Distribution and Specificity of Helminths in Microtine Rodents: Evolutionary Implications

The taxonomic status of anoplocephaline cestodes of microtine rodents has been reviewed. Of the genus Andrya Railliet, 1883, five species are considered valid: A. macrocephala Douthitt, 1915; A. primordialis Douthitt, 1915; A. montana Kirshenblat, 1941 ; A. arctica Rausch, 1952; A. bairdi Schad, 1954. Of the genus Paranoplocephala Luehe, 1910, six species are regarded as valid: P. omphalodes (Hermann, 1783); P. blanchardi (Moniez, 1891); P. infrequens (Douthitt, 1915); P. variabilis (Douthitt, 1915); P. lemmi Rausch, 1952; P. neofibrinus Rausch, 1952. Andrya caucasica Kirshenblat, 1938, and A. bialowizensis Soltys, 1949, are regarded as synonyms of A. macrocephala. Paranoplocephala brevis Kirshenblat, 1938, is regarded as a synonym of P. infrequens. Three species, A. macrocephala, P. omphalodes, and P. infrequens, are holarctic in distribution, occurring mainly in species of Microtus. The uniformity of microtine rodents as hosts for various helminths has been discussed. It is concluded that Dicrostonyx is the most isolated genus from this standpoint, having two nematodes which have not been recorded from members of other genera, and harboring few helminths in common with others. This agrees with Hinton's conclusions, based on morphological characters of Dicrostonyx. From the present concept of Pleistocene glaciations, it is concluded that P. omphalodes and P. infrequens reached the St. Matthew Islands, in Bering Sea, as parasites of a vole from which Microtus abbreviatus has evolved. It appears that this vole arrived on these islands before North America was invaded, in the late Pleistocene, by the palearctic M. oeconomus and Clethrionomys rutilus,/i>. The present known distribution of P. omphalodes in North America corresponds about to that of M. oeconomus on the continent.

The Chromosomal Complement of the Yellow-Cheeked Vole

The karyotype of Microtus xanthognathus (Leach) is described, based on material from one female and one male vole. The diploid chromosomal number was found to be 54, and the fundamental number 62. The metacentric X-chromosome was of medium size and averaged 6.6% of the haploid complement. The designated Y-chromosome was near acrocentric. The specific distinction of M. xanthognathus and Microtus chrotorrhinus (Miller) was confirmed by the recognition of major differences in karyotype and differences in fundamental number. The distributional history of M. xanthognathus is briefly discussed.

Heligmosomoides johnsoni sp. nov. (Nematoda: Heligmosomatidae) from the Heather Vole, Phenacomys intermedius Merriam

Heligmosomoides johnsoni sp. noy. is described from the cecum of the heather vole, Phenacomys intermedius Merriam, from the Olympic Mountains, Washington. The absence of longitudinal cuticular ridges dorsally separates H. johnsoni from species of Heligmosomoides other than H. hudsoni (Cameron, 1937), which occurs in varying lemmings, Dicrostonyx spp., and from which H. johnsoni is distinguished by its longer spicules, form of the dorsal ray, and other characters. Both Phenacomys and Dicrostonyx have a specialized cecum, with long villi around which the nematodes are found tightly coiled. The zoogeography of heligmosomid nematodes in Phenacomys is briefly discussed. French abstract: On décrit Heligmosomoides johnsoni sp. nov. parasite du caecum du rongeur néarctique, Phenacomys intermedius Merriam, des Montagnes Olympiques de Washington. L'absence de crêtes cuticulaires sur la face dorsaIe sépare H. johnsoni des autres Heligmosomoides à I'exception d'H. hudsoni (Cameron, 1937) qui se trouve chez Dicrostonyx spp., et duquel H. johnsoni se distingue par ses spicules plus longs, par la forme différente de la côte dorsale et par d'autres caractères. Phenacomys et Dicrostonyx ont un caecum spécialisé, muni de villosités allongées, autour desquelles les nématodes s'enroulent étroitement. La zoogéographie des nematodes héligmosomes chez Phenacomys est discutée.

