Pygmy Shrew Research Articles

Molecular evolution of Azagny virus, a newfound hantavirus harbored by the West African pygmy shrew (Crocidura obscurior) in Côte d'Ivoire

BackgroundTanganya virus (TGNV), the only shrew-associated hantavirus reported to date from sub-Saharan Africa, is harbored by the Therese's shrew (Crocidura theresae), and is phylogenetically distinct from Thottapalayam virus (TPMV) in the Asian house shrew (Suncus murinus) and Imjin virus (MJNV) in the Ussuri white-toothed shrew (Crocidura lasiura). The existence of myriad soricid-borne hantaviruses in Eurasia and North America would predict the presence of additional hantaviruses in sub-Saharan Africa, where multiple shrew lineages have evolved and diversified.MethodsLung tissues, collected in RNAlater®, from 39 Buettikofer's shrews (Crocidura buettikoferi), 5 Jouvenet's shrews (Crocidura jouvenetae), 9 West African pygmy shrews (Crocidura obscurior) and 21 African giant shrews (Crocidura olivieri) captured in Côte d'Ivoire during 2009, were systematically examined for hantavirus RNA by RT-PCR.ResultsA genetically distinct hantavirus, designated Azagny virus (AZGV), was detected in the West African pygmy shrew. Phylogenetic analysis of the S, M and L segments, using maximum-likelihood and Bayesian methods, under the GTR+I+Γ model of evolution, showed that AZGV shared a common ancestry with TGNV and was more closely related to hantaviruses harbored by soricine shrews than to TPMV and MJNV. That is, AZGV in the West African pygmy shrew, like TGNV in the Therese's shrew, did not form a monophyletic group with TPMV and MJNV, which were deeply divergent and basal to other rodent- and soricomorph-borne hantaviruses. Ancestral distributions of each hantavirus lineage, reconstructed using Mesquite 2.74, suggested that the common ancestor of all hantaviruses was most likely of Eurasian, not African, origin.ConclusionsGenome-wide analysis of many more hantaviruses from sub-Saharan Africa are required to better understand how the biogeographic origin and radiation of African shrews might have contributed to, or have resulted from, the evolution of hantaviruses.

American Pygmy Shrew, <em>Sorex hoyi</em>, Consumed by an Arctic Grayling, <em>Thymallus arcticus</em>

Arctic Grayling, Thymallus arcticus, are rarely reported to consume small mammals. We report an American Pygmy Shrew, Sorex hoyi, consumed by an Arctic Grayling caught in southern Yukon, Canada. This is the first record of an American Pygmy Shrew being consumed by an Arctic Grayling, and it confirms that Arctic Grayling will consume shrews (Sorex spp.) when they are available. We suspect that the body size of prey is a limiting factor in Arctic Grayling consuming small mammals, with some species of shrews being small enough for Arctic Grayling to consume.

Colonization of Ireland: revisiting ‘the pygmy shrew syndrome’ using mitochondrial, Y chromosomal and microsatellite markers

There is great uncertainty about how Ireland attained its current fauna and flora. Long-distance human-mediated colonization from southwestern Europe has been seen as a possible way that Ireland obtained many of its species; however, Britain has (surprisingly) been neglected as a source area for Ireland. The pygmy shrew has long been considered an illustrative model species, such that the uncertainty of the Irish colonization process has been dubbed 'the pygmy shrew syndrome'. Here, we used new genetic data consisting of 218 cytochrome (cyt) b sequences, 153 control region sequences, 17 Y-intron sequences and 335 microsatellite multilocus genotypes to distinguish between four possible hypotheses for the colonization of the British Isles, formulated in the context of previously published data. Cyt b sequences from western Europe were basal to those found in Ireland, but also to those found in the periphery of Britain and several offshore islands. Although the central cyt b haplotype in Ireland was found in northern Spain, we argue that it most likely occurred in Britain also, from where the pygmy shrew colonized Ireland as a human introduction during the Holocene. Y-intron and microsatellite data are consistent with this hypothesis, and the biological traits and distributional data of pygmy shrews argue against long-distance colonization from Spain. The compact starburst of the Irish cyt b expansion and the low genetic diversity across all markers strongly suggests a recent colonization. This detailed molecular study of the pygmy shrew provides a new perspective on an old colonization question.

