Zbigniew Borowski

Is there a linkage between metabolism and personality in small mammals? The root vole (Microtus oeconomus) example

Significant inter-individual variation in the rate of animal metabolism is a widespread phenomenon that has started to accumulate general interest. Here we follow recent calls to focus on linkage between the variation in energy metabolism and animal personality. By using wild caught root voles as a study species, we examined the relationship between the behavioral patterns (assessed in open field test) and resting metabolic rate (RMR), both of which are known to show large individual differences and intra-individual consistency in voles. Our results showed only a weak relationship between personality traits and metabolism, since the most parsimonious model (according to AICc) explaining RMR included only body mass and season as factors (explaining 84.8% of variation in RMR). However, the next two alternative models (within ΔAICc=2) also included the personality trait reflecting proactive behaviors (PC1) in addition to body mass, sex and season (85.2 and 85.8% of RMR variance explained, respectively). In all, our study does not provide compelling support for recent ideas of close linkage between behavior and metabolism. Still, our study highlights that even in the case of wild caught individuals, when behavior and metabolism often carry effects of both intrinsic and extrinsic conditions, the potential metabolic effects of varying energetically costly behaviors cannot be neglected.

Habitat selection and home range size of field volesMicrotus agrestis in Słowiński National Park, Poland

Habitat preference, home range size and intra-specific overlap were investigated in summer 1998 among field volesMicrotus agrestis (Linnaeus, 1761) in Słowiński National Park (N Poland). Eight individuals (2 females, 6 males) were radio-tracked for one week in August. Field voles were shown to exhibit a marked preference for meadow and the ecotone between grassland and habitats with common reed, while avoiding alder forest and proper reedbeds. No significant differences between night and day in habitat-use of voles were noted. The results suggest that, at the end of the breeding season, it was food resources, rather than the risk of predation, played an important role in the voles’ utilisation of space. The home ranges of males were larger and more diverse than those of females; their sizes being correlated with body mass, such that heavier males had larger home ranges. This further suggests that intra-sexual competition exists between males for females. The low number of females influenced their spatial behaviour, as females had completely exclusive home ranges. Four males (out of six) had overlapping home ranges with other males; three of the overlaps were of less than 20%. Attributes of promiscuity (such as a 3.5:1 operational sex ratio of males to females, intra-sexual competition between males and the territorial exclusivity of females) influenced the social system. However, the period of radio-tracking during this study was too short to define accurately the social system in the field vole population.

Unexpected population genetic structure of European roe deer in Poland: an invasion of the mtDNA genome from Siberian roe deer

Introgressive hybridization is a widespread evolutionary phenomenon which may lead to increased allelic variation at selective neutral loci and to transfer of fitness‐related traits to introgressed lineages. We inferred the population genetic structure of the European roe deer (Capreolus capreolus) in Poland from mitochondrial (CR and cyt b) and sex‐linked markers (ZFX, SRY, DBY4 and DBY8). Analyses of CR mtDNA sequences from 452 individuals indicated widespread introgression of Siberian roe deer (C. pygargus) mtDNA in the European roe deer genome, 2000 km from the current distribution range of C. pygargus. Introgressed individuals constituted 16.6% of the deer studied. Nearly 75% of them possessed haplotypes belonging to the group which arose 23 kyr ago and have not been detected within the natural range of Siberian roe deer, indicating that majority of present introgression has ancient origin. Unlike the mtDNA results, sex‐specific markers did not show signs of introgression. Species distribution modelling analyses suggested that C. pygargus could have extended its range as far west as Central Europe after last glacial maximum. The main hybridization event was probably associated with range expansion of the most abundant European roe deer lineage from western refugia and took place in Central Europe after the Younger Dryas (10.8–10.0 ka BP). Initially, introgressed mtDNA variants could have spread out on the wave of expansion through the mechanism of gene surfing, reaching high frequencies in European roe deer populations and leading to observed asymmetrical gene flow. Human‐mediated introductions of C. pygargus had minimal effect on the extent of mtDNA introgression.

