CYTOTAXONOMY of SHREWS of the GENUS CROCIDURA from MEDITERRANEAN ISLANDS P Vogel, T Maddalena, P Schembri

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CYTOTAXONOMY OF SHREWS OF THE GENUS CROCIDURA FROM MEDITERRANEAN ISLANDS P Vogel, T Maddalena, P Schembri

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P Vogel, T Maddalena, P Schembri. CYTOTAXONOMY OF SHREWS OF THE GENUS CRO- CIDURA FROM MEDITERRANEAN ISLANDS. Vie et Milieu / Life & Environment, Observatoire Océanologique - Laboratoire Arago, 1990, pp.124-129. hal-03035858

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CYTOTAXONOMY OF SHREWS OF THE GENUS CROCIDURA FROM MEDITERRANEAN ISLANDS

P. VOGEL1, T. MADDALENA1 , P.J. SCHEMBRI2 1 Institut de Zoologie et d'Ecologie Animale, Université de Lausanne, CH-1015 Lausanne, Suisse 2 Department of Biology, University of Malta, Msida, Malta

SORICIDAE RÉSUMÉ - Il a été possible de vérifier le statut taxonomique de diverses popu- CROCIDURA lations de Musaraignes insulaires grâce à l'étude chromosomique. Quatre espèces TAXONOMŒ ont été mises en évidence par cette méthode. Deux espèces, C. russula et C. sua- BIOGÉOGRAPHIE veolens, sont d'origine continentale, introduites sur les îles par l'homme. En re- vanche, pour deux autres espèces, C. sicula de Sicile et de Gozo et C. zimmermanni de Crète, aucune population continentale n'est connue et il faut les considérer comme survivantes des faunes insulaires du Pléistocène.

SORICIDAE ABSTRACT - Thanks to chromosome studies it was possible to review the tax- CROCIDURA onomic status of many insular populations of shrews and to demonstrate the pré- TAXONOMY sence of four distinct species. Two of thèse, C. russula and C. suaveolens, are of BIOGEOGRAPHY KARYOTYPE continental origin and have been introduced on the islands by man. On the con- trary, the other two species, C. sicula from Sicily and Gozo, and C. zimmermanni from Crète, are not known from continental land masses and we consider them to be survivors from the insular faunas of the Pleistocene.

INTRODUCTION continental species of Crocidura have distinct karyotypes (Fig. 1), this method was systemati- cally applied to island populations in an effort to According to the list compiled by Ellerman and résolve their taxonomy. The results of thèse stu- Morrison-Scott (1966), 27 species of the genus dies have been published in many scattered pub- Crocidura have been described from Europe. Most lications and it is useful therefore to présent a of thèse are local forms and modem taxonomists synthetic review. Four of the five European spe- like Jenkins (1976) and Corbet (1978) recognize cies here recognized are documented with pictures only three valid species : C. leucodon, C. russula of the living animais (Fig. 2). A map of the and C. suaveolens. This discrepancy is due to the Medterranean région showing the geographical fact that thèse species are morphologically very similar whereas intraspecific variability is rather Table I. - The history of the taxonomic interprétation high. The taxonomic assignment of island popu- of the shrews of Crète based on morphological analyses. lations is particularly problematic as morphology is strongly affected by genetic isolation and the particular sélective pressures of island environ- Author Lowland form Mountain form ments. The history of the taxonomic interprétation of the shrews of Crète provides a good illustration Miller 1909 C. caneae Bace 1913 C. (russula) caneae (Table 1). Wectstein 1953 C. russula caneae C. russula zimmermanni When morphological interprétations remain un- Richter 1970 C. gueldenstaedtii C. russula zimmermanni certain, other techniques are needed. One of the Vesmanis & Kahmann C. gueldenstaedtii C. zimmermanni* (1978) most effective is détermination of the karyotype, Hutterer 1981 C. suaveolens* C. russula zimmermanni which, in the genus Crocidura, is very différent between species, but shows minimal intraspecific variation (Reumer and Meylan 1986). As the three CROCIDURA FROM MEDITERRANEAN ISLANDS 125

A*—XX If-**" B~j||~Wl MA Si

HPinfcir S«r X Y X Y X Y

C. zimmermanni (2n = 34, NF = 44) C. russula (2n = 42, NF = 60) C. suaveolens (2n = 40, NF = 50)

01 1* nA m **

X Y X Y C. sicula (2n = 36, NF = 56) C. leucodon (2n = 28, NF = 56)

Fig. 1. - Karyotypes of the European species of the genus Crocidura. NF is the number of chromosome arms in the female.

