Herpetology Notes, volume 6: 301-306 (2013) (published online on 30 July 2013)
Do North African Fire Salamanders, Salamandra algira,
occur in Tunisia?
Sergé Bogaerts1*, David Donaire-Barroso2, Frank Pasmans3, Salvador Carranza4 and Wolfgang Böhme5
Abstract. Salamandra algira is patchily distributed from north-western Morocco to eastern Algeria. Its occurrence in Tunisia
is under debate. In order to examine the presence of S. algira in Tunisia, three field trips were made to suitable habitats in
the Medjerda mountains in north-eastern Tunisia. Additionally, phenotypic and morphological examinations of “Tunisian” S.
algira museum specimens originating from the ZFMK, Germany, were carried out. No indications for the presence of S. algira
in Tunisia were found during the field trips. The ZFMK specimens of Salamandra algira turned out to be most likely middle
or eastern European Salamandra salamandra. These results do not support earlier statements on the presence of the species
in Tunisia.
Key words. Amphibians, Urodela, Salamandra algira, Tunisian fauna, distribution
Introduction
The NorthAfrican Fire Salamander, Salamandra algira,
occurs in isolated populations throughout the northern
mountain ranges of north-western Africa (Thorn, 1968;
Schleich et al., 1996). Blanc (1935) mentioned that
S. algira might occur in Tunisia, as its type locality is
found fairly nearby in Algeria (approximately 60 km
from the border, Mount (Jebel) Edough, near Annaba).
Schleich et al. (1996) subsequently included localities
in Morocco and Algeria as part of the distribution of this
species, but did not mention a possible occurrence in
Tunisia. Despite the fact that Blanc (1935) encouraged
searches for S. algira in the Khroumiri, no subsequent
records were provided. Salvador (1996) was the first
Lupinelaan 25, NL-5582CG, Waalre, The Netherlands
C/Mar Egeo n° 7, E-11407, Jerez de la Frontera, Spain.
3
Department of Pathology, Bacteriology and Avian Diseases,
Faculty of Veterinary Medicine, Ghent University,
Salisburylaan 133, B9820 Merelbeke, , Belgium.
4
Institute of Evolutionary Biology (CSIC-UPF) CMIMA Passeig Marítim de la Barceloneta, 37-49
E-08003 Barcelona, Spain.
5
Zoologisches Forschungsmuseum Alexander Koenig,
Adenauerallee 160, D-53113, Bonn, Germany.
*
Corresponding author; e-mail: [email protected]
1
2
to map S. algira for Tunisia, which has been repeated
or ignored by subsequent authors (Thiesmeier, 2004;
Donaire-Barroso et al., 2009; Stuart et al., 2008;
Frost, 2013). The map in Salvador (1996) is based on
museum records. The presented data for Tunisia refers
to specimen of the Zoologisches Forschungsmuseum
Alexander Koenig (ZFMK, Bonn, Germany) and are
the only vouchers worldwide of S. algira from this
country.
Eiselt (1958) in his extensive work shows that S.
algira has, in comparisson with all other Salamandra
species and subspecies, an extreme long and round tail,
small head and the ventral side is pure black or with
only small yellow speckels or spots.
The aim of this study was to gather evidence on
the occurrence of S. algira in Tunisia. Therefore, we
conducted three field surveys and compared phenotypic
and morphological data of the ZFMK specimens with
confirmed S. algira specimens.
Material and methods
The “Tunisian” S. algira collection in the ZFMK, Bonn
consists of many animals, larvae, juveniles, subadults and
adults. They all come from a population kept in captivity
by Wolfgang Mudrack (Berlin) originally bought from
Werner Vogel (Hebertsfelden near Rottach-Inn), with an
exact locality of origin, ‘Toucabeur Brancon Gebirge,
100 km SW of Tunis’, which probably is a synonym of
Toukaber (or Toucabour in French). This place is situated
302
northwest of Mejez El Bab and is of archaeological
interest. These ZFMK specimens were compared with
S. algira specimens observed and measured in the field
in Morocco, and with Moroccan and Algerian museum
specimens from the Zoologische Museum Amsterdam
(ZMA), Museo Nacional de Ciencias Naturales Madrid,
Spain (MNCN) and Natural History Museum Vienna
(NHMW).
Different body measurements were taken by the same
person with a marking gauge and noted to the nearest
1 mm. For the comparison of measurements we used
animals of general similar size, except for the available
Annaba specimens which are all smaller in size. We
only used animals without visible tail injuries (which
could shorten the tail). Coloration and colour pattern
were noted and photographed.
For the field research we targeted the area closest
to the Algerian border in the north western Medjerda
mountains of Tunisia. This area has the highest annual
rainfall of Tunisia ranging between 800 – 1500 mm
a year (see Sicilia et al., 2009). Additionally, other
North African relict amphibian and reptile species
occur there (Brito et al., 2008; Bogaerts et al., 2013.).
