, Hero of Pshdar district. Photographs by Omar Al-Sheikhly.

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July 201 3 | Volume 6 | Number 4 | e68

Al-Sheikhly et al.

stages were found in Byara (ca. 12 km) to the southeast

of Ahmad Awa and near the Schneider and Schneider

(2011) sites in Tawale and Balkha (Fig.l). On the 5 June

2012, through interviews with local people, an adult

male was located in a mountain stream at an elevation of

ca.1254 m in Sargate area in Halabja (Table 1).

Lake Uremia newt (Neurergus crocatus)

Neurergus crocatus thrives in any suitable aquatic habitat

found at an elevation of ca. 1200-1500 m in the north-

western parts of the Zagros Mountain Ecoregion in

northern Iraq. In addition to the Schneider and Schnei-

der (2011) N crocatus localities, our 2012-2013 surveys

resulted in four new localities for N crocatus within the

Erbil and Duhok provinces. Four males and two females

were found (Table 1). However, it appears that there are

many potential areas of suitable habitat for N crocatus in

northern Iraq still to be discovered. Four new localities

(two in Erbil and two in Duhok) for N. crocatus were

located during 2007 field surveys, and during a short visit

to the Duhok area in 2013 (Fig.l).

In the Erbil Province two new localities were located.

On 17 August 2007 an adult male and female were found

in a mountain stream at elevation of ca. 1400 m in the

Grtk Mountains in the Choman district of the Erbil Prov-

ince (c. 15 km), close to the Iraq-Iran border (Fig. 4). On

25 August 2007 an adult male was found at elevation of

ca. 1200 m in a mountain stream in Doli Smaquli area

of Shaqlawa district in Erbil. On 1 September 2007 an

adult male was located at the Sulav area i^Aniedi district

at elevation of ca. 1400-1500 m. OnJ^^^B®Q13 and

during a short visit to the Ashawa S arsank^^erfal 1

an adult male and female was found at an elevatio®f ca.

1206 m (Table 1).

Discussion

There is a

newts in

and scatte'

tat

of info

Ferning Neurergus

newtSMF^e a restricted range

|on mainly confined to the habi-

ivtou^un Forest Steep Ecoregion. Our

surveys suggest that Neurergus newts are

/tS

Figs. 3a and 3b. Neurergus microspilotus (a): juvenile at Halsho of Pshdar district; (b): Adult male (below) and female (above) in

Qara mountain. Photographs by Omar Al-Sheikhly.

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045

July 201 3 | Volume 6 | Number 4 | e68

New localities of the Kurdistan and Lake Urmia newts

Fig. 4. Male (right) and female

Sheikhly.

still thriving in suitatfl^nabita^m tne nortnwn moun-

tains of Iraq, witl^^ations con^fctated mainly along

the border witl^Rm. Our surveys abided the known

range of N. j^^ospilo^fthat included seven new loca-

tions in the nkmtau^^n northeastern Iraq. In addition,

four neaJocalmBff^ N. crocjrs were discovered in this

in mountain stream at Grtk of Choman district in Erbil. Photograph by Omar Al-

tere are two allopatric species

Iraq with the populations of N.

wim^^motus t)emg*restricted mainly to the eastern and

northeastern mountains of Sulaymaniya Province with

notable o^centrations of populations in the Halabja and

Pshdar dismcts. Halabja and Pshdar had six new loca-

tions of the N. microspilotus with high number of eggs

and larvae. The Penjwin district also appears to pro-

vide many habitats for N. microspilotus. Schneider and

Schneider (2011) reported N. microspilotus from three

different localities in Penjwin, however, we believe that

further surveys in Pshdar and Penjwin districts will re-

veal new localities for N. microspilotus. The protection

of known localities in these three districts is urgently

needed to conserve N. microspilotus in Iraq.

Populations of N. crocatus in Iraq are mainly re-

stricted to the mountains and elevated grounds of Erbil

and Duhok provinces, close to Iraq-Turkey border. Scat-

tered populations of N. crocatus were located during our

2012-2013 surveys. However, many areas in the Erbil

and Duhok provinces suspected to host N. crocatus have

not yet been surveyed.