Small mammal mycophagy in hemiboreal forest communities of Lithuania

Abstract The diets of small mammals in different hemiboreal spruce-dominated, oak-dominated and mixed forests in western part of Lithuania were studied by examination of fungal spores in fresh fecal pellets of caught animals. In the diets of mice (Apodemus spp.), bank voles (Myodes glareolus), and common and pygmy shrews (Sorex araneus and S. minutus), 22 different fungal taxa were identified, 15 of which were hypogeous fungi. The sporocarp abundance and the spores in fecal samples of Elaphomyces fungi prevailed in study area during this investigation. Although most of the captured individuals consumed fungi, the consumption varied among small mammal species. The data show that the fungi were more frequent and taxonomically diverse in Myodes glareolus than in Apodemus spp. diets. The study provided evidence that the fungal component in the diets of insectivorous Sorex species is more diverse than previously known. The availability of sporocarps and the fungal component in the diets of small mammals showed seasonal effects. Annual hypogeous and epigeous sporocarp abundances did not vary significantly across forest types. The significant difference in mycophagy was observed across all forest cover types, with the greatest fungal diversity in fecal samples collected in mixed coniferous-deciduous tree stands.

Using multiple methods to assess detection probabilities of forest‐floor wildlife

AbstractMany previous comparisons of multiple sampling methods have assumed that detection probabilities for each method are either constant or equal to one. We used 4 sampling methods to estimate detection probabilities for forest‐floor dwelling amphibians, reptiles, and small mammals. We investigated associations between seasonality and precipitation on species detection and explored sample design tradeoffs for future studies. Although we captured 25 species, we could reliably detect (detection probability >0.15) only northern short‐tailed shrews (Blarina brevicauda) and pygmy and masked shrews (Sorex spp.) using drift fences and red‐backed salamanders (Plethodon cinereus) using visual encounter surveys (VES). The use of multiple sampling methods improved detection probabilities for only red‐backed salamanders (${\hat {p}}_{{\rm VES}} $ = 0.32, 95% CI: 0.24–0.38, ${\hat {p}}_{{\rm all methods}} $ = 0.38, 95% CI: 0.32−0.44). Parameter estimates indicated detection of both shrew species was positively related to increased precipitation. Detection probabilities for pygmy and masked shrews and red‐backed salamanders were positively and negatively associated with date, respectively. Our power analysis revealed that sampling during rain events increased the power of detecting a change in sorid occupancy by ≥40% (α = 0.05). Our results demonstrate the need to incorporate species detectability when comparing the effectiveness of different trapping methodologies. Furthermore, our study highlights the utility of power analyses for exploring study design tradeoffs for research and monitoring programs. © 2011 The Wildlife Society.

Investigation of the Ecology ofFrancisella tularensisDuring an Inter-Epizootic Period

A 1-year study of the ecological cycle of Francisella tularensis was performed in an enzootic area during an inter-epizootic period. The study was based on multiple sampling of all major constituents of the disease cycle. Seroprevalence of tularemia in the European brown hare (Lepus europaeus) population was 5.1% (10/197) with low antibody titers (1/10 and 1/20), and F. tularensis ssp. holarctica was isolated from four hares. F. tularensis was not detected in the 38 common voles (Microtus arvalis), 110 yellow-necked mice (Apodemus flavicollis), or 15 stripped field mice (Apodemus agrarius) trapped during the study, or the by-catch of 8 Eurasian pygmy shrews (Sorex minutus) or 6 common shrews (Sorex araneus). A total of 1106 Ixodes ricinus and 476 Haemaphysalis concinna ticks were collected from vegetation, and 404 I. ricinus, 28 H. concinna ticks, and 15 Ctenophtalmus assimilis and 10 Nosopsyllus fasciatus fleas were combed off small mammals. One H. concinna female and one nymph collected from the vegetation was found infected with F. tularensis ssp. holarctica by TaqMan polymerase chain reaction, thus resulting a 0.42% (2/476) prevalence. F. tularensis-specific DNA was not detected in environmental water samples, and the examined 100 sheep, 50 cows, and 50 buffalos grazed at the study area were all seronegative. During inter-epizootic periods, F. tularensis ssp. holarctica seems to persist only in the European brown hare--H. concinna cycle at the studied habitat. H. concinna may not serve exclusively as an arthropod vector, but it may also harbor bacteria for 3-4 years through multiple life stages and act as an important reservoir of F. tularensis. Rodent species probably do not serve as true reservoir hosts of tularemia.

