Comments on the large paleartic vipers Macrovipera and Daboia in North Africa

by Octavio Jiménez Robles & Gabriel Martínez del Marmol Marín.

In North Africa, three species of large paleartic vipers have been recorded inside the genus Macrovipera sensu Herrmann et al., 1992 (Schleich et al., 2006). Several phylogenetic studies suggest the allocation of two of these species inside the genus Daboia (Lenk et al., 2001; Garrigues et al., 2005; Wüster et al., 2008; Pyron et al., 2011): D. mauritanica (Duméril & Bibron, 1848), and D. deserti (Anderson, 1892). The third described clade in North Africa is Macrovipera lebetina transmediterranea Nilson & Andrén 1988, not included in any recent phylogenetic analysis. The validity of the taxa transmediterranea and deserti as full species is currently uncertain due to the scarcity of records along all their supposed distribution.

After its description in 1988, the existence of M. l. transmediterranea has never been accurately confirmed. It was described from five specimens tagged from Algiers and Tunis (the capitals of Algeria and Tunisia) as a sympatric species with D. mauritanica with shorter body length, reduced number of dorsal scale rows and different colour pattern (Nilson & Andrén, 1988). Another transmediterranea specimen not collected was mentioned to be observed in Djebel Murdjadjo, near Oran, Algeria (Nilson & Andrén, 1988). Bons & Geniez (1996) suggested the possibility that this viper occurs in northeast Morocco, although for the moment there is no information about it. Recently one (or several) snake(s) was(were) identified as M. l. transmediterranea after being captured in rocky areas of north Tunisia, without exact locality (Bazaa et al., 2005; 2006; 2009; Sanz et al., 2006; Liman et al. 2010). In those venom proteomic publications it is not specified whether this specimen was deposited in a scientific collection, so for the moment its identity as the taxon transmediterranea remains unverifiable. In Dobiey & Vogel’s book (page 143, 2007) there is a picture of a viper named as this species, but the specimen has an unknown origin (J.J. Calvete & A. Bazaa, pers. comm.), so it cannot be assigned neither to transmediterranea nor to Tunisia.

Table 1: Some of the main differences between D. mauritanica, D. deserti and M. l. transmediterranea
(based in Anderson, 1892; Kramer & Schnurrenberger, 1963; Nilson & Andrén, 1988; Herrmann et al., 1992).

mauritanica deserti transmediterranea
colour pattern wavy undulating zig-zag band along the back which constitutes 23 to 33 blotches or windings (sometimes reddish or brownish with weakly developped pattern) rather pale with wavy undulating band weakly developed or absent (it fades with age) 34 to 41 transverse bands (31-46; Herrmann et al., 1992)
number of scale rows between the dark blotches and the ventrals (Kramer & Schnurrenberger, 1963) 5 3-4 ?
midbody dorsal scale rows 27 27 25
neck scale rows 26-27 26-27 ~24
scales on upper surface of head keeled smooth keeled
canthus rostralis present absent present
rostral shield broader than high higher than broad broader than high
ventrals 157-174 ♀♀; 163-170 ♂♂ 164-170 ♀♀; 166-169 ♂♂ 150-164 ♀♀; 154-163 ♂♂
subcaudals 45-48 ♀♀; 45-50 ♂♂ 44-51 ♀♀; 46-51 ♂♂ 37-43 ♀♀; 42-51 ♂♂

Appart from its scarcity of records, the morphological diagnostic traits of transmediterranea are doubtful. Besides transmediterreanea dorsal colour pattern was described as transversal bars (see Table 1; Nilson & Andrén, 1988), several authors consider it similar to the wavy undulating pattern of mauritanica (Herrmann et al., 1992; Venchi & Sindaco, 2006). Other differences such as the reduced dorsal scales might be inside the variation of juveniles of mauritanica as well (Venchi & Sindaco). Hence, the validity of transmediterranea is questionable (Venchi & Sindaco, 2006; Agasyan et al., 2009; R. Sindaco, pers. comm.). However a specimen of the Natural History Museum of London has recently been identified as M.l. transmediterranea (W. Wuster, pers. comm.).

Head of Daboia deserti
Macrovipera lebetina transmediterranea” (paratype, NMW 25229), juvenile specimen from Tunis, Tunissia, collected in 1913 by A. Weidholz.
It is currently deposited in the Naturhistorisches Museum Wien, Vienna, Austria. Photos: © Tomas Mazuch.
Daboia lebetina
Vipera lebetina L. Levanthuggorm Algeriet” deposited in “Evolutionsmuseet”,
the Zoological museum in Uppsala (Sweden). Photo: © Alexander Westerström.

