Rediscovery of the critically endangered Nelson's

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Rediscovery of the critically endangered Nelson’s small-eared shrew (Cryptotis nelsoni), endemic to Volcań San Martıń, Eastern Me´xico Fernando A. Cervantesa,, La´zaro Guevaraa,b a

Departamento de Zoologia, Instituto de Biologia, Universidad Nacional Autońoma de Me´xico, Apartado Postal 70-153, Me´xico, Distrito Federal 04510, Me´xico b Facultad de Ciencias Biolo´gicas y Agropecuarias, Universidad Veracruzana, Apartado Postal 177, Co´rdoba, Veracruz, 94952, Me´xico Received 27 May 2009; accepted 10 June 2009

Keywords: Rediscovery; Shrews; Soricomorpha; Cloud forest; Me´xico

A series of 12 shrews was collected in May 1894 by Edward W. Nelson and Edward A. Goldman on Volcań San Martıń Tuxtla, Veracruz, Me´xico, at 4,800 feet. A year later, C. Hart Merriam described these specimens as a new species, Blarina nelsoni (Merriam 1895). The holotype (skin and skull, USNM 65437), a subadult female, was deposited along with the entire series at the National Museum of Natural History in Washington, D.C. Merriam (1895) reported that this shrew was known only from the isolated volcano of Tuxtla, and that was common in the forest on the mountain ranging up to the extreme summit at 5,400 feet. This species was later transferred to the genus Cryptotis as C. nelsoni by Miller (1912); Choate (1970) treated it as a distinctive subspecies of C. mexicana-C. mexicana nelsoni and named the type locality as ‘‘Volcań San Martıń’’. Recently, Woodman and Timm (1999) recognized Nelson’s small-eared shrew as a distinctive species, C. nelsoni, after examination of the 12 known museum specimens, and Carraway (2007) concurred with this taxonomic status. Choate (1970) after extensive review of all specimens of Middle American Cryptotis in the world’s collections stated that no specimens of C. m. nelsoni had been obtained since the original series Corresponding author. Tel.: +52 55 5622 9067; fax:+52 55 5550 3639. E-mail address: [email protected] (F.A. Cervantes).

collected by Nelson and Goldman in 1894. Since 1895, all subsequent publications discussing this shrew, other than recopilations or list of species, always cite the original description by Merriam (1895). The biology of this shrew is essentially unknown, and it was even thought that it might be extinct. Recently, our field party from the Instituto de Biologıá, UNAM (Universidad Nacional Autońoma de Me´xico) working on inventories of mammals in the tropical region of Los Tuxtlas, in eastern Veracruz, Me´xico, actively searched for and rediscovered C. nelsoni in 2003. Thus, 109 years after the first published record we can reconfirm that Nelson’s small-eared shrew continues to occur in the same forested region where the species was first discovered. We were fortunate to obtain C. nelsoni at three localities in the vicinity of the type locality reported by Merriam (1895). They are: Volcań San Martıń Tuxtla, Ejido Campeche, 11-11.5 km N San Andre´s Tuxtla, Municipio San Andre´s Tuxtla, Veracruz, Me´xico, 1,300, 1395, and 1,500 m above sea level, 181320 5200 N, 951110 3000 W, 181330 1500 N, 951110 3000 W, and 181330 0400 N, 951110 4300 W, respectively (Fig. 1). These localities lie on the south face of the volcano and just to the northwest of the nearby Lago Catemaco (Catemaco Lake). We used 1-liter capacity pitfall traps to catch shrews over four nights during three trips between November 2003 and March 2004; we set 100 traps a night,

1616-5047/$ - see front matter r 2009 Published by Elsevier GmbH on behalf of Deutsche Gesellschaft fu¨r Saügetierkunde. doi:10.1016/j.mambio.2009.06.002 Mamm. biol. 75 (2010) 451–454

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Fig. 1. Geographical distribution of the Nelson’s small-eared shrew (Cryptotis nelsoni) in the forested midlands of Volcań San Martıń Tuxtla, Municipio San Andre´s Tuxtla, Veracruz, Me´xico (modified from Woodman et al. 2008). The arrow points to the Volcań San Martıń Tuxtla, in eastern Me´xico.