On the Ecology and Distribution of Echinococcus spp. (Cestoda: Taeniidae), and Characteristics of Their Development in the Intermediate Host. II. Comparative Studies on the Development of Larval E. multilocularis Leuckart, 1863, in the Intermediate Host

This paper reports the results of a comparative study of the development of the larval Echinococcus multilocularis Leuckart, 1863), and associated tissue reaction in naturally and experimentally infected mammals representing 31 species. The histogenesis of the larval cestode was traced in detail in arvicoline rodents of several species, and interspecific differences were defined. In arvicoline rodents, the developing larva exhibited host-specific characteristics within about a month after infection was established. The tissue reaction in Microtus oeconomus was characterized by the production of a large quantity of detritus around the larva, and by the formation of a thick epithelioid zone. In one subspecies, M. oeconomus innuitus, development of the larva was retarded, and the detrital mass was often calcified; in another, M. oeconomus operarius, the detritus rarely became calcified and the larva proliferated more rapidly. In M. pennsylvanicus, the tissue reaction was minimal, and little detritus was present. The characteristics of the tissue reaction in M. montebelli placed it in an intermediate position between the aforementioned species. In Clethrionomys rutilus, a thin epithelioid zone and an outer zone of loose collagenous fibers composed the adventitial layer; exogenous budding was retarded in this vole. A minimal tissue reaction occurred in Lagurus curtatus. In Lemmus spp., larger cysts were characteristic, but areas of small-cystic proliferation were always present. Similar differences in species or subspecies of Citellus and Dicrostonyx were described. Lesions of alveolar bydatid disease in man also were studied. The invasive growth of the larval cestode in the human liver involves a process comparable to small-cystic proliferation in the natural intermediate hosts. Although the later stages of development of the larval cestode are inhibited in man, exogenous proliferation of vesicles continues for the life of the host. The lesion in man was compared with a morphologically similar formation produced by anomalous development of the larval E. granulosus in the bovine liver. The latter is distinguished by the absence of areas of small-cystic proliferation. Non-echinococcal lesions found in the tissues studied, some of which resembled foci caused by the larval E. multilocularis, were briefly discussed.

Virus-Associated Tumours of the Harderian Gland in Laboratory-Reared Voles, Clethrionomys rutilis (Pallas)

Tumors of the Harderian gland occurred frequently in red-backed voles, Clethrionomys rutilus (Pallas), in a captive colony maintained since 1957. Although the tumors became obvious only in animals about a year old and older, early stage changes were histologically evident in glands from younger, clinically normal voles. The tumors ranged in type from poorly differentiated adenoma to adenocarcinoma, with invasion of adjacent tissues and characteristic deformation of the zygomata. Electron micrographs disclosed viral particles in the cytoplasm of glands from clinically normal animals as well as in glands showing malignant changes. The tumor was not observed in arvicoline rodents of other species maintained in the same rooms with the red-backed voles.

Description of Paranoplocephala etholeni n. sp. (Cestoda: Anoplocephalidae) in the Meadow Vole Microtus pennsylvanicus, with a Synopsis of Paranoplocehala s. l. in Holarctic Rodents

Paranoplocephala etholeni n. sp, parasitizing the meadow vole Microtus pennsylvanicus in Alaska and Wisconsin, USA. is described Paranaplocephala etholeni is morphologically most closely related to the Nearctic Paranoplocephala ondatrae (Rausch, 1948). Available data suggest that P. etholeni is a host-specific, locally rare species that may have a wide but sporadic geographical distribution in North America. The finding of P. ondatrae-like cestodes in Microtus spp. suggests that this poorly known species may actually be a parasite of voles rather than muskrat (type host). A tabular synopsis of all the known species of Paranoplocephala s. I. in the Holarctic region with their main morphological features is presented.

The Specific Status of the Narrow-Skulled Vole (Subgenus Stenocranius Kashchenko) in North America

