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Microscopic anatomy of the desert shrew, Notiosorex C. Crawfordi.


Two male desert shrews, Notiosorex c. crawfordi (Coues), representing two localities from the Central Desert, Valle de los Cirios, of Baja California, Mexico, were studied by light microscopic techniques to delineate baseline morphological criteria. The specimens were made into study skins in the field which eliminated the skulls and skins for possible study by microscopic techniques. A general survey was made of the major organ systems: muscular, skeletal and body wall; hematopoetic; central nervous; gastrointestinal; genito-urinary; endocrine; cardiovascular and respiratory. The presence of shoulder glands is described although their function is not known. The animals were parasitized by tapeworms (Cestoda: Hymenolepididae) and nematodes (Nemata).

Key words: Desert shrew, Notiosorex c. crawfordi, anatomy, Baja California, Mexico, Central Desert, Valle de los Cirios


Dos machos de la musarana deserticola, Notiosorex c. crawfordi (Coues), representando dos Iocalidades del Desierto Central, Valle de los Cirios, de Baja California, Mexico, se estudiaron por las tecnicas microscopicas delinear la base criterio morfologico. Las pieles del estudio de los ejemplares se hicieron en el campo; este elimino los craneos y las pieles de la posibilidad de estudiar con las tecnicas microscopicas. Una inspeccion general se hizo de los sistemas de los organos mayores: el muscular, esqueleto y la pared del cuerpo; el hematopoetico; el nervioso central; el gastrointestinal; el genito-urinario; el endocrino; el cardiovascular; y el respiratorio. La presencia de las glandulas del hombro se describe aunque su funcion no es cococida. Las Iombarices solitarias (Cestoda: Hymenolepididae) y nematodes (Nemata) fueron parasitos de los animales.


We could find little literature references concerning the microscopic anatomy of shrews. In their detailed review of Notiosorex c. crawfordi (Coues) Armstrong and Jones (1972) reported little concerning the microscopic anatomy of the species and stated "The post-cranial skeleton of N. crawfordi has not been studied in detail."

Merritt et al. (1994) provide a good review of the biology of shrews on a worldwide basis and include a few chapters relating to shrew microanatomy (Carson et al. 1994, Foresman 1994, and Hyvarinen 1994). Rose (1994) briefly reviews reasons that studies of shrew anatomy can be potentially rewarding. Laakkonen et al. (2001) provide some of the most current biological information related to N. crawfordi in an adjacent region (southern California).

We could find no literature concerning the microscopic anatomy relating to that of the desert shrew. For this reason we report our findings on the microscopic anatomy of these desert shrew specimens. This paper is part of ongoing research in the Central Desert (Valle de los Cirios Natural Protected Area) by the Orma J. Smith Museum of Natural History, The College of Idaho.

The two collections of N. c. crawfordi represented range extensions to the south into the Central Desert, Valle de los Cirios (Armstrong and Jones 1972; Clark and Yensen 1982, Yensen and Clark 1986). The information increases our knowledge of both shrew anatomy and of this region of Baja California.


Two male desert (gray) shrews, N. c. crawfordi, were collected in the Central Desert (Valle de los Cirios) of Baja California, Mexico, in June 1981 (Clark and Yensen 1982 and Yensen and Clark 1986). The specimens were collected by the use of pitfall traps similar to those described by Clark and Blom (1992) except they contained no preservative. The two study sites are known as El Crucero and El Arco. The El Crucero site is located in a broad, sandy area and is described in several publications (Clark et al. 1985, 1989, and Clark and Ward 2000). The El Arco site is more volcanic in nature with similar vegetation plus the addition of Yucca valida.

The specimens were skinned and decapitated and the bodies fixed in 10% buffered formalin in the field. We preserved the bodies for examination of microscopic characteristics in the laboratory. We examined them by light microscopic techniques to delineate baseline morphological criteria, for purposes of comparison to other species still under study. Because of their small size, no attempts were made at detailed dissection. Each animal was serially cross-sectioned at 2-3mm intervals, into twelve blocks and completely embedded. The blocks were decalcified to improve sectioning. The sections were stained with hexatoxylin and eosin (H and E), periodic acid Schiff (PAS) and with Masson's trichrome. The sections were discarded following study and photography.

