Hisashi Yanagawa

Phylogeography of the Russian flying squirrel (Pteromys volans): implication of refugia theory in arboreal small mammal of Eurasia.

A phylogeographical study of the Russian (Siberian) flying squirrel (Pteromys volans) was carried out using the complete mitochondrial (mt) cytochrome b gene sequences with special reference to the refugia theory for the arboreal traits of this species. We examined 31 specimens from 24 localities, resulting in 28 haplotypes. One breeding specimen with a unique haplotype from Hokkaido, Japan was included in the phylogenetic analysis. There were three mtDNA lineages: Hokkaido, Far Eastern, and northern Eurasia. Divergence data among lineages demonstrated that the Hokkaido group separated from the other groups during the Holsteinian interglacial. The phylogeographical pattern of P. volans is different from that previously reported for terrestrial rodents associated with treeless habitats. Unlike grasslands, forests decreased during glaciation and moved southward because of the cold and arid environmental conditions. The glacial refugia of P. volans would have been associated with forest dynamics in the Pleistocene.

Phylogenetic Relationships among Six Flying Squirrel Gener,a Inferred from Mitochondrial Cytochrome b Gene Sequences

Abstract Petauristinae (flying squirrels) consists of 44 extant species in 14 recent genera, and their phylogenetic relationships and taxonomy are unsettled questions. We analyzed partial mitochondrial cyto-chrome b gene sequences (1,068 base pairs) to investigate the phylogenetic relationships among six flying squirrel genera (Belomys, Hylopetes, Petaurista, Petinomys, and Pteromys from Asia and Glaucomys from North America). Molecular phylogenetic trees, constructed by neighbor-joining and maximum likelihood methods, strongly indicated the closer relationship between Hylopetes and Petinomys with 100% bootstrap values. Belomys early split from other flying squirrels. Petaurista was closely related to Pteromys, and Glaucomys was most closely related to the cluster consisting of Hylopetes and Petinomys. The bootstrap values supporting branching at the deeper nodes were not always so high, suggesting the early radiation in the evolution of flying squirrels.

Gliding ability of the Siberian flying squirrel Pteromys volans orii

ABSTRACT Forest fragmentation is a threat to flying squirrel population due to dependence on gliding locomotion in forests. Therefore, it is essential to understand their gliding ability. The gliding locomotion of Pteromys volans orii, were observed from July 2003 to June 2005, in Obihiro, Hokkaido, Japan. The horizontal distance and glide ratio obtained from 31 glides were employed as indicators to know their gliding ability. The gliding ability was not affected by weight and sex in the Siberian flying squirrel. Mean horizontal distance and glide ratio were 18.90 m and 1.70 with great variation. Although maximum values were 49.40 m (horizontal distance) and 3.31 (glide ratio), most of the horizontal distance and glide ratio were in the ‘10–20 m’ and ‘1.0–1.5’, respectively. Therefore, to retain the flying squirrel populations, forest gaps should not exceed the distance traversable with a glide ratio of 1.0 (distance between forests/tree height at the forest edg).

Different Nest Site Selection of Two Sympatric Arboreal Rodent Species, Siberian Flying Squirrel and Small Japanese Field Mouse, in Hokkaido, Japan