Conclusion

The mountain dwelling Neurergus newts are living in re-

lictual aquatic environments which may make them par-

ticularly vulnerable to environmental changes. However

the geographical range and distribution of Neurergus

newts in Iraq are not yet fully accessed and little is known

about their ecology and conservation biology. From our

survey results and a literature search we consider that

habitat destruction including pollution when combined

with climate extremes, and especially droughts, are the

main threats to these newts. Urban expansion and rapid

development combined with severe drought especially

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046

July 201 3 | Volume 6 | Number 4 | e68

Al-Sheikhly et al.

during the current years have impacted many fresh water

springs, streams, ponds, and waterfalls which are consid-

ered the main habitats for Neurergus newts in northern

Iraq. Solid wastes produced by tourism and agro-chemi-

cal pollutants, mainly from the use of agricultural pesti-

cides and herbicides, are considered as the main pollut-

ants that may impact Neurergus populations.

Therefore, serious conservation actions should be ur-

gently undertaken in light of various factors negatively

impacting populations of these unique salamanders. The

Iraqi government is responsible for protecting mountain

biota including Neurergus spp., and particularly the Crit-

ically Endangered N microspilotus, as they are iconic

species for conservation. Greater international coopera-

tion between researchers and conservation agencies in

Iraq, Iran, and Turkey, countries sharing similar moun-

tainous habitats and water resources, should be strength-

ened in order to conserve the Neurergus species. The

populations of N microspilotus and N crocatus and their

unique habitat in the mountains of northern Iraq need to

be urgently included in long-term monitoring programs

with the aim of: 1) estimating the effective size and con-

servation significance of genetically distinct populations;

2) quantify the main threats and gathering additional in-

formation of the threats to salamander populations; 3)

undertake in situ actions such as land/water mana;

and protection; and 4) raising educational awa:

should be prioritized to protect and conserve the g

Neurergus in Iraq.

Acknowledgments. — We than

of Environment, Land and

of Environment (IMoE)

ture Iraq for their suppo

Iraq (Kurdistan region

Barbanera; Dr. MijAtar K

Dr. Jorg Feryahqijrand Mr. Ali Ne

assistance d

Taha (Unive

l, and Na-

surve^l&Mi northern

extend to^^. Filippo

Elnaz N aj afimaj d,

alaman for their

Mrs. Zainfi Mahmod and Ali

r their notes and photo-

wa - Sarsank in Duhok

for his helpful support to

ran Nilson for his advice and

ogical studies in Iraq.

Literature Cited

Al-Adhami MA, Hameed AK. 1988. Ultrastructural

study of the thyroid gland of the salamander, Neurer-

gus crocatus crocatus (Cope, 1862). Bulletin of the

Iraq Natural History Museum 8: 25 4 1 .

Allouse BG. 1955. A bibliography on the vertebrate

fauna of Iraq and neighboring countries, reptiles and

amphibians. Iraqi Natural History Mm mum Publica-

tion 6: 1-23.

Cope ED. 1862. Notes upon som^EFTILES o^ k Old

World. Proceedings of the Accn^ry of Nature mSci-

: 337-;

on the

. 96 pp.

on SA. 1992.

and Reptiles.

and Reptiles,

A systematic list of the verte-

ral History Museum Publica-

ences of Philadelphia

KhalafKT. 1959. Reptile

amphibians. Ar-Rc

Leviton AE, Andemof^

Handbook to^mddle

Society Study ol

Oxforc

MahdiN,

‘Iraq.

26: 1-104.

^The newt Neurergus crocatus (Cope,

mqi Natural History Museum Publica-

iaya U. 2010. A newly found locality of

critically endangered Yellow Spotted Newt Neu-

microspilotus (Nesterov, 1916), nourishes hope

for its conservation (Salamandridae: Caudata). Zool-

ogy in the Middle East 51:5 1-56.