Fig. 2. - A. C. russula (from Switzerland), B. C. suaveolens (from Corsica), D. C. sicula (from Gozo), D. C. leucodon (from Georgia, USSR). No photographs of living C. zimmermanni exist. 126 P. VOGEL, T. MADDALENA, P.J. SCHEMBRI

Fig. 3. — Distribution of Crocidura spp. on Mediterranean islands as determined by chromosomal and biochemical analyses. Islands : 1 = Ibiza, 2 = Minorca, 3 = Corsica, 4 = Sardinia, 5 = Sicily, 6 = Gozo, 7 = Crète, 8 = Cyprus. distribution of the karyologically determined island. According to an analysis of owl pellets by populations is also given (Fig. 3). F. Poitevin (pers. comm.) two species may occur on Lesbos.

MATERIAL AND METHODS Crocidura russula (Hermann, 1780)

The source of the material which served for Greater white-toothed shrew. According to chromosomal analysis (carried out either in Jenkins (1976) and Corbet (1978), this species oc- Lausanne or in Montpellier) is as follows : Cor- curs from the Near East (Israël, Turkey), through sica : R. Fons (Banyuls, F); Crète : M. Geiger & R Middle and South Europe, to North Africa. By Vogel (Lausanne, CH); Cyprus and Lesbos : F. means of cytotaxonomy it was possible to show Catzeflis & C. Doerig (Lausanne); Gozo : RJ. its absence south of the Alps (Meylan and Hausser Schembri, M. Borg (Malta) & P. Vogel (Lausanne); 1974) and to demonstrate that the populations Ibiza and Minorca : F. Poitevin (Montpellier, F); from eastern Europe and the Near East assigned Sardinia : A. Geraets & R. Hutterer (Bonn, D.); to this species in fact ail belong to C. suaveolens Sicily : P. Vogel (Lausanne). (Catzeflis et al. 1985). Thus the continental distribution of C. russula is limited to parts of Cen- In some cases the karyotypes were prepared tral and southwestern Europe, as well as to North directly in the field. Two techniques were em- Africa, its probable place of origin (Catzeflis ployed, either the squash method using fragments 1984, Vogel and Maddalena 1987). On Mediter- of the spleen (Meylan 1967) or the air-drying tech- ranean islands C. russula occurs only on Sardinia nique using bone marrow (Baker et al. 1982). In (Catzeflis 1983) and Ibiza (Catalan et al. 1988). order to study other parameters from the same According to Sans-Coma et al. (1985) and Vigne shrews, laboratory breeding populations were es- and Alcover (1985) it was introduced during his- tablished when possible. torical times.

DISTRIBUTION OF THE SPECIES Crocidura suaveolens (Pallas, 1811) Crocidura leucodon (Herman, 1780) Lesser white-toothed shrew. This species orig- Bicoloured white-toothed shrew. This shrew inates in Asia (Catzeflis 1984) but now occupies may occur on Lesbos, Greece (two spécimens as- a wide distributional range from Portugal to Korea signed by Ondrias, 1969, to C. lasiura), but Catze- (Corbet 1978). In North Africa, C. whitakeri was flis et al. (1985) found only C. suaveolens on this previously considered to be a subspecies of C. CROCIDURA FROM MEDITERRANEAN ISLANDS 127