Numerous vertebrates use tree cavities as nest resources. Mammals such as Carnivora (Zalewski 1997; Wilson and Nielsen 2007), rodents (Taulman 1999; Shibata et al. 2004; Holloway and Malcolm 2007), bats (Sedgeley and O’Donnell 1999; Boonman 2000; Willis and Brigham 2007), and marsupials (Lindenmayer et al. 1991; Smith et al. 2007; Crane et al. 2010), as well as birds (Aitken et al. 2002; Martin et al. 2004; Adamik and Kral 2008), use tree cavities for daily rest, reproduction, and/or overwintering. Sympatric cavity-users often partition their nest cavities to avoid interspecific competition (van Balen et al. 1982; Martin et al. 2004; Shafique et al. 2009). In Hokkaido, northern Japan, there are two cavitynesting rodents, the Siberian flying squirrel (Pteromys volans) (Nakama and Yanagawa 2009; Suzuki et al. 2011) and the small Japanese field mouse (Apodemus argenteus) (Nakata et al. 2009). There may be competition between these two rodents for tree cavities, but their favored nest sites have not yet been compared. Do they select tree cavities of different types, and, if so, what characteristics are their selections based on? These rodents have different physical and ecological characteristics. Pteromys volans (weight, 110 to 142 g; head and body length, 130 to 167 mm; Hanski et al. 2000; Asari et al. 2007; Oshida 2009) is 5 to 14 times heavier than A. argenteus (weight, 10 to 20 g; head and body length, 65 to 100 mm; Nakata et al. 2009). In addition, P. volans, which is an aerial and arboreal user, spends most of its time in the canopy and almost never walks on the ground, even when crossing wide fields (Selonen and Hanski 2003, 2004). Apodemus argenteus also uses arboreal space (Imaizumi 1978; Abe et al. 1989; Sekijima 2004), and it is able to climb to a height of 18 m (Ida et al. 2004). However, it more frequently uses foods on and under the ground than above the ground (Abe 1986). These differences in size and habit between the two species may result in different choices of tree cavities. Larger species of cavity-nesting mammals and birds tend to nest in larger cavities with larger entrances (Martin et al. 2004). Larger flying squirrels use larger trees with larger entrances than do smaller flying squirrel species (Shafique et al. 2009). Larger bird species also nest in larger entrance cavities than do smaller species (van Balen et al. 1982). Thus, we hypothesized that P. volans, with a larger body than that of A. argenteus, would nest in trees with greater diameters at breast height and in larger cavities with larger entrances. In addition, we hypothesized that P. volans, which is usually active in the upper layer of trees, would nest in higher cavities than A. argenteus, which commonly lives on and under the ground. We examined these hypotheses by surveys of tree cavities and nest boxes.

Characteristics of tree cavities used by Pteromys volans orii in winter

Flying squirrels, such as northern flying squirrels (Glaucomys sabrinus), southern flying squirrels (G. volans), and Siberian flying squirrels (Pteromys volans) often use tree holes or abandoned bird nests as nesting sites (Taulman 1999; Goldingay 2000; Airapetyants and Fokin 2003). There have been several reports on the characteristics of the tree cavities used by flying squirrels (e.g. Taulman 1999; Meyer et al. 2005). Although the Hokkaido-native Pteromys volans orii is also known to nest in tree cavities (Muraki and Yanagawa 2006), there have been no detailed investigations of the cavities that can be used by these animals. Flying squirrels consume more energy at low temperatures due to their gliding membranes that add considerably to their surface area-to-volume ratio (Stapp et al. 1991). In these species, to minimize this energy loss, adaptive features such as reduced activity time in winter (Yamaguchi and Yanagawa 1995) and group nesting (Layne and Raymond 1994; Carey et al. 1997; Masuda 2003a), have been observed. In addition, requirements for nesting sites in winter may be more specific than those in other seasons. A warmer nest, which can reduce the animals’ energy consumption, was assumed to be required in winter. Here we investigated the conditions required for tree cavities used by P. v. orii in winter by comparing the characteristics and inside temperatures of tree cavities used in winter with those in other seasons.

Detecting Nesting Trees of Siberian Flying Squirrels (Pteromys volans) Using Their Feces

Forty-three species of flying squirrels are known worldwide (Goldingay 2000). They frequently use tree cavities for daily rest, reproduction and/or wintering (Taulman 1999; Hanski et al. 2000; Nakama and Yanagawa 2009; Shafique et al. 2009). Cavity trees are thus crucial resources for these species. Recent advances in research on the northern flying squirrel (Glaucomys sabrinus) and the southern flying squirrel (G. volans) have revealed that they prefer large dead trees for building their nests (Meyer et al. 2005; Holloway and Malcolm 2007; Hough and Dieter 2009) and are selective for tree species (Hackett and Pagels 2003; Menzel et al. 2004; Holloway and Malcolm 2007). Siberian flying squirrels (Pteromys volans) also nest inside tree cavities; however, not much is known about their preference for tree types. Nest sites of P. volans have been studied in some regions, including Finland, where they often nest inside tree cavities of the common aspen (Populus tremula) (Hanski et al. 2000). In Japan, P. volans does not show any preference in the diameter at breast height or between dead and living trees in small woods (Asari et al. 2009). Radio telemetry research has been used to identify the nesting trees of P. volans (Hanski et al. 2000; Asari et al. 2009) in the same way as G. sabrinus and G. volans. This method, however, requires considerable labor, and catching the squirrels may disturb them. Inserting CCD cameras to peer into tree cavities to confirm their presence (Muraki and Yanagawa 2006) also risks disturbing the individuals in their nests, in some cases causing them to move elsewhere. Tree cavities are also used for breeding and resting by small mammals such as mice and bats, as well as many species of birds (Kotaka and Matsuoka 2002; Muraki and Yanagawa 2006). Peering into cavities using cameras may disturb these animals, increasing the risk of their abandoning their nest-building activities, especially during breeding periods. These facts prompted us to develop a method of finding cavity trees used as nests by P. volans, other small mammals and birds without causing serious disturbance. Feces tends to accumulate at the foot of nesting trees used by P. volans (Kadosaki 2001). In addition, P. volans usually defecates on the tree trunk near its nesting cavity (Kadosaki 2001). This can be used as an indication that the cavity tree is inhabited by this species (Hanski et al. 2000). Finding trees being used for nesting simply by looking for feces at the foot of trees with cavities is unlikely to affect the animals very much, but the accuracy of this method of confirming the presence of squirrels has so far not been determined. In this study, we verified the accuracy of this method.