On morphological and zoogeographical grounds, discussed in the present paper, it is concluded that the narrow-skulled vole in North America, previously designated Microtus (Stenocranius) miurus Osgood, is conspecific with the Eurasian M. (Stenocranius) gregalis Pallas. Fourteen subspecies in Eurasia and 5 in North America are now recognized, but it is probable that the number in Eurasia will be reduced through future investigation. The Eurasian subspecies of this vole comprise two major groups, of which one occupies the tundra zone and the other occurs across central Asia below latitude 60° N; their geographic ranges are largely separate but evidently become confluent in northeastern Siberia. The members of the northern group of Eurasian subspecies and the North American forms are closely related; the present distribution of the latter indicates post-glacial dispersal from the Amphiberingian Refugium. It is believed that the tundra-inhabiting voles in Eurasia likewise survived the Pleistocene glaciations in northern refugia, while the members of the southern group of subspecies probably represent populations that survived south of the limits of the continental glaciers. The ranges of the two Eurasian groups probably have become confluent during post-glacial time in northeastern Siberia as a result of the southward spread of the northern forms. At least, the subspecies having the intervening range closely resembles members of the northern group. Some of the ecological and ethological characteristics of these voles are briefly discussed. The chromosome number of one of the North American subspecies of narrow-skulled vole was determined to be 54; this is the first time that the chromosomes of a member of the subgenus Stenocranius have been investigated. A karyogram has been included. German abstract: Auf morphologischen und tiergeographischen Grundlagen, die in dieser Arbeit besprochen wurden, ist festgestellt worden, daß die schmalschädlige Wiihlmaus in Nordamerika, friiher Microtus (Stenocranius) miurus Osgood bezeichnet, mit der palaearktischen Art M. (Stenocranius) gregalis Pallas identisch ist. Zur Zeit gelten 14 Unterarten in Eurasien und 5 in Nordamerika als unterscheidbar; vermutlich aber wird die Zahl der palaearktischen Unterarten durch eingehendere Untersuchungen künftig vermindert werden. Auf Grund ihrer Verbreitung bilden die palaearktischen Unterarten zwei beinahe vollständig getrennte Gruppen. Die Wühlmäuse der nördlichen Gruppe bewohnen die Tundrazone, während die Vertreter der zweiten Gruppe über Mittelasien südlicher als 60° N.B. verbreitet sind. Die Verbreitungsgebiete der zwei Gruppen verbinden sich anscheinend. Die nordamerikanischen schmalschädligen Wühlmäuse sind mit den in der Tundrazone vorkommenden palaearktischen Formen nahe verwandt; sie haben sich wahrscheinlich während der Postglazialzeit aus dem Amphiberingschen Refugium verbreitet. Möglicherweise überlebten die tundrabewohnenden Wühlmäuse Eurasiens die Eiszeit ebenfalls in vereinzelten Refugien in Nordostsibirien, während die Formen der südlichen Gruppe sie jenseits der Grenzen des Festlandsgletschers überlebten. Wahrscheinlich wurden die zwei Verbreitungsgebiete dieser Art in Eurasien erst während der Postglazialzeit durch das Vordringen der nordischen Formen verbunden, da eine nähere Verwandtschaft zwischen den nördlichen und der dazwischenliegenden Unterart besteht. Einige ökologische und ethologische Eigentümlichkeiten dieser Wühlmäuse werden kurz besprochen. Es wurde festgestellt, daß eine der nordamerikanischen Unterarten der schmalschädligen Wühlmaus 54 Chromosomen hat; sie ist der einzige Vertreter der Untergattung Stenocranius, dessen Chromosomen untersucht worden sind.

Protein Hydrolysates Are Avoided by Herbivores but Not by Omnivores in Two-Choice Preference Tests

Background: The negative sensory properties of casein hydrolysates (HC) often limit their usage in products intended for human consumption, despite HC being nutritious and having many functional benefits. Recent, but taxonomically limited, evidence suggests that other animals also avoid consuming HC when alternatives exist. Methodology/Principal Findings: We evaluated ingestive responses of five herbivorous species (guinea pig, mountain beaver, gopher, vole, and rabbit) and five omnivorous species (rat, coyote, house mouse, white-footed mouse, and deer mouse; N = 16–18/species) using solid foods containing 20% HC in a series of two-choice preference tests that used a nonprotein, cellulose-based alternative. Individuals were also tested with collagen hydrolysate (gelatin; GE) to determine whether it would induce similar ingestive responses to those induced by HC. Despite HC and GE having very different nutritional and sensory qualities, both hydrolysates produced similar preference score patterns. We found that the herbivores generally avoided the hydrolysates while the omnivores consumed them at similar levels to the cellulose diet or, more rarely, preferred them (HC by the white-footed mouse; GE by the rat). Follow-up preference tests pairing HC and the nutritionally equivalent intact casein (C) were performed on the three mouse species and the guinea pigs. For the mice, mean HC preference scores were lower in the HC v C compared to the HC v Cel tests, indicating that HC’s sensory qualities negatively affected its consumption. However, responses were species-specific. For the guinea pigs, repeated exposure to HC or C (4.7-h sessions; N = 10) were found to increase subsequent HC preference scores in an HC v C preference test, which was interpreted in the light of conservative foraging strategies thought to typify herbivores. Conclusions/Significance: This is the first empirical study of dietary niche-related taxonomic differences in ingestive responses to protein hydrolysates using multiple species under comparable conditions. Our results provide a basis for future work in sensory, physiological, and behavioral mechanisms of hydrolysate avoidance and on the potential use of hydrolysates for pest management.