suaveolens, but this interprétation is no longer ac- Crocidura zimmermanni Wettstein, 1953 ceptée! (Hutterer 1986, Rzebik-Kowalska 1988). However, Vesmanis (1988) recently assigned one Zimmermann's shrew. This shrew was origi- skull of Tunisian origin to C. suaveolens. Because nally described as a subspecies of C. russula. of the uncertain taxonomic value of teeth charac- Based on morphological criteria, Vesmanis and ters, a cytogenetic investigation of Crocidura of Kahmann (1978) raised this taxon to species rank. the North African région is needed. The validity of this interprétation was confirmed Populations of the Near East still présent a tax- by the particular karyotype (Vogel 1986). Fossils onomic problem. Russian authors (Gureev 1971, of this species, together with others of Kritimys, Tembotova 1983, Grafodatskii et al. 1988) con- have been found in karst fissures infilled with sider them as a separate species, C. gueldenstaedtii Pleistocene sédiments (Reumer 1986). To day, this (Pallas, 1811). Their interprétation is based on shrew is not known from anywhere outside Crète morphological variations, whereas the karyotype is and it is therefore considered endémie to this is- absolutely identical to that of C. suaveolens land. Its numerical dominance in the mountains (Catzeflis et al. 1985, Tembotova 1987, Grafodat- and its absence in the fertile plains of the island skii et al. 1988). Considering the interfertility be- (Vogel et al. 1986, Pieper in press) are probably tween suaveolens and gueldenstaedtii (Catzeflis et the conséquence of direct compétition with the in- al. 1985), the absence of sympatry (Zaitsev in litt.) vading C. suaveolens. and their close biochemical relationship (Mad- dalena 1990), we include ail thèse populations in the species C. suaveolens. CONCLUSIONS The présence of C. suaveolens on the following islands was confirmed by cytotaxonomy : Cyprus and Lesbos (Catzeflis 1983, Catzeflis et al. 1985), Thanks to cytogenetic methods, the systematic Corsica (Catalan 1984, Poitevin et al. 1986), status of the shrews of many Mediterranean is- Minorca (Catalan et al. 1988), Crète (Vogel et al. lands has now been clarified. This has not been 1986). In ail cases this species was most probably without surprising results. In some cases, previous introduced by man. In the case of Crète this was morphological interprétations have been con- most probably during the Minoan period, about firmed, e.g. that of Vesmanis and Kahmann (1978) l'500 BC (Reumer and Payne 1986). The bio- concerning Zimmermann's shrew, at the same time chemical similarity of Cretan populations with resolving such complex problems as the uncertain those from Turkey reveals the origin of this island interprétation of Miller's type spécimens from Sic- population (Vogel et al. 1986). On Minorca C. ily. In other cases, previous morphological inter- suaveolens arrived about 200 BC (Vigne and Al- prétations have been shown to be wrong as, for cover 1985). On Corsica its présence was at first example, those of ail former authors dealing with documented only from the Middle Ages (Vigne the shrews of Gozo. The présent state of our and Alcover 1985), however new findings provide knowledge gives a solid basis for further zoogeo- évidence of a much earlier introduction (Vigne and graphical investigations which, sustained by bio- Marinval-Vigne, in press). chemical techniques, can help to détermine the genetic relationship between populations and thus, together with palaeontology and archaeology, allow a reconstruction of the exciting history of Crocidura sicula Miller, 1901 island colonization.

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VIGNE J.D. & M.C. MARINVAL-VIGNE, 1990. Nou- VOGEL P., T. MADDALENA & F. CATZEFLIS, 1986. velles données sur l'histoire des Insectivores Sori- A contribution to the taxonomy and ecology of cidés en Corse. Vie Milieu 40 (2/3). shrews (Crocidura zimmermanni and C. suaveolens) VOGEL P., 1986. Der Karyotyp der Kretaspitzmaus from Crète and Turkey. Acta Theriol. 31 : 537-545. Crocidura zimmermanni Wettstein, 1953 (Mammalia, VOGEL P. & T. MADDALENA, 1987. Note sur la rép- Insectivora). Bonn. zool. Beitr. 37 : 35-38. artition altitudinale et la fréquence de la musaraigne VOGEL P., 1988. Taxonomical and biogeographical musette (Crocidura russula yebalensis) au Maroc. problems in Mediterranean shrews of the genus Mammalia 51 : 465-467. Crocidura (Mammalia, Insectivora) with référence to WETTSTEIN O., 1953. Die Insectivora von Kreta. Z. a new karyotype from Sicily (Italy). Bull. Soc. vaud. Sàugetierk. 17 : 4-13. Sci. nat. 79 : 39-48. VOGEL P., R. HUTTERER & M. SARA, 1989. The cor- rect name, species diagnosis and distribution of the Reçu le 14 novembre 1989; received November 14, 1989 Sicilian shrew. Bonn. zool. Beitr. 40 : 243-248. Accepté le 12 janvier 1990; accepted January 12, 1990