Genetic and morphological variation in a Mediterranean glacial refugium: evidence from Italian pygmy shrews, Sorex minutus (Mammalia: Soricomorpha)

At the Last Glacial Maximum (LGM), the southern European peninsulas were important refugia for temperate species. Current genetic subdivision of species within these peninsulas may reflect past population subdivision at the LGM, as in ‘refugia within refugia’, and/or at other time periods. In the present study, we assess whether pygmy shrew populations from different regions within Italy are genetically and morphologically distinct. One maternally and two paternally inherited molecular markers (cytochrome b and Y-chromosome introns, respectively) were analysed using several phylogenetic methods. A geometric morphometric analysis was performed on mandibles to evaluate size and shape variability between populations. Mandible shape was also explored with a functional approach that considered the mandible as a first-order lever affecting bite force. We found genetically and morphologically distinct European, Italian, and southern Italian groups. Mandible size increased with decreasing latitude and southern Italian pygmy shrews exhibited mandibles with the strongest bite force. It is not clear whether or not the southern Italian and Italian groups of pygmy shrews occupied different refugia within the Italian peninsula at the LGM. It is likely, however, that geographic isolation earlier than the LGM on islands at the site of present-day Calabria was important in generating the distinctive southern Italian group of pygmy shrews, and also the genetic groups in other small vertebrates that we review here. Calabria is an important hotspot for genetic diversity, and is worthy of conservation attention. © 2010 The Linnean Society of London, Biological Journal of the Linnean Society, 2010, 100, 774–787.

Effects of non-native spruce plantations on small mammal communities in subarctic birch forests

Voles and shrews are key species in northern forest ecosystems. Thus, it is important to quantify to what extent new forestry practices such as planting of non-native tree species impact these small mammals. In northern Norway stands of coastal subarctic birch forests have increasingly been converted to non-native spruce stands during the last century. This leads to changes in the forest floor vegetation and soil conditions that can be expected to negatively impact the community of ground-dwelling small mammals. In this 10-year trapping study we contrasted seasonal small mammal population abundances in spruce plantations with four birch forest varieties. Six different small mammal species were trapped (in descending order of abundance; common shrew Sorex araneus, red vole Myodes rutilus, field vole Microtus agrestis, grey-sided vole M. rufocanus, pygmy shrew S. minutus and water shrew Neomys fodiens). None of the voles appeared to exhibit temporal dynamics resembling population cycles. The three most numerous species were clearly less abundant in the spruce plantations compared to the other forest types. Autumn abundances were most impacted by spruce plantations, indicating that growth rates in the reproductive season were more influenced than winter declines. Species associated with productive forest habitats (i.e. field vole and common shrew) were most impacted by tree species conversion. Still young spruce plantations inter-mixed with birch trees and the ecotone habitat, sustained small mammal abundances comparable to the native birch forests. This implies that managing spruce plantations to maintain a mix of different tree species and high spatial heterogeneity (i.e. more ecotones), will reduce the negative impacts on the small mammal community. On the contrary, if young spruce plantations, as they age become spruce monocultures covering larger parts of the landscapes than they do presently, the negative effects on small mammal communities may be larger than observed in the present study.