Besides, we visited Toukaber once. We examined
suitable habitats, based on experience with S. algira
in Morocco (see Donaire-Barroso & Bogaerts, 2003;
Bogaerts & Donaire-Barroso, 2003; Beukema et al.,
2010). The Mediterranean Oak forests of the Medjerda
mountains are characterized by high humidity and
winter rain carrying streams, which seem suitable for
the development of Salamandra larvae. Several streams
were checked for larvae and their surroundings for
adults at daytime and at nighttime with flashlights. In
total, three field investigations to this area were made;
from 5 to 11 February 2000, from 4 to 12 March 2001
and from 26 to 29 March 2005.
As an indirect second method, we also showed colour
pictures of several reptiles and amphibians, including S.
algira, to shepherds and hunters we met in the field to
ask them if they had ever seen the species in the area. It
is important to stress that confusion with other animals is
unlikely due to the striking species colouration pattern.,
which makes the use of photographs a fine tool.
Results
Examination of museum material
We found marked differences in colouration between
the presumed Tunisian museum specimens (ZFMK
3738-37343, ZFMK 40211-40219) and confirmed S.
algira (Figure 1). While all Moroccan and Algerian
Sergé Bogaerts et al.
specimen examined had unspotted or very scarcely
spotted undersides, the ZFMK specimen always
possessed spots, sometimes covering more than 50%
of the venter (see Figures 2 and 3). The arrangement
of the spots on the dorsal side is different as well;
several ZFMK specimen presented two dorsal rows of
spots, which rarely occurs in S. algira. The snout was
more pointed in the ZFMK specimen compared to that
of confirmed S. algira. Tails were much shorter in all
ZFMK specimen (see Table I) than all S. algira. One
way ANOVA and post hoc LSD tests showed that the
supposedly Tunisian salamanders had a significantly
higher SVL/TaL compared to S. algira (p < 0.001).
Field research
Besides Discoglossus pictus and Bufo bufo, no other
amphibians were found in the examined streams.
Toukaber was found to be unsuitable. In total, we
showed the pictures of reptiles and amphibians to four
shepherds and two hunters in the Medjerda mountains.
None of them had ever seen an animal resembling a
member of the genus Salamandra, but they recognised
many others that live in the area, like Testudo graeca
and Timon pater.
Discussion
Morphological and phenotypical examination of the
ZFMK “Tunisian” specimen revealed that these are
not Salamandra algira but Salamandra salamandra,
and therefore represent an error. The ZFMK specimen
show also large similarities in colouration pattern and
morphology with central European specimens, such as
those originating from the area were S. s. terrestris and
S. s. salamandra meet or with Ukrainian S. salamandra
(see pictures in Thiesmeier, 2004). Especially the
latter show slender bodies with relatively long tails. A
distinct colouration feature are the bellies and throats.
The ZFMK specimen typically have yellow colouration
on the chin, which is found in European specimens
but does never occur in S. algira. The bellies of the
ZFMK specimens are all heavily covered with yellow
dots, which is not seen in S. algira (see Eiselt, 1958;
Beukema et al., 2013). Furthermore some of the ZFMK
“Tunisian” specimen have two dorsal rows of spots,
also typical for middle European individuals, but not
typical for S. algira (Eiselt, 1958; Pasteur & Bons,
1958; Bogaerts & Donaire-Barrosso, 2003; Beukema et
al., 2013). Böhme et al. (2013) describe another distinct
character, black dotted pore exits on the yellow parts of
the paratoids, that is not seen in S. algira or Salamandra
Do North African Fire Salamanders, Salamandra algira, occur in Tunisia?
303
Figure 1. Dorsal and ventral views of Salamandra algira. A and B: Neotype of Salamandra algira algira from Jebel Edough,
Annaba, Algeria. C and D: Salamandra algira splendens. from Jebel Tazzeka, Taza, Morocco. E and F: Salamandra algira
tingitana from Jebel Tagramt, Tetouan, Morocco.
infraimmaculata but in all S. salamandra subspecies
and in Salamandra corsica. These black dotted exits are
clearly visable in the ZFMK specimen.
Although the field research resulted in no indication of
S. algira occurring in Tunisia, the Medjerda mountains
are the most suitable area to look for S. algira. The habitat
is also inhabited by other North African relict species
such as Bufo bufo, Natrix natrix, Coronella girondica,
Vipera latastei and Podarcis vaucheri (Bogaerts et al.,
2002; Brito et al., 2008), which, except for N. natrix
and V. latastei, were found during our excursions. Other
recent, more intensive surveys did neither find S. algira
in northwest Tunisia (Sicilia et al., 2009; Ben Hassine
& Nouira, 2012), but revealed new data on B. bufo
(Ben Hassine & Nouria, 2012; Bogaerts et al., 2013).