The specimen data and voucher specimen locations are as follows: Orma J. Smith Museum of Natural History, The College of Idaho, Caldwell #98 (field # EY319), 3.2km S. El Arco, Lat. 28[degrees]00'N, Long. 113[degrees]23'W, elevation 240m, 24 June 1981, 83-29-10-9=3.2, right testis 5x2.5, E. Yensen and W.H. Clark; Instituto de Biologia, Departamento de Zoologia, Universidad Nacional Autonoma, Mexico City (field # EY338), El Crucero, Lat. 29[degrees]16'N, Long. 114[degrees]09'W, elevation 610m, 30 June 1981, 86-29-9-7=2.6, right testis 4x3, left testis 3x3, E. Yensen and W.H. Clark. The length of the bodies studied is as follows: EY319--total length 83mm, tail 29mm (head + body = 54mm); and EY338--total length 86mm, tail 29mm (head + body = 57mm).


The results of the microscopic examination of the specimens were as follows:

MUSCULAR SKELETAL SYSTEM AND BODY WALL. The muscle bundles were tightly packed with little intervening stroma, except for interposed thick layers of brown, multilocular, "hibernating" fat, predominantly on the back. In EY338 there was a well-preserved, flat linear shoulder gland (Fig. 1) consisting of tightly clustered, well-defined, acinar structures, arranged around prominent ducts (Fig. 2). The acini were lined by a single layer of plump, cuboidal cells with a centrally positioned, round to oval nucleus, surrounded by uniformly granular cytoplasm. The cytoplasm shows minimal affinity for PAS. In the same animal, an anterior paramedian glandular structure was located, recognizable as a salivary gland (Fig. 3). There was a mixed pattern of both mucinous and serous acini, the latter showing a strong PAS positivity (Fig. 4). The bony structures, including the vertebral bodies and spines, and tail, consist of delicate, trabecular bone, honeycombed with hematopoetic marrow.

HEMATOPOETIC SYSTEM. There was a ubiquitous hypercellularity of the bone marrow, consisting almost exclusively of cellular elements, with minimal stroma (Fig. 5). There was marked granulocytopoesis with a myeloid:erythroid ratio varying from 1:1 to 4:1. The thymus was located in the anterior mediastinum (Fig. 6) and consisted of ill-defined cortical and medullary zones (Fig. 7). In the cortex, the small dark thymocytes were tightly packed. In the medullary zones, there was an admixture of histiocytic cells and a looser arrangement of the various components (Fig. 8). No Hassel's bodies were identified. Lymph nodes were rarely encountered and usually consist of nodular aggregates of lymphocytic and histiocytic cells adjacent to fat (Fig. 9). Cortical and medullary demarcations or distinct follicles or germinal centers were not readily evident. The spleen in both animals consisted of a crescent-shaped organ with tightly packed lymphocytes (Fig. 10). Well-defined follicular structures and multiple megakaryocytes were also found (Fig. 11).





CENTRAL NERVOUS SYSTEM (SPINAL CORD). Multiple cross sections at various levels showed well-defined dorsal and ventral horns, containing large numbers of ganglion cells (Fig. 12). The dorsal and ventral nerve roots were well established as was the paravertebral ganglion chain (Fig.13). In none of the cross sections was a clear-cut central canal.

GASTROINTESTINAL SYSTEM. The esophagus was lined by plump squamous cells four to six layers thick (Fig. 14). There was an inconsistent granular layer, but no frank keratinization. The mucosa was supported by a scanty, delicate submucosa and a three-layered muscularis. The stomach was lined by an elaborately plicated, glandular mucosa and was partially filled with digested vegetable and chitinous material. The mucosal glands were tubular, straight, and abound in both chief and parietal cells (Fig. 15). The gastroesophageal and gastroduodenal junctions showed smooth transition between typical epithelial types (Figs. 14 and 15). The duodenum was characterized by clusters of Brunner's glands. The small intestine mucosa was extensively autolytic. No ileocecal junction was identified in either animal.





Both animals had intestinal parasites. In one EY338, a cross section of the intestine revealed a nematode (Nemata). Another view of the same shrew intestine specimen, serial sectioning cut a tapeworm longitudinally, showing typical segmentation (Cestoda: Hymenolepididae) (Fig.18). No eggs were noted in the surrounding stool.

The pancreas lay in close association with the left kidney, adrenal gland, and spleen with little intervening stroma. The pancreatic tissue was characterized by tightly packed, PAS+, acinar structures. Scattered clusters of pale, uniform, large, hexagonal cells representing the islets of Langerhan's were identified.

The liver examined was typically mammalian. The periportal areas, generally devoid of stroma, were identified by the presence of a large, dilated vessel and a small bile duct (Fig. 20). The hepatic parenchyma was composed of well-preserved, eosinophilic, cuboidal hepatocytes, arranged in cords one to two cells thick, radiating from a congested central vein (Fig. 21). Both specimens had a gallbladder-like structure, consisting of a hollow organ with an elaborately plicated mucosa, lined by a single layer of tall columnar cells. No bile pigment was found (Fig. 22).