Northern glacial refugia for the pygmy shrew Sorex minutus in Europe revealed by phylogeographic analyses and species distribution modelling

The southern European peninsulas (Iberian, Italian and Balkan) are traditionally recognized as glacial refugia from where many species colonized central and northern Europe after the Last Glacial Maximum (LGM). However, evidence that some species had more northerly refugia is accumulating from phylogeographic, palaeontological and palynological studies, and more recently from species distribution modelling (SDM), but further studies are needed to test the idea of northern refugia in Europe. Here, we take a rarely implemented multidisciplinary approach to assess if the pygmy shrew Sorex minutus, a widespread Eurasian mammal species, had northern refugia during the LGM, and if these influenced its postglacial geographic distribution. First, we evaluated the phylogeographic and population expansion patterns using mtDNA sequence data from 123 pygmy shrews. Then, we used SDM to predict present and past (LGM) potential distributions using two different training data sets, two different algorithms (Maxent and GARP) and climate reconstructions for the LGM with two different general circulation models. An LGM distribution in the southern peninsulas was predicted by the SDM approaches, in line with the occurrence of lineages of S. minutus in these areas. The phylogeographic analyses also indicated a widespread and strictly northern‐central European lineage, not derived from southern peninsulas, and with a postglacial population expansion signature. This was consistent with the SDM predictions of suitable LGM conditions for S. minutus occurring across central and eastern Europe, from unglaciated parts of the British Isles to much of the eastern European Plain. Hence, S. minutus likely persisted in parts of central and eastern Europe during the LGM, from where it colonized other northern areas during the late‐glacial and postglacial periods. Our results provide new insights into the glacial and postglacial colonization history of the European mammal fauna, notably supporting glacial refugia further north than traditionally recognized.

Late Pleistocene fauna from Zesch Cave, Mason County, Texas

The Zesch Cave local fauna is one of the most diverse fossil vertebrate localities from central Texas, and one of the only three sites on the Edwards Plateau juxtaposed to the Llano Uplift. At least 70 vertebrate taxa are identified in this local fauna including fish, four lissamphibians, six sauropsids, eight birds, and fifty-one mammal species. A largely granitic structural dome, the Llano uplift differs from the rest of the predominantly carbonate Edwards Plateau in geology, soils and ecology. This is reflected in the Zesch Cave local fauna as well, which has greater similarity to high plains faunas than those recorded 80 km or more to the south. Notably, this local fauna contains the first record of Sorex hoyi (pygmy shrew) and Pica pica (magpie) from central Texas, which indicates similarity or connection with a Rocky Mountain fauna. The Zesch Cave vertebrates provide a more complete picture of faunal zones as they existed in the Rancholabrean.

Responses of wild small mammals to a pollution gradient: Host factors influence metal and metallothionein levels

We investigated how host factors (species, age, gender) modulated Cd, Pb, Zn, and Cu concentrations, metallothionein levels (MTs) and their relationships in 7 sympatric small mammal species along a pollution gradient. Cd concentrations in liver and kidneys increased with age in all species. Age effect on other metals and MTs differs among species. Gender did not influence metal and MT levels except in the bank vole. Three patterns linking internal metal concentrations and MTs were observed along the gradient: a low metal accumulation with a (i) high (wood mouse) or (ii) low (bank vole) level of MTs accompanied by a slight or no increase of MTs with Cd accumulation; (iii) an elevated metal accumulation with a sharp increase of MTs (common and pygmy shrews). In risk assessment and biomonitoring perspectives, we conclude that measurements of MTs and metals might be associated because they cannot be interpreted properly when considered separately.

The Celtic fringe of Britain: insights from small mammal phylogeography.