Multiple paternity in free-living root voles (Microtus oeconomus)

We used 10 microsatellite loci to determine the mating system and male reproductive success in a natural population of the root vole (Microtus oeconomus). By genotyping 21 females and their 111 offspring (5.28+/-0.27 S.E. pups per female), we found evidence for multiple paternity in 38% of the litters sired by two or three males. Paternity was not significantly skewed away from the null expectation of equal proportions of offspring sired in any of the multiple-sired litters, and the most successful male fathered between 40% and 60% of the pups in a litter. The results indicate that promiscuity is a common mode of reproduction, consistent with the previous classification of the mating system based on the spatial structure of the root vole population.

Damage caused by rodents in Polish forests

Abstract The impact of small rodents on Polish forest trees was examined at both the national and regional levels. Detailed information based on a questionnaire was collected at the national level in 1993. Field studies at the regional level were carried out from 1994 through to 1997. The damage due to rodents constituting a significant economic problem occurred in only 4% of the Forest Districts in Poland. The tree species that small rodents preferred most were larch, ash, beech and maple, whereas birch, Norway spruce, Scots pine and black alder were the least preferred. Regional field studies were conducted in localities with the highest levels of damage situated in the Sudety Mountains (southern Poland). In this region, the most common rodent species was the field vole. Levels of tree-seedling damage were correlated with vole population density in the Autumn. I conclude that: (1) at the national level, the damage caused by small rodents has limited impact on Polish forestry; (2) at the regional level small rodents may exert considerable pressure on the over-wintering survival of tree seedlings.

Field vole ( Microtus agrestis ) seasonal spacing behavior: the effect of predation risk by mustelids

There are numerous studies showing that predation risk may change different aspects of the behavior of prey, such as habitat use, activity pattern, and foraging. Prey should exhibit the strongest antipredatory response against their most deadly predator. Small mustelids are considered the most important mammalian predators of voles. Nevertheless, there is no general agreement as to whether strong antipredatory reactions exist in natural free-living populations of voles. Here, we studied the field vole Microtus agrestis spatial reaction to high predation risk from small mustelids in the breeding (August) and nonbreeding (October) seasons under natural conditions. Voles were exposed to a caged weasel (Mustela nivalis) and a stoat (Mustela erminea), as well as to the odors of these predators. The reactions of 30 field voles were monitored with radiotelemetry. The field voles were found to display antipredator reactions that varied with season. In the breeding period, in response to predation risk, voles reduced locomotory activity and daily-range size, whereas in the nonbreeding period they did not. Changes in home range position were similar for control and treatment voles, in both the breeding and nonbreeding periods. The results indicate that mustelid predators modify the spatial behavior of small rodents in natural conditions depending on season. This might be a reflection of differences in state-dependent responses to predation from sexually active or inactive individuals. This suggests that the basic antipredatory reaction of voles under high predation risk from small mustelids limits their locomotory activity.

Relationships between dominance, testosterone level and scent marking of males in a free-living root vole (Microtus oeconomus) population.

In many species, dominance increases a males mating success via intrasexual competition and/or female choice. The level of androgen hormones, mainly testosterone (T), the intensity of scent marking and body mass are traits that are known to be linked to mammalian male social rank. Recently, however, it has been noted that this link between male dominance and the aforementioned traits in natural free-living populations is not universal and does not exist in some species. That is why we tested the hypothesis of whether a males social rank is related to the expression of T, scent-marking and his body mass. We conducted the study on the promiscuous rodent species, root voles (Microtus oeconomus), which originated from a natural population (wild-born). These tests provided support for the following conclusions: (1) the social status of a male root vole is partly related to his level of testosterone; (2) the highest T level was observed in subdominant males; (3) T levels proved to be independent of male body mass; (4) marking frequency was not dependent on a males social status nor their body mass; and (5) the mean body mass of dominant, subdominant and subordinate individuals was similar. Our results indicate that in natural free-living populations, the link between the T levels and dominance behaviour of root vole males is ambiguous. Moreover, there is no link between the social status and the intensity of scent-marking. We therefore conclude that in this species, male marking intensity cannot be used as an indicator of social rank.