GENITO-URINARY SYSTEM. The kidney was a unipapillary structure capped by a uniform cortex. The cortices were composed predominantly of tightly packed tubular structures, often lying back to back with little interposed stroma (Fig. 23). The glomeruli were small, measuring approximately one and a half times the diameter of the large proximal tubulus. The glomeruli appear to be more concentrated in the mid-cortex, where the estimated tubular:glomerular ratio was approximately 12:1. Each glomerulus was associated with a prominent macula densa (Fig. 24). As expected, within the pelvic cavity, intra-abdominal testes, epididymis, spermatic vesicles, prostrate glands and bladder were evident (Fig. 25). The seminiferous tubules showed active spermatogenesis and prominent clusters of interstitial cells (Fig. 26). Adjacent to the testis was a large, prominent, epididymis with dilated tubules, eosinophilic granular secretion, and varying numbers of spermatozoa (Fig. 27). The prostatic gland (Fig. 28) was Iobulated and characterized by tightly packed tubules with papillary fronds projecting into the lumen. Occasional myoepithelial cells were also identified. The bladder was composed of circumferential, smooth muscle layers, supporting a plicated transitional epithium four to six cells thick.





ENDOCRINE SYSTEM. The adrenal gland was roughly circular in cross section and shows a well-developed cortex and medulla (Fig. 29). Within the cortex three layers were identified: a thin, inner, zona reticularis, composed of small dark cells; a broad central zone, approximately 90% of the thickness the zona fasciculata, consisting of large cuboidal cells; and a thin outer glomerulosa.





CARDIOVASCULAR SYSTEM. The heart had a well-developed muscular syncytium and four chambers, which was characteristic of the mammals. The "cardiac skeleton" consists of minimal amounts of loose connective tissue without development of a central fibrous body. A cross section through the aortic valve and pulmonary trunk was noted in one animal (EY338) (Fig. 30).

RESPIRATORY SYSTEM. Cartilagenous rings were found only in the midline and hilar structures (Fig. 31). The intrapulmonary airway system contained bronchioles (smooth muscle without cartilage), which split into two or three generations before reaching the level of the terminal bronchiole (Fig. 31). From there they underwent three to four generations of branching before reaching the alveolar structures (Figs. 33 and 34). The alveolar ducts lay within 1mm of the pleural surface where they branched into alveolar structures. The septa consisted of delicate capillary structures and widely-spaced pneumocytes. Throughout the lung were prominent perivascular and peribronchiolar lymphocytic and plasmacytic infiltrates (bronchiolar associated lymphoid tissue or BALT). The pulmonary vasculature tended to be markedly engorged. Occasional septal and alveolar hemorrhages were evident.






The microscopic fabric of the thoracic and abdominal organs of the male desert shrew, Notiosorex c. crawfordi, as expected, had features comparable to other mammalian species (Altschuler et al. 1979; Carleton 1973, 1980, and 1981; Chiasson 1980; Davis and Golley 1963; Klingener 1968; McLaughlin and Chiasson 1979; Thorpe 1968 and Wells 1964). Carson et al. (1994) presented ultrastructure of the olfactory epithelium (not available for study in our specimens) of the short-tailed shrew. Foresman (1994) gave comparative embryonic information of the Sorcidae through the examination of female specimens.





There was a remarkable economy of tissue organization in the two male specimens of the desert shrew. The organs were composed of the maximal amount of parenchyma and an absolute minimum of stroma (Fig. 35). There was recruitment of every available bony structure, including the tail, for hematopoesis. The fat layers were exclusively of the brown, multiocular type, high in unsaturated fats, commonly seen in hibernating animals and rodents (Leake 1976, and Hyvarinen 1994). The desert shrew may not hibernate, since Laakkonen et al. (2001) found them active year round in southern California and found that minimum temperatures did not have a significant effect on capture. The species is capable of entering a state of torpor (Allen 2000).

The shoulder glands show histological characteristics of other pure serous-type glands such as pancreas and parotid. The histological and staining Characteristics were distinctly different from the mixed salivary gland. The parotid gland was not available for comparison and, so, the exact nature of the shoulder gland remains obscure, although it may represent a modified sweat gland rather than a digestive organ, because of the poor affinity for glycogen (PAS). Hoffmiester and Goodpaster (1962) described skin glands (average 5.5x4mm in external size), situated posteriorly in N. crawfordi males, which, they termed "lateral skin gland" and these authors postulated no function for the lateral skin glands. It is not known if the "shoulder glands" were distinct entities, or anterior "lateral glands." Lateral and ventral scent glands have been reported from the short-tailed shrew, Blarina brevicauda (Pearson 1946), and the salivary gland or glands of the shrew were described in Pearson (1942). Skin glands have been reported in other mammals such as Dipodomys (Quay 1953).