Recent genetic studies have challenged the traditional view that the ancestors of British Celtic people spread from central Europe during the Iron Age and have suggested a much earlier origin for them as part of the human recolonization of Britain at the end of the last glaciation. Here we propose that small mammals provide an analogue to help resolve this controversy. Previous studies have shown that common shrews (Sorex araneus) with particular chromosomal characteristics and water voles (Arvicola terrestris) of a specific mitochondrial (mt) DNA lineage have peripheral western/northern distributions with striking similarities to that of Celtic people. We show that mtDNA lineages of three other small mammal species (bank vole Myodes glareolus, field vole Microtus agrestis and pygmy shrew Sorex minutus) also form a 'Celtic fringe'. We argue that these small mammals most reasonably colonized Britain in a two-phase process following the last glacial maximum (LGM), with climatically driven partial replacement of the first colonists by the second colonists, leaving a peripheral geographical distribution for the first colonists. We suggest that these natural Celtic fringes provide insight into the same phenomenon in humans and support its origin in processes following the end of the LGM.

The worm in the fruit of the mitochondrial DNA tree

The worm in the fruit of the mitochondrial DNA tree

Distribution and coexistence of shrews in patchy landscapes: A field test of multiple hypotheses

Despite the important role of shrews (Soricomorpha: Soricidae) in the functioning of ecosystems, as predators and prey, the effects of habitat loss and fragmentation on this guild of mammals are still unclear. We studied the distribution of 5 species (the greater white toothed shrew Crocidura leucodon; the lesser white toothed shrew Crocidura suaveolens; the pigmy shrew Sorex minutus; the Appennine shrew Sorex samniticus and the Etruscan shrew Suncus etruscus) in a fragmented landscape in central Italy. Shrews were trapped with pitfall traps made from plastic water bottles, the number of traps increased with patch size. A total of 170 individuals, of 5 species of shrews were captured. Shrews were widely distributed in our study area, however patch occupancy was determined mainly by vegetation and geometrical characteristics of the patches. Our data supports the hypotheses that patterns of habitat selection and the dynamics of seasonal abundance (habitat and temporal partitioning between similarly sized species) reduce competitive pressure, thus allowing coexistence of shrews in relatively species-rich assemblages, for such small amounts of habitat. The most important outcome of our results is the crucial role played by vegetation structure in determining distribution patterns. These results strongly suggest that measurements of the vegetation structure of habitat patches should always be included as explanatory variables when studying the distribution of shrews in fragmented landscapes.

Genetic variation in Irish pygmy shrews Sorex minutus (Soricomorpha: Soricidae): implications for colonization history

The status of the pygmy shrew (Sorex minutus L.) as a native or an introduced species in Ireland has been subject to much debate. To examine this and other aspects of the colonization history of the Irish pygmy shrew, genetic variation was determined in 247 pygmy shrews collected throughout Ireland, using mitochondrial control region sequences and five polymorphic microsatellite loci. Genetic diversity was low for both types of marker. The median-joining network for control region sequences was star-like, suggesting that the colonization of Ireland involved a small number of founders and rapid population expansion thereafter; this was supported by other statistics. Molecular dating with both mitochondrial DNA and microsatellite data is consistent with a human introduction. This would have been several thousand years ago; a recent colonization within historical times can be ruled out. This is the first detailed population genetic study of the pygmy shrew anywhere in its range. © 2009 The Linnean Society of London, Biological Journal of the Linnean Society, 2009, 97, 918–927.

Cornea, retina, and lens morphology in five Soricidae species (Soricomorpha: Mammalia)

We analyzed the cornea, retina, and lens of five species of Soricidae (pygmy shrew, Sorex minutus; common shrew, Sorex araneus; Millet's shrew, Sorex coronatus; water shrew, Neomys fodiens; greater white-toothed shrew, Crocidura russula) by light and electron microscopy. In all of these species, the corneal epithelium showed a dead cell layer, which may increase the refractive power of the cornea, thereby reducing the hypermetropy that would be expected in a small eye. Moreover, the anterior surface of the lens was more curved than the posterior, thus minimizing spherical aberrations. The thicker lens and its smaller radii of curvature indicated that Sorex species and N. fodiens have a higher refractive lens power than the most nocturnal species, C. russula. In addition, only in the retina cone inner segments of the most diurnal species (genus Sorex) did we find megamitochondria that might act as microlenses to enhance the efficiency of cones. In C. russula, the scarcity of cones and the relatively small yet abundant rod nuclei were found to be consistent with its habits. The flat lens and its more anterior arrangement, together with the lack of megamitochondria in the retina of C. russula, indicated that this species has less visual acuity than the other shrews studied here.