Efficient placement of nest boxes for Siberian flying squirrels Pteromys volans: effects of cavity density and nest box installation height

To improve the effectiveness of research into the Siberian flying squirrel Pteromys volans, we investigated the optimal placement of nest boxes. Of the 96 boxes which we installed under various conditions at 10 sites, 47 were occupied by Siberian flying squirrels between spring and autumn. Nest-box height was positively correlated with box occupation; 90% of boxes installed at 2-2.8 m height were used. Cavity density was negatively correlated with occupation, with boxes more frequently used in forests with < 2 cavities/ha. Research in Siberian flying squirrels can thus be made more efficient if nest boxes are installed at a height of 2-2.8 m in forests with < 2 cavities/ha, and by doing observations between spring and autumn.

Banded karyotypes of the hairy-footed flying squirrel Belomys (Trogopterus) pearsonii (Mammalia, Rodentia) from Taiwan

Abstract The chromosomes of the hairy-footed flying squirrel Belomys pearsonii from Taiwan were analyzed with conventional and Ag-NOR staining and G- and C-banding technique. The diploid chromosome number (2n) and fundamental autosomal arm number (FN) were 38 and 72, respectively. The karyotype consisted of six pairs of metacentrics (nos. 1–6), twelve pairs of submetacentrics or subtelocentrics (nos. 7–18), an unusually large-sized metacentric X chromosome, and an acrocentric Y chromosome. The satellite structure, which corresponded to the NOR detected by silver-staining, was observed on the long arm of no. 1 chromosomes. All autosomes and the X chromosome had centromeric constitutive heterochromatin (C-heterochromatin), and the long arms of nos. 17 and 18 chromosomes were entirely heterochromaic. By the C-banding technique, the Y chromosome was entirely stained somewhat darkly than euchromatic region, but did not seem to be genuinely heterochromatic. On the basis of the cytogenetical characteristics of sex chromosomes, the phylogenetic position of Belomys in the group of flying squirrels was briefly referred.

Invasive cutleaf coneflower seeds cached in nest boxes: possibility of dispersal by a native rodent

Invasive species present serious problems for ecosystems and economies. One such species, the invasive cutleaf coneflower (Rudbeckia laciniata L.), has several modes of seed dispersal, namely autochory, anemochory, epizoochory, myrmecochory and anthropochory. Because we found caches of this invasive plants seeds in two nest boxes, suggesting the possibility of synzoochory, we report here the details of the caches. In one of the boxes, many of the seeds were cached in autumn and eaten during the winter. Automatic sensor cameras directed at the boxes revealed that three rodent species and two avian species visited the boxes. The characteristics of the caches and the nest-box visitors suggested that the small Japanese field mouse (Apodemus argenteus Temm.) was the animal most likely to have cached the seeds in the boxes.

Escaping Height in a Tree Represents a Potential Indicator of Fearfulness in Arboreal Squirrels

Abstract. The distance at which animals start to flee from approaching threats should reflects the degree of fearfulness, and thus, provides a useful measurement to evaluate animal personality and tolerance to human disturbance. Such metrics measurements, however, are mostly limited to open, high visible habitats, such as grasslands and urban parks. Alternative measurements are required for other types of habitats, such as typical forests. For arboreal species, we expect that a vertical escape distance (VED), the height at which animals stop climbing in a tree toward approaching threats, would reflect animal fearfulness. We compared VED and two commonly used metrics, alert distance (AD) and flight initiation distance (FID) in the Eurasian red squirrel (Sciurus vulgaris) towards human approach. We found that VED was significantly related with FID, but not AD. Data collection rate in VED was two to three times higher than that in the two previous metrics in vegetated areas. In natural environments, VED would also reflect the degree of fearfulness in arboreal species.