We did not search in the Toukaber Mountains other
304
Sergé Bogaerts et al.
Figure 2. Dorsal views of seven ZFMK specimen.
Figure 3. Ventral views of seven ZFMK specimen.
than once and briefly, as none of the species from the
above mentioned herpetological community species is
found there and the annual rainfall is much lower (< 500
mm a year). This leads us to believe the area is highly
unsuitable for S. algira and makes the origin of the
ZFMK specimens even more questionable.
A last hypothesis for not finding S. algira is that
the Tunisian populations are producing completely
developed young, and therefore go easily unnoticed
while searching for larvae, like S. algira tingitana in
305
Do North African Fire Salamanders, Salamandra algira, occur in Tunisia?
Table 1. Measurements of S. algira. Measurements are given in mm and abbreviated as follows: total length (TL), snout vent
length, including cloaca (SVL), tail lenght (TaL), standard deviation (SD).
Sex
M
M
M
F
Origin
ZFMK 37338
ZFMK 37339
ZFMK 37827
ZFMK 37343
TL
173.5
175.6
167.5
160
169.2
(7.0)
SVL
105.5
105.6
103.4
96.4
102.7
(4.4)
TaL
68
70
64.1
63.6
66.4
(3.1)
SVL/TaL
1.55
1.51
1.61
1.52
1.55
(0.05)
Remarks
F
M
M
MNCN 41037
ZMA 20011
ZMFK 77415
162.2
187.4
173.5
174.4
(12.6)
96.8
106.4
98.5
100.6
(5.1)
65.4
81
75
73.8
(7.9)
1.48
1.31
1.31
1.37
(0.10)
Holotype
Paratype
Paratype
S. a. splendens
S. a. splendens
S. a. splendens
S. a. splendens
S. a. splendens
S. a. splendens
S. a. splendens
Mean
(SD)
Chefchaouen F
Chefchaouen F
Chefchaouen M
Chefchaouen M
Chefchaouen M
Chefchaouen M
Chefchaouen F
live specimen
live specimen
live specimen
live specimen
live specimen
live specimen
live specimen
191.1
195
195.2
173.5
192.2
194
193
190.6
(7.7)
111.1
106
111
95.5
105.5
104
110
106.2
(5.5)
80
89
84.2
78
86.5
90
83
84.4
(4.5)
1.39
1.19
1.32
1.22
1.22
1.16
1.33
1.26
(0.08)
S. a. algira
S. a. algira
S. a. algira
Mean
(SD)
Jebel Edough
Jebel Edough
Jebel Edough
NHW 9251/1
NHW 9251/2
NHW 9251/3
149.5
119.5
155.9
141.6
(19.4)
85.5
66.5
84.9
78.1
(10.8)
64
53
71
62.7
(9.1)
1.34
1.25
1.20
1.26
(0.07)
?
?
?
?
Mean
(SD)
Locality
"Toucabour"
"Toucabour"
"Toucabour"
"Toucabour"
S. a. tingitana Jebel Musa
S. a. tingitana Jebel Musa
S. a. tingitana Jebel Musa
Mean
(SD)
the north of Morocco (Donaire-Barroso & Bogaerts,
2001; 2003). However, one specific environmental
condition is very different, in comparison to viviparous
populations of S. algira. Northwest Tunisia consists of
sandstone, whereas all Moroccan S. algira are found in
limestone areas. Also Mount Edough, Algeria, the S.
algira closest to Tunisia consists of limestone (Thomas
Schöttler, pers. comm.).
We conclude that the ZFMK specimen are Salamandra
salamandra and there is no direct or indirect evidence
yet that Salamandra algira occurs in Tunisia. We
therefore recommend it to be removed from the Tunisian
herpetofauna species list until proven otherwise.
Acknowledgements. We thank Dave Herbert (United Kingdom)
is for his support on the field trip in 2000, David Buttle (United
Kingdom) for sharing his field data, Mohsen Kalboussi (Tunisia)
for his research work, Chantal Ruijgrok for turning old slides into
decent digital figures 1 and 2, Thomas Schöttler (Germany) for
Neotype
Paratype
Paratype
information on S. algira localities at Mount Edough, Algeria.
Franz Tiedemann and Heinz Grillitsch (NHMW) are kindly
thanked for their kind help in the museum.
References
Ben Hassine, J., Nouira, S. (2012): Répartition géographique et
affinités écologiques des amphibiens de Tunisie. 67 (4): 437457.
Beukema, W., de Pous, P., Donaire, D., Escoriza, D., Bogaerts, S.,
Toxopeus, A.G., De Bie, C.A.J.M., Roca, J., Carranza, S. (2010):
Biogeography and contemporary climatic differentiation
among Moroccan Salamandra algira. Biological Journal of
the Linnean Society 101: 626–641.
Beukema, W., de Pous, P., Donaire-Barroso, D., Bogaerts, S.,
Garcia-Porta, J., Escoriza, D., Arribas, O.J., El. Mouden, H.,
Carranza, S. (2013): Review of the systematics, distribution,
biogeography and natural history of Moroccan amphibians.
Zootaxa 3661 (1): 001–060.
Blanc, M. (1935): Reptiles et Batraciens. In: Faune tunisienne 3,
Tunis, 267-277.
306
Bogaerts, S., Pasmans, F., Donaire-Barroso, D. (2002): Über
einige Lacertiden aus Marokko und Tunesien. Die Eidechse
13(3): 77-84.
Bogaerts, S., Donaire-Barroso, D. (2003): Sobre el politipismo en
Salamandra algira Bedriaga, 1883. Boletín de la Asociación
Herpetológica Española 14 (1-2): 47-51.
Bogaerts, S., Donaire-Barroso, D., Pasmans, F., Herbert, D.,
Beukema, W. (2013): New data on distribution of Bufo bufo in
Tunisia. Herpetology Notes 6: 203-207.
Böhme, W., Hartmann, T., Fleck, J., Schöttler, T. (2013:
Miscellanous notes on Oriental fire Salamanders (Salamandra
infraimmaculata Martens, 1885) (Lissamphibia: Urodela:
Salamandridae. Russian Journal of Herpetology 20 (1): 6672.
Bons, J., Geniez, P. (1996): Amphibiens et Reptiles du Maroc.
AHE. Barcelona. 267: 637-649.
Brito, J.C., Feriche, M., Herrera, T., Kaliontzopoulou, A.,
Martínez-Freiría, F., Nesbitt, D., Omolo, D., Ontiveros,
D., Quiñoz, L., Pleguezuelos, J. M., Santos, X., Sillero, N.
(2008): En los límites de su distribución: anfibios y reptiles
paleárticos en el noroeste de Túnez. Boletín de la Asociación
Herpetológica Española 19: 75-82.
Domergue, C. (1959): Liste des Batraciens, Chéloniens et Sau­
riens de Tunisie et d’Afrique du Nord. Bulletin de la Société
des Sciences Naturelles de la Tunisie 12: 75-79.
Donaire-Barroso, D., Bogaerts S. (2003): A new subspecies of
Salamandra algira Bedriaga, 1883 from northern Morocco.
Pod@rcis, 4: 84-100.
Donaire-Barroso, D., Martínez-Solano, I., Salvador, A., GarcíaParís, M., Recuero Gil, E., Slimani, T., El Mouden, H.,
Geniez, P., Mateo, J. ( 2009): Salamandra algira. In: IUCN
2012. IUCN Red List of Threatened Species. Version 2012.2.
www.iucnredlist.org. Downloaded on 03 December 2012.
http://www.iucnredlist.org/details/59464/0
Sergé Bogaerts et al.
Eiselt, J. F. (1958): Der Feuersalamander, Salamandra
salamandra, Beiträge zu einer taxonomischen Synthese.
Abhandlungen und Berichte für Naturkunde und Vorgeschichte
Museum Magdeburg, 10 (6): 77–154.
Frost, D. R. 2013. Amphibian Species of the World: an Online
Reference. Version 5.6 (9 January 2013). Electronic Database
accessible at http://research.amnh.org/herpetology/amphibia/
index.html. American Museum of Natural History, New York,
USA. (accessed at 25-05-2013).
Salvador, A. (1996): Amphibians of northwest Africa. Smithsonian
Herpetological Information Service no. 109. 43 pp.
Schleich H. H., Kästle W. & Kabisch K. (1996): Amphibians and
Reptiles of North Africa. Koeltz Scientific Books. Koenigstein,
627 pp.
Sicilia, A., Marrone, F., Sindaco, R., Turki, S., Arculeo, M.
(2009): Contribution to the knowledge of Tunisian amphibians:
notes on distribution, habitat features and breeding phenology.
Herpetology Notes 2: 107-132.
Stuart, S. N., Hoffmann, M., Chanson, J., Cox, N., Berridge, R.,
Ramani, P., Young, B. (Eds.) (2008): Threatened Amphibians
of the World. Lynx Editions, Barcelona, Spain. ISBN
Thiesmeier, B. (2004): Der Feuersalamander. Laurenti Verlag,
Bielefeld. ISBN 3-933066-21-2.
Thorn, R. (1968): Les salamandres d’Europe, d’Asia, et d’Afrique
du Nord. 376 pp. Éditions Paul Lechevalier. Paris.
Accepted by Zoltan T. Nagy