The impact of forest ski-pistes on diversity of ground-dwelling arthropods and small mammals in the Alps

Forest clearing for winter sport activities is the major force driving loss and fragmentation of the alpine forests. The establishment of ski-pistes involves impacts on every ecosystem component. To assess the extent of this threat we studied ground-dwelling arthropods (namely ground beetles and spiders) and small mammals (shrews and voles) at two ski resorts in north-western Italian Alps by pitfall trapping. Diversity parameters (mean abundance, species richness and Shannon index) of spiders and macropterous carabids increased from forest interior to open habitats (i.e., ski-piste or pasture), whereas parameters of brachypterous carabids significantly decreased from forest interior to open habitats. Diversity parameters of macropterous ground beetles were higher on pastures than on ski-pistes. Small mammals were virtually absent from ski-pistes. Observed frequencies in the three adjacent habitats were significantly different from expected ones for the bank vole Myodes glareolus and the pygmy shrew Sorex minutus. Generalized linear models showed that abundance, species richness and diversity of spiders and macropterous carabids of ski-pistes were best modelled by combination of factors, including grass cover and width of the ski-piste. Indicator Species Analysis showed that species that significantly preferred ski-pistes were less than those preferring pastures, and species which were exclusive of ski-pistes were very few. To retain arthropod ground-dwelling fauna of open habitats environmentally friendly ways of constructing pistes should be developed. After tree clearing, only the roughest ground surfaces should be levelled, in order to preserve as much natural vegetation as possible. Where necessary, ski-pistes should be restored through the recovery of local vegetation.

Population dynamics of the common shrew and pygmy shrew (Soricomorpha: Soricidae) in a clear-cut of a mixed forest in eastern Lithuania

Population dynamics (density, age structure, and sex ratio) of Sorex araneus and S. minutus was studied in late summers of 1987-1993 during small mammal community formation in a growing-up clear-cut area within a mixed forest in eastern Lithuania (Molėtai District; 55°09' N, 25°20' E). In the studied area the density of the common shrew was significantly greater and its multi-annual variation in density was more stable compared with the pygmy shrew (18.64 ± 2.49 and 5.57 ± 2.75 ind./ha, p < 0.0017; s = 0.258 and s = 0.625, respectively). Changes in the age structure (subadults/adults) and sex ratio of both shrew species correlated with density variations.

Analysis of animal spatial patterns on the basis of marking on transects: An example of red-toothed shrews

The spatial patterns of individually marked juveniles of red-toothed shrews--the masked shrew (Sorex caecutiens), common shrew (S. araneus), and pygmy shrew (S. minutus)--have been determined by comparing the ratio of traps visited by different numbers of animals (0, 1, 2, 3, etc.) with the Poisson distribution and by using the index of relative variance sigma2/m. These tests characterize both the distribution of animal load over different points of the study area and the spatial pattern of individual home ranges. A random type of spatial pattern within relatively uniform biotopes prevails in juveniles of all three red-toothed shrew species, regardless of their properties, abundance, and factors accounting for it. This facilitates the formation of a system of nonoverlapping home ranges of adult females after wintering. The stability of spatial patterns contributes to the efficiency of population self-regulation.

Non‐invasive genetic identification of small mammal species using real‐time polymerase chain reaction

DNA identification of non-invasive samples is a potentially useful tool for monitoring small mammal species. Here we describe a novel method for identifying five small mammal species: wood mouse, bank vole, common shrew, pygmy shrew and water shrew. Species-specific real-time polymerase chain reaction primers were designed to amplify fragments of the mitochondrial cytochrome b gene from hair and scat samples. We also amplified nuclear DNA from scats, demonstrating their potential as a source of DNA for population genetic studies.