Notes on Microtine Rodents from the Brooks Range, Arctic Alaska

In connection with parasitological studies carried on during 1949 for the U.S. Public Health Service, the writer collected a considerable number of mammals from the northern edge of the "Endicott" section of the Brooks Range, in Arctic Alaska. The mammalian fauna of this region is poorly known, since apparently no previous collecting has been done here. About 200 microtine rodents were collected, mostly near Tolugak Lake (latitude 68° 24' N, longitude 151° 26' W), near the head of the Anaktuvuk River Valley. A few specimens were also taken at Umiat, on the Colville River, about 80 miles north of Tolugak Lake (latitude 69° 23' N, longitude 152° 10' W). Five species are represented: Clethrionomys rutilis dawsoni (Merriam), Microtus oeconomus macfarlani Merriam, Microtus miurus paneaki, n. subsp., Lemmus trimucronatus alascensis Merriam and Dicrostonyx groenlandicus rubricatus (Richardson). More complete details concerning their ecology and reproduction will be presented in a later paper, at which time the other mammals obtained will also be considered. The specimens have been deposited in the U.S. National Museum.

Dynamics of the Arctic Fox Population on St. Lawrence Island, Bering Sea

English abstract: We hypothesized that the arctic fox, Alopex lagopus (Linnaeus), population on St. Lawrence Island was cyclic and that its fluctuations in size. structure, and productivity were correlated with the relative size of the population of northern voles, Microtus oeconomus Pallas, the primary prey. Based on a nine-year study, we determined that the variations in size of the fox and vole populations were similar, but they both were of low amplitude and not closely correlated. The high pregnancy rate (mean, 86%/yr) and numbers of young conceived (mean, 11.5/pregnancy) did not vary significantly among years, probably because of the consistently abundant and diverse food supply available to the foxes. The age composition of the trappers' catch of foxes each winter also was comparatively stable, but it was closely correlated with the size of the vole population in the previous summer. The survival of the young foxes during the summer probably was dependent on the availability of the voles, The composition of the catch also appeared to be influenced by immigration of faxes from the adjacent continents via the pack ice. French abstract: Nous avons émis I'hypothèse que la population du renard arctique, Alopex lagopus (Linnaeus), sur I'île Saint Lawrence était cyclique el que les fluctuations concernant sa tailIe, sa structure et sa productivité étaient corrélées à la taille relative de la population du campagnol nordique. Microtus oeconomus Pallas, sa principale proie. En nous appuyant sur une étude menée sur neuf ans, nous avons déterminé que les variations dans la taille des populations du renard et du campagnol étaient semblables. mais que toutes deux avaient une faible amplitude et n'étaient pas corrélées de façon étroite. Le taux de grossesse élevé (moyenne 86 p. cent/an) et Ie nombre dc petits conçus (moyenne 11,5/grossesse) ne variaient pas de façon significative au cours des ans, probablement à cause de I'abondance et de la variété de sources de nourriture pour les renards. La composition d'âge des prises des trappeurs était également stable d'un hiver à I'autre, mais elle était corrélée de façon étroite avec la taille de la population dc campagnols au cours de I'été précédent. La survie des renardeaux au cours de I'été dépendait probablement de la disponibilité des campagnols. La composition des prises semblait aussi être influencée par I'immigration des renards venant des terres continentales adjacentes par la voie de la banquise.

BURROW-BUILDING STRATEGIES AND HABITAT USE OF VOLES IN PACIFIC NORTHWEST ORCHARDS

Seidel and Booth (1960) wrote that the "life histories of the genus Microtus are not numerous in the literature." In support of his observation he cited 6 publications, all dated between 1891 and 1953. Since then the literature has exploded with a proliferation of publications. An international literature review recently revealed over 3,500 citations for the genus. When Pitymys and Clethrionomys are included another 350 and 1,880, respectively, were found. Over the last 10 years approximately 3 new publications on voles appeared every 4 days; a significant output for what some would consider such an insignificant species. Most of the publications were the result of graduate research projects on population dynamics and species ecology. As such, many do not explore more than the rudimentary ecological relationships between the animal and their environments. Unfortunate, as well, is that all but one confined their observations to only a small part of their total environment. For many of these animals, their life underground may be more important for their survival than that above ground. Trapping studies conducted by Godfrey and Askham (1988) with permanently placed pitfall live traps in orchards revealed a significant inverse population fluctuation during the year. During the winter, when populations are expected to decrease, as many as 6 to 8 mature Microtus montanus were collected at any 1 time in the traps after several centimeters of snow accumulation. During the summer, when populations are expected to increase, virtually no animals were collected in the traps. According to current population dynamics theory, greater numbers of animals, including increasingly larger numbers of immature members of the community, should appear in any sample between the onset of the breeding period, generally in the spring, taper off during the latter part of the production season, usually late summer, and then decline as the limiting factors begin to take effect. For us, we trapped more animals in the fall and early winter than we did during the spring and summer. A review of the above literature did little to answer our question. Where are the animals going during the summer and why?