therefore, making a total of 400 a trip. Specimens obtained in the pitfall traps were preserved as conventional museum specimens-skin, skeleton, and tissue samples. No other small mammal species was caught in the pitfall traps, nor were any other shrew species discovered in the same habitat as C. nelsoni. The taxonomic identity was confirmed as Cryptotis nelsoni using several literature sources (Choate 1970; Hall 1981; Carraway 2007; Woodman and Timm 1999) and direct comparison with other shrew species. All specimens are catalogued in the Mexican National Collection of Mammals [Coleccioń Nacional de Mamı´feros (CNMA), Instituto de Biologıá] of Universidad Nacional Autońoma de Me´xico, in Me´xico City. To determine the age of the specimens, we examined teeth and cranial sutures following Choate (1970). The specimens include one adult male, one male juvenile, and one female adult (# CNMA 41982, # CNMA 42000, ~ CNMA 41975). Their body measurements (mm), total length, vertebral tail length, right hindfoot length, ear length, and weigh (g) (respectively) are: 97, 29, 12, 3, 9; 95, 28, 12, 3, 7; 92, 23, 13, 2, 8; their cranial measurements are, respectively: condylobasal length, 19.1, ?, 19.4; palatal length, 7.9, 7.8, 7.9; maxillary breadth, 6.8, 6.6, 6.7; interorbital breadth,

5.0, 4.9, 5.0; length of maxillary toothrow, 7.3, 7.3, 81 6.9; cranial breadth, 10.3, ?, 10.6; length of M2, 1.6, 1.5, 1.5. These measurements are similar to the values (mm) reported for the holotype (total length, 110; length of tail, 31; length of hind foot, 14; condylobasal length 19.8; palatal length, 8.4; maxillary breadth, 6.8, interorbital breadth, 5.3; length of maxillary toothrow, 7.4; cranial breadth, 10.7; length of M2, 1.6), and are larger than those for C. mexicana (Choate 1970). The specimens also display characters of C. nelsoni reported previously (Merriam 1895; Choate 1970). The pelage is uniform sooty brown (Fig. 2), resulting in a slightly darker pelage than C. mexicana. The skull of C. nelsoni is larger and heavier than that of C. mexicana. Similarly, the braincase is larger and flatter, and their interpterygoid fossa broader than those of C. mexicana (Fig. 3). The habitat reported by Merriam (1895) for the holotype and paratypes was evergreen tropical forest, represented by well-conserved vegetation that consisted of areas covered by layers of volcanic sand and ashes and trees of large size (Choate 1970; Goldman 1951). The vegetation where our specimens were obtained was cloud forest. In one of the three localities sampled (elevation 1,500 m), the trees of the canopy were


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Fig. 2. Male adult (CNMA 41982) of the Nelson’s small-eared shrew (Cryptotis nelsoni) collected on 13 February 2004 in Volcań San Martıń Tuxtla, Ejido Campeche, 11 km N San Andre´s Tuxtla, Municipio San Andre´s Tuxtla, Veracruz, Me´xico, 1,300 m above sea level (Photograph by La´zaro Guevara).

unusually low, and local people call this vegetation ‘‘bosque enano’’ (dwarf forest). The vegetation of the volcano is a gradient where, from the lowest to the higher elevations, it includes coastal vegetation, evergreen tropical forest, cloud forest, and deciduous ´ lvarez del Castillo 1977). tropical forest (A The geographical location and the habitat of our specimens confirms that the range of C. nelsoni is extremely small and the species is restricted to the isolated Volcań San Martıń, located at the northern end of the range of mountains at present named Sierra de Los Tuxtlas, in eastern Veracruz. According to Choate (1970), ca. 120 km of tropical scrub forest and savannas not suited ecologically for C. nelsoni prevent this species from contacting C. mexicana further west. It was hypothesized earlier that this shrew probably occurs in suitable habitats throughout that Sierra (Choate 1970). However, a recent study on the mammalian diversity of Sierra de Santa Martha, Veracruz ( ¼ Sierra de los Tuxtlas excluding Volcań San Martıń), did not record the presence of C. nelsoni (Gonza´lez Christen 2008). Therefore, our recent research allows us to document that C. nelsoni is a highly endemic species of the specious shrew genus Cryptotis. The specimens of C. nelsoni collected in this research are, to our knowledge, the only specimens obtained after

