Wednesday, August 7, 2019

[Mammalogy • 2018] Myotis crypticus & M. zenatius • Two New Cryptic Bat Species within the Myotis nattereri Species Complex (Vespertilionidae, Chiroptera) from the Western Palaearctic

Myotis crypticus 
Ruedi, Ibáñez, Salicini, Juste & Puechmaille

in Juste, Ruedi, Puechmaille, Salicini & Ibáñez, 2019. 

The Myotis nattereri species complex consists of an entangled group of Western Palaearctic bats characterized by fringing hairs along the rear edge of their uropatagium. Some members are relatively common while others are rare but all forms are morphologically very similar and their taxonomy is unresolved. Recent studies based on different molecular markers have shown that several major and unexpected lineages exist within this group of forest-dwelling bats. All the mitochondrial and nuclear markers tested to date have shown that these major lineages evolved as fully independent and coherent units and therefore each qualifies as distinct species. In the absence of proper morphological diagnosis, these lineages are informally referred to in the literature under different names. We explore here the external and craniodental variation of these lineages. Although all morphological measurements were overlapping between these lineages, we show that lineages can be completely discriminated in a multivariate morphometric space. Consistent with previous molecular reconstructions, these four major lineages represent two pairs of related species, each represented by a named species (Myotis nattereri s. str. and M. escalerai, respectively) and by unnamed forms (Myotis sp. A and Myotis sp. B, respectively). Herein we describe formally these two unnamed forms to clarify the taxonomy within this species complex. This new taxonomic view has important implication for the protection of these species, as three of the four taxa must now be considered as range-restricted species in need of conservation actions.

KEYWORDS: cryptic species, DNA, systematics, speciation, taxonomy

Myotis crypticus pictured on a swarming site from the Jura Mountains in the province of Vaud.

photo: Manuel Ruedi (Natural History Museum of Geneva)

Myotis crypticus sp. nov.
Ruedi, Ibáñez, Salicini, Juste and Puechmaille

Myotis nattereri (Kuhl, 1817): Miller (1912) (partim): Simmons (2005) (partim).
Myotis nattereri North Iberia (Kuhl, 1817): Ibáñez et al. (2006)
Myotis sp. (Mayer et al., 2007).
Myotis sp. A (García-Mudarra et al., 2009).
Myotis sp. A and Clade A (Salicini et al., 2011).
Myotis sp. A and M. sp A (Salicini et al., 2013).
Myotis sp. A and Myotis sp. C (Galimberti et al., 2012).
Myotis sp. A (Puechmaille et al., 2012): (Allegrini and Puechmaille, 2013).
M. nattereri 2 (Kuhl, 1817): Ruedi et al. (2013).
Myotis nattereri (Kuhl, 1817): Bogdanowicz et al. (2015).

Diagnosis: Externally, the combination of a long, S-shaped calcar without epiblema, very long and pointed tragus, smooth and unnotched rear edge of ears and presence of stiff hairs along the uropatagium margin distinguish M. crypticus sp. nov. and other members of the M. nattereri species complex from all remaining Eurasian Myotis taxa. The wing membrane insertion at the base of the toe (Fig. 4) as described by Puechmaille et al. (2012) and the pattern of curved nature of the stiff uropatagial hairs (Fig. 5) further distinguish M. crypticus sp. nov. from species related to the M. escalerai clade. The skull shape is very similar to that of M. nattereri s. str. but is relatively more slender in M. crypticus sp. nov., particularly the rostral and occipital regions, which seem narrower in the latter species (Fig. 3). Finally, numerous diagnostic mutations in both mitochondrial and nuclear sequences clearly support the uniqueness of M. crypticus sp. nov. compared to any other species in this group.

Etymology: The epithet crypticus is derived from the Greek ‘kryptos’, which means hidden or concealed, in reference to this species' long history of remaining undetected.

Proposed vernacular names: Kryptisches Mausohr (German), cryptic myotis (English), murin cryptique (French), murciélago ratonero críptico (Spanish).

Distribution: Animals identified as M. crypticus sp. nov. based on molecular characters were recorded in mountain areas of provinces of central and northern Spain (Salicini et al., 2011), southern France (Salicini et al., 2011; Puechmaille et al., 2012), across the Italian Peninsula (Salicini et al., 2011; Galimberti et al., 2012) and probably to the adjacent southwestern parts of Austria (Mayer et al., 2007). Based on nuclear genetic markers (unpublished data), marginal areas to the north and west of the Alps, e.g. in western Switzerland or Rhône-Alpes (France), are also occupied by M. crypticus sp. nov. However, the northern and eastern limits of the distribution of M. crypticus sp. nov. notably in relation to the occurrence of M. nattereri s. str., are unknown. Furthermore, as the populations from Sicily and southern Italy show important genetic discontinuities (Salicini et al., 2013; Bogdanowicz et al., 2015), they deserve further scrutiny as they might present further taxonomic complexity.