Nesterov PV. 1917 (1916). Tri novych chvostatych am-

fibii is Kurdistana [Three new forms of amphibians

from Kurdistan], Ezhegod. Museum of Zoology, Nauk

Petrograd 21: 1-30. [In Russian].

Schneider C, Schneider W. 20 1 1 . The Kurdistan newts of

the Genus Neurergus in Iraq (Caudata: Salamandri-

dae). Herpetozoa 23(3/4): 3-20.

Received: 14 May 2013

Accepted: 16 June 2013

Published: 15 July 2013

Omar F. Al-Sheikhly is an assistant teacher and wildlife expert at the Department of Biology, College of

Science at the University of Baghdad. He has worked as a field team leader, wildlife expert, and provisional

photographer in the Canada-Iraq Marshland Initiative (CIMI) and Nature Iraq. Omar has trained many Iraqi

biologists who now work at the Iraqi environmental institutes such as the Iraqi Ministry of Higher Education

(IMHE) and the Iraqi Ministry of Environment (IMoE) on wildlife field monitoring methodologies. He has

studied and photographed most of Iraq wildlife rarities including Neurergus microspilotus.

amphibian-reptile-conservation.org

047

July 201 3 | Volume 6 | Number 4 | e68

New localities of the Kurdistan and Lake Urmia newts

Iyad Nader is a senior professor in mammals and wildlife expert worked in Nature Iraq Wild Mammals

Advisory Team (NIMAT). His special interest is the conservation of the wildlife of Iraq and he has published

numerous papers and conducted field research with the wild biota of Iraq.

Nasrullah Rastegar-Pouyani earned his B.S. in zoology from Razi University Kermans hah, I ran, in 1986

and his M.S. in zoology from Tehran University, Tehran, Iran, in 1991, where he studied the

agamids as the central object. He started his Ph.D. in Gothenburg University, Swedei^^rl994 uncAfche ad-

visement of Professor Goran Nilson and graduated in 1999, working on taxonomy an^Kjgeography ol

Plateau agamids, with Trapelus as the main objective. He is a professor and head of tl^fckdogy departf

Razi University. His research interests include taxonomy and biogeography IraniaH^teau, the^

East, and central Asian herpetofauna.

Robert Browne, director of the journal Amphibian & Rep A

and practical experience in many research fields suppo

sustainability.

range of academic

ion and environmental

amphibian-reptile-conservation.org

048

July 201 3 | Volume 6 | Number 4 | e68

CONTENTS

Administration, journal information (Instructions to Authors), and copyright notice Inside front cover

Mozafar Sharifi, Hossein Farasat, and Somaye Vaissi — Sexual size dimorphism in Neurergus kaiseri (Cauda-

ta: Salamandridae) in south-western Zagros Mountains, Iran 1

Serge Bogaerts, Henry Janssen, Jennifer Macke, Gunter Schultschik, Kristina Ernst, Francois Mail-

let, Christoph Bork, Frank Pasmans, and Patrick Wisniewski — Conservation biology, husbandry, and

captive breeding of the endemic Anatolia newt, Neurergus strauchii Steindachner (1887) (Amphibia: Cauda-

ta: Salamandridae) 9

Nasrullah Rastegar-Pouyani, Mohsen Takesh, Akbar Fattahi, Marzieh Sadeghi, Fatemeh Khorshidi,

and Robert Browne — Ecology of Kurdistan newt {Neurergus microspilotus : Salamandridae): Population

and conservation with an appraisal of the potential impact of urbanization 30

Elnaz Najafi-Majd and Ugur Kaya — Rediscovery of the Lake Urmia newt, Neurergus crocatus Cope, 1862 (Cau-

data: Salamandridae) in northwestern Iran after 150 years 36

Retracted: Omar Fadhil Al-Sheikhly, Iyad A. Nader, Nasrullah Rastegar-Pouyani, and Robert K.

Browne — New localities of the Kurdistan newt Neurergus microspilotus and Lake Urmia newt Neurergus

crocatus (Caudata: Salamandridae) in Iraq 42

Table of Contents Back cover

VOLUME 6

2013

NUMBER 4