Fig. 3. Ventral, dorsal, and lateral views of cranium and mandible of an adult female Nelson’s small-eared shrew (Cryptotis nelsoni) from Volcań San Martıń Tuxtla, Ejido Campeche, 11.5 km N San Andre´s Tuxtla, Municipio San Andre´s Tuxtla, Veracruz, Me´xico, 1,500 m above sea level (CNMA 41975). Condylobasal length is 19.4 mm (Photographs by Susana Guzmań).

the type series was collected, 109 years ago. Furthermore, these specimens are topotypes since they were taken from the type locality of the species. Therefore, the rediscovery of this highly endemic mammal and the museum specimens confirms the existence and taxonomic status of this species and provides additional museum materials including complete skeletons and properly preserved genetic material to more fully document the distinctiveness and the systematic position of this species. It has recently been shown that the humeri and foreclaws are important characters in building phylogenetic trees to better understand the origin, evolution, and biogeography of small-eared shrews (Woodman and Timm 1999). After confirming

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that this unique shrew species still survives, our research team is studying its morphology and molecular systematics. The entire geographical distribution of C. nelsoni lies within a natural protected area, the ‘‘Reserva de la Bio´sfera Los Tuxtlas’’, a member of the UNESCO’s Man and the Biosphere (MAB) Network. However, C. nelsoni occurs in an extremely small area which is completely surrounded in the lowlands and by a high density of human settlements. The use of the land within the Reserve frequently involves logging, cattle grazing, induced fires, and crops. Consequently, the habitat of C. nelsoni is gradually changing or disappearing. According to the standards of the International Union for the Conservation of Nature and Natural Resources (IUCN) criteria, this endemic shrew is correctly listed as critically endangered since it occurs in only one location in a range of less than 100 km2, and its habitat is shrinking (Woodman et al. 2008). In fact, C. nelsoni is the only species of the genus (ca. 30 species) ranked in the highest level of extinction risk (Hutterer 2005). Similarly, this species, under the spelling Cryptotis mexicana nelsoni, is listed as ‘‘sujeta a proteccioń especial’’ (‘‘under special protection’’) by the Mexican government (Luiselli Fernańdez 2002) since C. nelsoni displays a potential small distributional range occurring only on a small forested volcano. The addition of C. nelsoni to the mammal list of Mexican protected species is critically important because the genus Cryptotis is the most diverse genus of shrews in Me´xico with 14 taxa (Carraway 2007), including C. nelsoni. A specific conservation action plan is needed in order to buffer and eventually halt alterations of its habitat and protect the integrity of the populations of C. nelsoni. This should be worked out along and in agreement with the management plan of the Reserve. Since there is a continuing decline in the extent and quality of its habitat (Woodman et al. 2008), local people, government agencies, public institutions, and private organizations must work together and focus their join efforts in the conservation of the ecosystems of Volcań San Martıń. The finding of C. nelsoni and the evidence documented through museum specimens should assist government offices in charge of environmental policies to protect and conserve wild mammals and habitats in the region.

Acknowledgements We thank C. Absalon, A. Arango, F. Ponce, N. Ramı´rez, S. Ramı´rez, and J. Vargas for invaluable field and curatorial assistance. The Protected Natural Areas office of the Mexican government granted authorization

to collect within the grounds of ‘‘Reserva de la Bio´sfera Los Tuxtlas’’ under the collecting permit FAUT 0002 issued by the Mexican Ministery of the Environment to Cervantes. IUCN granted permission to reprint the distribution map of C. nelsoni. S. Guzmań prepared photographs of the skull of C. nelsoni. Editorial suggestions by two anonymous reviewers improved this manuscript. We dedicate this paper to Jerry R. Choate, mammalogist, teacher, and friend, for his important research contributions to Mesoamerican shrews.

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