Myotis zenatius sp. nov.
Ibáñez, Juste, Salicini, Puechmaille and Ruedi

Myotis nattereri (Kuhl, 1817): Brosset (1963): Gaisler (1983): Gaisler (1983–1984): Horáček and Hanák (1984) (partim): Kowalski et al. (1986): Aulagnier and Thevenot (1986): Kowalski and Rzebik-Kowalska (1991).
Myotis nattereri (Kuhl, 1817): Horáček et al. (2000) (partim): Benda et al. (2004): Simmons (2005) (partim): Dieuleveut et al. (2010).
Myotis sp. B (García-Mudarra et al., 2009):  (Puechmaille et al., 2012).
Myotis sp. B and Clade B (Salicini et al., 2011).
Myotis sp. B and Clade B (Salicini et al., 2013).

Diagnosis: Externally, M. zenatius sp. nov. shares all the char acters previously referred to for M. crypticus sp. nov. that distinguish this and the other members of the M. nattereri complex from all remaining European Myotis taxa. The wing membrane is inserted in the mid-metatarsus (Fig. 4) as in M. escalerai but contrary to M. crypticus sp. nov. and M. nattereri s. str. that have the wing membrane inserted at the base of the toe (Puechmaille et al., 2012). This character was first used by Cabrera (1904) in the original description of M. escalerai and later validated by Puechmaille et al. (2012). Similarly, the characteristic stiff fringing hairs bordering the tail membrane show the same distinct pattern described for M. escalerai by Agirre-Mendi and Ibáñez (2012); accordingly, the hairy edge of this membrane looks thicker than in M. nattereri and M. crypticus sp. nov. due to the presence of an additional line of relatively long and conspicuous stiff hairs facing inwards (Fig. 5). The sharing of these two morphological characters between M. escalerai and M. zenatius sp. nov. is in agreement with their phylogenetic relationships, which place them as sister species, while they are distinct from M. nattereri s. str. and M. crypticus sp. nov. Nevertheless, the darker and more greyish dorsal fur colour in adult M. ze natius sp. nov. (resembling a juvenile coloration in other Myotis species) distinguishes the new species from adult M. escalerai. Again, the skull morphology is very similar between M. zena tius sp. nov. and M. escalerai, but is in general more delicate in the new species and slightly smaller in all dimensions (as previously described by Benda et al., 2006), except for the postorbital constriction which is wider in M. zenatius sp. nov. (Table 2). The braincase is also relatively broader and more globose in the new species than in M. escalerai).

Etymology: The epithet zenatius is derived from the word ‘Zanatah’ which refers to a little known Berber tribe that lived in the Maghreb region of North Africa in the Middle Ages. The Zanatah people were famous for their horse riding skills and mobility.

Proposed vernacular names: Zenati Mausohr (German), Zenati myotis (English), murin Zenati (French), murcielago ratonero Zenate (Spanish).

Distribution: The species Myotis zenatius sp. nov. is probably endemic from the Mediterranean region of Morocco and Algeria, and possibly Tunisia. In Morocco it is very rare, known only from three localities in the central part and western coast (Benda et al., 2004), and from one locality in the hills of Rekkam, in the eastern part of the country (Dieuleveut et al., 2010). We add in this study three new localities (see  Supplementary Table S1 (01-AC-20-2-p-285–300_Supplement.pdf)) plus another one in Azrou (Ait-Sebaa) where six additional individuals were biopsied and released. In the Appendix of Salicini et al. (2013), the species is wrongly mentioned from Errachidia. The mistake stems from the switching between the similar names of two caves, Kef Azigza (near Errachidia) where M. zenatius sp. nov. does not occur, and Kef Aïssa (the correct locality). The species is thus rare but widely distributed across Morocco from the northern slopes of the Riff (near Tetouan) to the dry mountains of the Great Atlas (e.g. Wintimdouine Cave). The Atlas Mountains apparently delineate two distinct haplogroups (Salicini et al., 2013) that may represent distinct subpopulations. We can assume that the Algerian populations previously classified as M. nattereri (see e.g., Ko wal ski and Rzebik-Kowalska, 1991) represent M. ze natius sp. nov., given that the distance between the easternmost known locality from Morocco (Rekkam Hills — Dieuleveut et al., 2010) is only around 200 km far from the westernmost known locality from Algeria (near Tlemcen — Kowalski et al., 1986). The new species occurs in the northern parts of Algeria, where it is known only from three localities (Kowalski and Rzebik-Kowalska, 1991; Ahmim, 2017). As no specimen from this country has been analysed genetically, it is however unknown to which extent these represent interconnected or isolated subpopulations.

Natural history: 
Very little is known about this species, which is one of the rarest bats in the Mediterranean. As most identified individuals were captured at cave roosts, including breeding females from nursery colonies, it shares with M. escalerai troglophilous habits through out the year. Such strong cave-dwelling habits mark a significant ecological contrast with the other two species (M. nattereri s. str. and M. crypticus sp. nov.), which roost preferably in tree holes during the summer. Furthermore, the maternity colonies of M. zenatius sp. nov. can reach up to 300 individuals (Kowalski et al., 1986; authors' unpublished data), which are distinctly larger than the tree-dwelling species.

  Javier Juste, Manuel Ruedi, Sébastien J. Puechmaille, Irene Salicini, and Carlos Ibáñez. 2019. Two New Cryptic Bat Species within the Myotis nattereri Species Complex (Vespertilionidae, Chiroptera) from the Western Palaearctic.  Acta Chiropterologica. 20(2); 285-300. DOI: 10.3161/15081109ACC2018.20.2.001