Purifying Selection, Density Blocking and Unnoticed Mitochondrial DNA Diversity in the Red Deer, Cervus elaphus

The trajectories of postglacial range expansions, the occurrence of lineage patches and the formation and maintenance of secondary contact between lineages may mostly reflect neutral demographic processes, including density blocking, that may leave long-lasting genetic signatures. However, a few studies have recently shown that climate may also play a role. We used red deer, a large, mobile herbivore that is assumed to be sensitive to climate change, to test hypotheses of possible selection on the mitochondrial DNA cytochrome b gene (mtDNA cytb) and competitive and/or density-blocking (using mtDNA control region). We searched for a possible link between the phylogeographic structure and abiotic climatic variables. Finally, we tested for isolation by distance and isolation by environment and assessed the impact of human-mediated translocations on the genetic structure of red deer. Our analysis of 30 red deer populations in Poland using the mtDNA control region (N = 357) and cytochrome b (N = 50) markers not only confirmed the presence of the Western and South-Eastern lineages of the species but also indicated the presence of a previously unnoticed, rare relic haplotype that grouped together C. e. italicus from Italy (the Mesola deer). No significant signs of positive selection were detected for the mtDNA cytb gene in the studied red deer. However, a significant signal for purifying selection was found in our study that may explain the narrowness of the contact zone because gene flow between the Western and South-Eastern lineages should drive relatively strong mito-nuclear incompatibilities. MtDNA control region differentiation among red deer populations in Poland correlated with different abiotic climatic variables. Strikingly, the southernmost ice sheet limits during the Elsterian was the most important factor, and it explained the largest amount of variation. However, neither isolation by distance (IBD) nor isolation by environment (IBE) were recorded, and a very limited impact of human translocations was evident. The above-mentioned results suggest that in contemporary red deer populations in Poland, the phylogeographic pattern is well preserved, and long-term processes (density and/or competitive blocking) still play a major role.

Spatial Responses of Field (Microtus Agrestis) and Bank (Clethrionomys Glareolus) Voles to Weasel (Mustela Nivalis) Odour in Natural Habitat

The odors of predatory mammals, i.e. mustelids, might be recognised by potential prey, i.e., small rodents, as a signal of predation risk. Using the sense of smell, rodents could detect the presence of predators and respond accordingly by avoiding areas where they have encountered the predator’s scent (Jedrzejewski et al., 1993). Early recognition of predation risk by detection of predator odors might thus increase the chances for survival for small rodents (Borowski, unpublished data). For example, experiments in both laboratory and field conditions demonstrated that exposure to weasel odors caused voles to exhibit antipredatory reactions (Jedrzejewski et al., 1993). Voles that are in danger of predation by mustelids apparently reduce the risk of predation by moving to a microhabitat that lacks evidence of predators (Korpimaki et al., 1996). Voles under predation risk might also limit or change their feeding preferences (Sullivan et al., 1988; Borowski, 1998a) and reduce their locomotor activity to a smaller home range area (Gorman, 1984; Jedrzejewski et al., 1993; Borowski, 1998b). Seasonal differences in responses to weasel odors in field populations of root voles (Microtus oeconomus) have been demonstrated: during the breeding season, voles avoided the weasel odour to a greater extent than during the non-breeding season (Borowski, 1998b).

Radiotelemetry Applied to Field Studies of Shrews

Abstract Radiotelemetry is a widely used method to study ecology, behavior, and physiology of different animals but has rarely been used on shrews. Small body size, wide neck and narrow skull, high mobility, and fragility of shrews cause problems for both transmitter attachment and the safety of the animals. We developed a method for nonpermanent attachment of transmitters, which allowed us to track such small mammals as the Eurasian water shrews (Neomys fodiens; n  =  39, mean body mass 14.9 g), Mediterranean water shrews (Neomys anomalus; n  =  32, 10.9 g), and common shrews (Sorex araneus; n  =  51, 8.1 g). We used microtransmitters weighing 0.47 g, but those we applied to the larger Neomys species were heavier (0.67 g) because we fortified them with a layer of hard material to prevent damage from biting. We glued a transmitter directly to the skin on a shrews back, with the anterior edges particularly well sealed. We tracked shrews in the wild and in outdoor enclosures. Transmitters usually dropped off together with peeled skin (on average, after 56.0 hr, n  =  92 observations), but if not dropped and if the signal was not lost, mean duration of monitoring was 96.7 hours (n  =  37) and in 2 cases exceeded 194 hours. Other advantages of our attachment method were 1) it was less invasive and easier to apply than implantation of transmitters into the body cavity, and 2) we could find dropped transmitters and reuse them. We give suggestions on how to minimize the risk of injury to animals by correct handling, manipulation, and gluing. In conclusion, we recommend radiotelemetry as a useful technique for studying shrew behavior in both free-living populations and experimental enclosures.