The apparent absence of a central canal in the spinal cord represents an interesting departure from the normal mammalian pattern. Further study is needed to rule out this being an anomaly or an artifact.




The renal morphology, with the predominance of tubules and prominent juxtaglomerular apparatus, is consistent with the adaption towards an arid habitat where the species lives and a necessity to produce highly concentrated urine. The active spermatogenesis in intra-abdominal testes is known from a wide variety of mammals including monotremes and some insectivores, including shrews. According to Gunderson (1976) mammals in which testes are retained in the coelomic cavity have viable sperm at higher temperatures, or other mechanisms, unknown at present are in operation.

The components of the hematopoetic and immunological systems are all present, but show certain differences to other mammals; namely the persistence of the thymus (which might be related to the ages of the individuals since EY319 appears to be a young animal), poorly-differentiated lymph nodes, and the presence of extra medullary hematopoesis in the spleen. Within the lower gastrointestinal tract, no well-developed lymphoid tissues (Peyer's patches) were found. This may be due in part to the extensive autolytic changes. Within the lungs, however, there is a well-established bronchiolar associated lymphoid tissue (BALT).

The morphological features of the stomach suggest that it is a single-chambered, non-partitioned, cardiac pouch. The stomach is used exclusively as a digestive organ rather than a storage pouch for undigested food, as in the forestomach modification seen in desert rodents (Carlton 1973).

In both animals there was infestation by tapeworms (Cestoda, Hymenolepididae) and at least one by a nematode (Nemata). Literature concerning the parasitology of desert animals is scarce. Frandsen and Grundmann (1961); Barus et al. (1970); Rodenberg and Pence (1978); and Dubrovsky (1983) all listed tapeworm parasites for desert rodents. Fisher (1941) recorded a tapeworm, Raillietina, from the gut of a male desert shrew from Nevada. Haukisalmi et al. (1994) reported three groups of gastrointestinal helminthes (including Cestoda, Hymenolepididae as well as Nemata) from two Sorexspecies in Finnish Lapland.

Within both livers there was a large peripheral structure with morphological features suggestive of a gallbladder but with no demonstrable bile. This may be a gallbladder of a ductus choledochus as in rodents (Chiasson 1980).

These findings are meant to serve as a base line for further study of the desert shrew. Even though the sample size was limited and consisted of two males, the study provides the first such information on the desert (gray) shrew. In general, the desert shrew microscopic anatomy is typical of other desert mammals.


This research was supported, in part, by grants from EARTHWATCH and The Center for Field Research (WHC) of Watertown, MA. A.V. and P.E. Blom; R.D. Bratz (deceased); C.J., E.M., and M.E. Clark; S.D. Farley, M. Twitchell; D. Ward, Jr.; and E. Yensen provided assistance in the field. E. Yensen kindly read an earlier draft and provided valuable comments. Dr. R.S. Hoffmann examined the specimens and made the subspecific determinations. The Manter Laboratory of Parasitology, University of Nebraska, Lincoln, provided the parasite identifications. J. Luther provided the Spanish translation of the abstract and E. Clark assisted with preparation of the manuscript. R.L. Rausch assisted with the literature. We thank Josefina Antonia Zuniga (deceased) and Francisco Espinosa Quintero of Rancho Santa Ines for their hospitality during our fieldwork. B. Villa-R (deceased) gave assistance and encouragement throughout the study. C. Kapica and P.E. Blom offered encouragement and editorial assistance. C. Kapica scanned the figures from he original black and white photographs.


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Abraham Lincoln School of Medicine

University of Illinois

Chicago, Illinois 60612



Orma J. Smith Museum of Natural History

The College of Idaho

Caldwell, Idaho 83605-4494



Museo de Artropodos del CICESE

Departamento de Biologia de la Conservacion

Centro de Investigacion Cientifica y de Educacion Superior de Ensenada

Apado. Postal 2732 CP 22830, Ensenada, Baja California, Mexico

(1) Present address: 458 W Utley Road, Elmhurst IL 60126-3218 USA, (Former Clinical Assistant Professor Department of Pathology, Retired)

(2) Address all correspondence to: William H. Clark, Orma J. Smith Museum of Natural History, The College of Idaho, Caldwell, ID 83605 USA.
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Author:Ostrin, Samuel L.; Clark, William H.
Publication:Journal of the Idaho Academy of Science
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Date:Jun 1, 2010
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