The only concise way of solving this uncertainty on the phylogenetic allocation of the taxon transmediterranea, would be including genetic material of the syntypes in next molecular phylogenetic studies. We suspect the taxon transmediterranea will be probably allocated in the Daboia clade, as it is widely separated from other Macrovipera populations in the Eastern Mediterranean, and close to other Daboia. Evenmore, transmediterranea might be a synonymy of D. mauritanica.

Mapa

Map showing the supposed distribution for D. mauritanica, D. deserti, D. palestinae, M. schweizeri and M. lebetina, with the approximate type localities of their subspecies. All the ranges as stated in the IUCN red list of species (Miras et al., 2006a; 2006b; Böhme et al., 2009; Hraoui-Bloquet et al., 2009) excepting for M. lebetina (modified from Stümpel & Jöger 2009).

Daboia deserti was described as a subspecies of M. lebetina differing from the type of D. mauritanica by the absence of canthus rostralis and interorbital scales not keeled (Anderson, 1892). As an anecdote, Anderson used for comparison some two of the specimens that later would become syntypes of transmediterranea (Nilson & Andrén, 1988). The colour pattern of deserti was described as “pale yellowish brown above with very faint indications of the dorsal and lateral dark spots distinctive of Algerian and Cyprian examples of the typical form” (Anderson, 1892).

Head of Daboia mauritanica Head of Daboia deserti
Head details of Daboia mauritanica in Morocco (left) and Daboia deserti in Tunissia (right). Note the keeled interorbital scales in D. mauritanica,
smooth in D. deserti. Photos: © Tomas Mazuch.

Since the description of deserti its distribution and phylogenetic relations with mauritanica are not clear. Kramer & Schnurrenberger (1963) suggested that deserti should be regarded as a subspecies of D. mauritanica. They stated a disjunct distribution for both taxa: north of the High Atlas Range and coastal areas of Algeria for mauritanica, and from south of the Atlas Range to Libya for deserti. Another morphologic trait was pointed for the diagnosis: the number of scale rows between the dorsal dark blotches and the ventrals is normally more than 5 in mauritanica and 3-4 rows in deserti (Kramer & Schnurrenberger, 1963).


Illustrations showing the differences in number of scale rows between dark blotches
and ventral scales in Daboia mauritanica (upper) and D. deserti (lower)
(from Kramer & Schurrenberg, 1963; published with permission).
Head of Daboia deserti Head of Daboia mauritanica
Left: Daboia mauritanica with contrasted pattern. Casablanca (Morocco). Photo: © Gabri Mtnez.
Right: Daboia deserti. Yogurth Hill (Tunissia). Photo: © Tomas Mazuch.

After considering deserti as a close taxon to mauritanica due to morphologic similarities (Kramer & Schnurrenberger, 1963), the work of Herrmann and collaborators (1987; 1992) with non-genetic molecular methods showed differences to separate them again as independent species. The immunological distance of mauritanica to the Cypriotic M. l. lebetina , was smaller than the distance with deserti (Herrmann et al., 1987).

In Morocco some specimens with a pale colour pattern have been found (Destre et al., 1989). They were attributed to a pale morph of D. mauritanica (Saint Girons, 1956; Nilson & Andren, 1988) distributed along the Antiatlas and the south of the High Atlas (Geniez et al., 1991; Bons & Geniez, 1996). However, other authors identified them as D. deserti (Destre et al., 1989; Schleich et al., 1996).

Daboia
Specimen of Daboia with pale colouration. Tendrara (Morocco). Photo: © Philippe Geniez.

In more recent phylogenetic research with mitochondrial DNA fragments both mauritanica and deserti were grouped together with very short branches (Lenk et al., 2001; Pyron et al., 2011), suggesting a very low genetic differentiation, even below the species level (Miras et al., 2006; Stümpel & Jöger, 2011; U. Jöger, pers. comm.).

The separation of deserti and mauritanica as different species (Herrmann et al., 1987; 1992) has been criticized from the morphological point of view (Wade, 2008), because specimens of the most separated limits of the distribution of both species were used: D. mauritanica of Aouolouz, Morocco and D. deserti of Djebel Nefusa, Libya, without examining specimens of the middle of the distribution of both species (Algeria). The analysis of specimens of the “pale morph” of D. mauritanica in Algeria suggests the possibility of a clinal differentiation from northwest to southeast (Wade, 2008). In fact, apart from the colour pattern, some of the traits used in the description of deserti, such as the smooth upper head scales, are not consistent in all the currently known specimens (Schleich et al., 1996).

Daboia mauritanica Daboia mauritanica
Daboia mauritanica: female (left) and male (right). Ksar Chellala (Algeria). Photos: © Peter Stafford
Mapa

Map showing the conflictive distribution of the different morphs of Daboia in the Maghreb. Yellow colour for “pale” Daboia mauritanica and Daboia deserti; Red colour for Daboia mauritanica with contrasted pattern; Grey colour for indeterminate individuals (probably “pale” mauritanica/deserti individuals); Green colour for supposed localities of Macrovipera lebetina transmediterranea. Aproximate type localities of the three taxa are represented as red dots. Black dots are other localities for transmediterranea (Tunis, Tunissia and Djebel Mudjadjo, Oran, Algeria). Map based in Nilson & Andrén, 1988; Bons & Geniez, 1996; Geniez et al., 2004; Dobiey & Vogel, 2007; Wade, 2008; Phelps, 2010; M. Schweiger, pers. comm.; T. Mazuch, pers. comm. Different proposed borders between deserti and mauritanica are represented as well (modified from Schleich et al., 1996).

The distribution areas of both coloration patterns remain unclear. The contrasted morph of mauritanica is found in north Atlas and coastal areas of Algeria; while the pale morph of mauritanica/deserti has been observed from south of Atlas range to Lybia through the Saharan Atlas in Algeria and Tunisia. However exceptions to this range pattern have been found. The variability in the coloration of Daboia in the Maghreb is rather high.

The specimen from Djebel Murdadjo (Algeria; Nilson & Andrén, 1988) might belong to the pale morph of Daboia mauritanica/ Daboia deserti (P. Geniez, pers. comm.).

Mario Schweiger found two sympatric specimens with different colouration south of the Atlas: one contrasted (male) and one pale (female).

Daboia Daboia
Daboia mauritanica: male (left) and female (right). Ouarzazate. Photos: © Mario Schweiger.

Whereas Tomas Mazuch and collaborators (pers. comm.) found two Daboia specimens with “deserti” pattern in Mediterranean habitat in northwest Tunisia, Karel Rozínek found a specimen with “mauritanica” pattern in Chambi National Park, Atlas range, where Daboia deserti should be the expected species (T. Mazuch, pers.comm.). A possibly similar pattern is found in the Chalcides ocellatus species complex, as specimens of a North Moroccoan-Algerian clade were found in Redeyef, aproximately 90 km south of Jebel Chambi (Kornilios et al., 2010).

Daboia mauritanica Daboia deserti
Left: Daboia mauritanica. Chambi National Park (Tunissia). Photo: © Karel Rozínek.
Right: Daboia deserti. Lake Ichkeul (Tunissia). Photo: © Tomas Mazuch.

In the areas between Agadir and Tan-tan (Morocco) it is even possible to find individuals of both morphs, intermediate individuals and sometimes specimens of both “morphs” with a reddish coloration. This pattern was described for D. mauritanica (Saint-Girons, 1956, Nilson & Andrén, 1988).

Daboia mauritanica Daboia mauritanica
Left: Daboia mauritanica, redish phase with a “pale zigzag”. Guelmim (Morocco). Photo: © Daniel Gómez.
Right: Daboia mauritanica, redish phase with a “contrasted zigzag”. Agadir (Morocco). Photo: © Hazel Skeet.
Daboia mauritanica Daboia mauritanica
Daboia mauritanica with intermediate morph.
Guelmim (Morocco). Photos: © Daniel Gómez.

Further research with genetic phylogenies with a wide sampling all over northwest Africa, is necessary to clarify the identity of clades such us transmediterranea or deserti as full species (or subspecies). They might be simply morphological variations of D. mauritanica, or something else as a consequence of certain isolation. In a next future the population structure of this species complex will be better known.

Acknowledgements

We thank Roberto Sindaco, Ulrich Joger, Tomas Mazuch, Wolfgang Wuster, Mario Schweiger, Ed Wade, Philippe Geniez, Fernando Martínez Freiría, Juan Timms, Daniel Gómez, Hazel Skeet, Karel Rozínek, Juan Jose Calvete, Amine Bazaa, Alexander Westerström, Raúl León and Peter Stafford’s family for their pictures, articles or information.

To cite this page:
Octavio Jiménez Robles & Gabriel Martínez del Mármol Marín: Comments on the large paleartic vipers Macrovipera and Daboia in North Africa.
Published on March 05, 2012. Updated on April 23, 2012. Available from http://blog.moroccoherps.com/vipers-macrovipera-and-daboia-in-north-africa. Accessed December 12, 2017.

To cite www.moroccoherps.com as a whole:
Amphibians & Reptiles of Morocco and Western Sahara.
Available from www.moroccoherps.com. Accessed December 12, 2017.

Bibliography: