Journal of Ethology

, Volume 25, Issue 1, pp 41–48 | Cite as

Interspecific social interactions and behavioral responses of Apodemus agrarius and Apodemus flavicollis to conspecific and heterospecific odors

Article

Abstract

The social interactions between Apodemus agrarius and A. flavicollis, and their behavioral responses to conspecific and heterospecific odors, were studied in male–male and female–female interspecific dyadic encounters, and an attraction–avoidance test was used in order to clarify the behavioral mechanisms which control their relationships in wild populations. The experiments were carried out at the beginning and at the end of the breeding season—in spring and in autumn. In spring the aggressiveness was higher than in autumn. Males of both species showed attraction to conspecific odors from the opposite sex, while the females were indifferent. In autumn both males and females displayed attraction to conspecific odors from the same sex. However, mice of both species showed avoidance to heterospecific odors from the same and the opposite sex in spring, and indifference to heterospecific odors from the same and the opposite sex in autumn. Based on these findings, it could be assumed that the patterns of social interactions and responses to conspecific and heterospecific odors undergo seasonal changes in their life cycle. Probably the avoidance response to heterospecific odors could serve as a spacing mechanism to avoid aggressive encounters between A. agrarius and A. flavicollis in syntopic habitats during the breeding period.

Keywords

Apodemus Interspecific aggressiveness Chemosensory behavior Odor cues Response seasonality 

Introduction

The striped field-mouse Apodemus agrarius (Pallas 1771) and the yellow-necked mouse Apodemus flavicollis (Melchior 1834) are closely related species, common in central and eastern Europe. In Bulgaria their populations frequently occur syntopically in moist habitats, but little is known about their social life and interspecific relationships. Nevertheless, it is possible that some eco-ethological mechanisms exist in their natural populations.

Aggressive interactions often play an important role in the ecology of closely related wood mice, and affect their coexistence. Andrzejewski et al. (1978) found that in syntopic habitats with A. sylvaticus, A. agrarius reached high density, while A. sylvaticus remained poorly represented. In the absence of A. agrarius, A. sylvaticus occupied its niche (Yalden 1980; Dickman and Doncaster 1986). In laboratory experiments, Frynta et al. (1995) confirmed that in aggressive interactions A. agrarius individuals displayed superiority over A. sylvaticus. A. sylvaticus is a subordinate species in its interactions with A. flavicollis as well (Hoffemeyer 1973; Montgomery 1978, 1980; Čiháková and Frynta 1996). However, the role of aggressiveness in competitive relationships between A. agrarius and A. flavicollis and their spacing behavior has not yet been studied.

Responses to conspecific and heterospecific odors can provide insight into the socio-ecology of species even when little is known about relationships of the animals in nature. Moreover, among small rodents olfactory cues are the most important cues used for conspecific, kin, sex, reproductive and social status recognition (Brown 1979; Cox 1984, 1989; Halpin 1986; Hurst 1989, 1990; Laukaitis et al. 1997; Stopka and Macdonald 1999; Talley et al. 2001; Musolf 2002; Bimova et al. 2005). As mentioned by White et al. (2004), if captive-living animals avoid same-sex odors and show signs of sexual motivation in response to opposite-sex odors, one might infer that these chemical signals play an important role in competition and reproductive strategies in nature. Other works based on olfactory tests have shown that seasonality is an important aspect of chemical communication in many mammal species, and odor preferences may differ between breeding and non-breeding seasons because chemical signals serve different functions at these times (Ferkin and Seamon 1987; White et al. 2004).

Apodemus agrarius and A. flavicollis are seasonal breeders, and their conspecific interactions change across the season. Direct observations of relationships between captive individuals in these two Apodemus species and their close relative—A. sylvaticus—during the breeding period showed the presence of aggressiveness between conspecifics (Hoffemeyer 1973; Montgomery 1978; Čihákova and Frynta 1996; Frynta et al. 1995; Simeonovska-Nikolova 2006). According to Wolton and Flowerdew (1985), Čihákova and Frynta (1996), and Musolf (2002), during the breeding period wood mice and yellow-necked mice are semi-social, and there are no stable associations between individuals. However, other authors have documented the existence of larger or smaller family groups in the populations of the wood mouse, the yellow-necked mouse (Brown 1966, 1969), and the striped field-mouse (Popov and Sedefchev 2003). Although the social organizations of Apodemus species are still being discussed, it could be suggested that there are mechanisms regulating relations between relatives. For instance, in captivity Čihákova and Frynta (1996) observed a high aggressiveness between unrelated A. flavicollis individuals, leading to serious wounding or even killing of the subordinate male in the group. By molecular techniques it was demonstrated both in the wild and in an enclosure experiment that female A. agrarius as well as female A. sylvaticus mate and have offspring with more than one male at a time (Baker et al. 1999; Bartmann and Gerlach 2001; Musolf 2002). However, the female A. sylvaticus showed a preference for unfamiliar and unrelated male odors compared to odors of familiar and even unfamiliar brothers (Musolf 2002). Probably, this ability avoids inbreeding with related males. In winter the striped field-mice and yellow-necked mice form monosexual groups (Montgomery 1980; Kosoj 1984). In A. flavicollis a tendency for association of kin in winter and spring was found also by analysis of the mtDNA (Rosakis 1999). Some resent research showed that beyond the reproductive period amicable interactions between striped field-mice prevailed over agonistic ones (Simeonovska-Nikolova 2006). A similar tendency was observed in A. flavicollis by the latter author (unpublished data). Because conspecific interactions change across the seasons, one might predict that responses of A. agrarius and A. flavicollis to conspecific odors also change with the season. Olfactory preferences also play an important role in spacing behavior and species isolation when closely related species are sympatric (Heth et al. 1996).

In the present work, the social interactions between A. agrarius and A. flavicollis and their behavioral responses to conspecific and heterospecific odors were studied in male–male and female–female interspecific dyadic encounters, and an attraction–avoidance test was used in order to clarify the behavioral mechanisms which control their relationships in wild populations. In Bulgaria, breeding of both species occurs from March to the end of October (Peshev et al. 2000). The possible relationships between the amicable–agonistic interactions in interspecific dyadic encounters and the attraction–avoidance behavior of A. agrarius and A. flavicollis to conspecific and heterospecific odors were also checked. The patterns of amicable–agonistic behavior, as well as responses to conspecific odors from the same and opposite sex, could be related to seasonal changes in their social lifestyle and reproductive strategies. Having in mind that the agonistic interactions between two species increase aversive responses toward heterospecific odors, it could be suggested also that mice might avoid bedding being soiled by the heterospecific mice, if aggressiveness is increased.

Materials and methods

The striped field-mice and the yellow-necked mice were captured from two syntopic populations in the region of north-western Bulgaria (latitude 42°57′N, longitude 23°46′E). The climate is continental, with cold winter and a warm summer. Both species were captured in spring (April–May) and in autumn (September–October) of 2003 and 2004 by live-traps from the terrace of a small river, the Tzerovitza River. The live-traps were distributed randomly within the ecosystem to reduce the possibility of capturing kin-related mice. The behavior of the captured mice was studied in each capture period. The main herbaceous species in the study area were Urtica dioica, Poligonum hudropiper, Poa nemoralis, Andropogon repens, Thypha latifolia, Sparaganum spp. The dominant tree species were Alnus glutinosa, Salix fragilis, Robinia pseudoacacia and Sambucus ebulus, while the dominant shrub species were Rosa canina, Cornus sanguina, Prunus spinosa and Rubus sp.. There were also cultivated lands close to the river.

The captured striped field-mice and yellow-necked mice were used in two experiments: (1) in dyadic encounters for ascertaining their interspecific social interactions, and (2) in a attraction–avoidance test in a T-maze with bedding material containing urine cues from individuals for studying their response to conspecific and heterospecific odors.

A total of 64 A. agrarius individuals and 64 A. flavicollis individuals from 2003 to 2004 were studied in the experiments both in spring and in autumn. Since age is an important factor that can modulate relationships between mice and their responses to odors, only adult and sexually active individuals were included in the experiments—male testes were in scrotal position, females were with open vagina. Pregnant mice were not used. The mice tested had an average weight of 26.8±0.4 g for males and 25.8±0.3 g for females for A. agrarius, and 27.9±1.0 g for males and 25.3±0.3 g for females for A. flavicollis. The weight criterion in combination with some exterior features about the reproductive stage of the mice were used to estimate the age of experimental animals according to other work with wood mice (Cockel and Ruf 2001; Zgrabszyńska and Piłacińska 2002) and personal experience from the field.

The captured animals were individually housed in standard laboratory rodent cages for at least 2 weeks prior to the beginning of the experiments. Each species was placed in a separate laboratory room. The floor of each cage was covered with sawdust. Hay and pieces of tree bark were put in the cages as shelters. The mice were fed a mixed-seed diet supplemented with carrots and apples, and provided with water ad libitum. According to the season, the mice were maintained at natural ambient temperatures, 15–20°C and 9–12 h of light/day during the experiments.

Experiment 1: Interspecific dyadic encounters

Social interactions were studied in six male–male and six female–female encounters in spring, and six male–male and six female–female encounters in autumn. Six males and six females of each species were used in each spring and autumn test, respectively. The encounters were carried out on “neutral ground” in a 50×50 cm2 glass cage provided with fresh sawdust as bedding and hay for shelters. The duration of each encounter was 10 min. Mice were tested in the morning and in the evening. Natural light during the morning and artificial red light during the evening were used for observations. The cage was cleaned before each test. Each animal was used for one encounter only.

All behavioral events were directly observed and registered by shorthand into the protocols. Then, behavioral events were listed and categorized as follows: Agonistic behavior–offensive behavior (threat, attack, fight, chase, offensive-upright and sideways postures), and defensive behavior (defensive-upright posture, retreat, running away, jumping apart), amicable behavior (passing above, grooming, clambering on, standing side-by-side) and introductory behavior (approaching, following, nose–nose, nose–anal, nose–body). Patterns of behavior and terms used in each pattern were cited from other studies on rodents (Mackintosh 1981; Dixon and Fisch 1989; Livoreil et al. 1993; Čihákova and Frynta 1996). The number of behavioral events demonstrated were calculated for each encounter and averaged for male–male and female–female encounters, separately for the spring and the autumn sample. The results are represented by the median and the dispersion—by the extremes. To compare specific levels of agonistic, amicable, and introductory behavior between males and females and between seasons, data were quantitatively analyzed. The significance of species-specific, sexual, and seasonal differences between behavioral patterns demonstrated by the mice was estimated by the Mann–Whitney U-test at P<0.05.

The tested animals in the first experiment were not used in the second one.

Experiment 2: Attraction–avoidance to odor cues

The responses of A. agrarius and A. flavicollis to conspecific and heterospecific odors from same and opposite sex were studied with 20 adult A. agrarius (10 males and 10 females), and 20 adult A. flavicollis (10 males and 10 females) in each study period. The bedding material from individual cages where mice from both species had lived for at least 2 weeks was used as an odor source. The samples were collected in each season from different A. agrarius and A. flavicollis individuals, which were used in the dyadic encounter test. The soiled bedding from the different individuals was kept in a freezer (−4°C). It was defrosted 15 min before testing (ambient temperature). Thus, in spring and autumn, male and female mice from both species were tested for their response to the bedding material from male and female donors from each species. This constituted a 32-cell matrix of experimental groups. Every animal took part in the four tests. Because the mice were used in more than one test, the tests were separated by at least 1 week.

The apparatus was a tunnel T-maze, made of transparent Plexiglas (Fig. 1). The initial runway ended in a T-junction (choice point) where the mouse had to turn to the left or the right in order to continue through the maze and go into the goal box. The same construction and dimensions of start box and goal boxes (16.5×8×6 cm3) allowed for their exchange and thus, disturbance of the animals by handling was limited. During the habituation phase, the animal ran through the maze eight times without any stimulus present. The direction that it turned at the choice point was recorded. When left:right turn ratios were 4:4, 3:5 or 5:3, it was considered that the animal did not show an initial side preference and the experiment continued. The stimulus was placed in one small dish on the floor, 5 cm to the left or to the right of the junction (choice point). After the animal detected the stimulus by sniffing or touching it with its nose, the mouse was allowed to complete eight more trials. The direction which the animal turned (toward the stimulus or to the opposite side) was recorded for these eight trails. Turn ratios of 4:4, 3:5 or 5:3 showed indifference, 2:6, 1:7, and 0:8 showed avoidance, and 6:2, 7:1, and 8:0 showed attraction. During these eight consecutive trials the same odor donor was used. To avoid any side preference, the position of stimulus was changed for each trial. The tunnel system was placed on a glass floor, which facilitated its cleaning. The floor was cleaned between each trial. The experiments in which the mouse remained immobile in the apparatus or where it showed an initial side preference during the habituation phase were not taken into account.
Fig. 1

Plexiglas tunnel T-maze for assessing behavioral responses to chemostimuli in A. agrarius and A. flavicollis

The response of mice to conspecific and heterospecific odors was assessed by subtracting the number of turns away from the stimulus from the number of turns toward the stimulus for each animal and then determining whether the mean difference for each male, female, and male–female group was significantly different from zero, using a paired t-test at P<0.05–0.001 (Fowler et al. 1998). Significantly negative differences indicated “avoidance” of the stimulus, whilst significantly positive differences indicated “attraction” toward the stimulus. The insignificant differences were considered as “indifference”. The described method for assessing behavioral responses to olfactory stimuli used in this experiment was borrowed from other similar research on rodents (Heth and Todrank 1995; Heth et al. 1996).

The investigation conformed to the international requirements for ethical attitude towards animals (Lehner 1996; Rudran and Kunz 1996). After finishing the laboratory experiments the mice were taken back to their habitats. The research complied with the current laws of the Republic of Bulgaria.

Results

Interspecific dyadic encounters

The initial actions of the animals in the experimental cage were directed to exploring the surroundings. Their next behavior was orientated to exploration of the partner by numerous events such as approach, nose–nose, nose–anal, and nose–body. Conflicts occurred both as a result of accidental clashes during exploration and as purposeful attacks. Differences in frequency of behavioral events displayed by mice in encounters indicated sexual and seasonal differences in the patterns of agonistic, amicable, and introductory behavior (Table 1).
Table 1

Median and extreme values (minimum and maximum) of agonistic, amicable and introductory behavior events displayed by A. agrarius and A. flavicollis in male and female interspecific dyadic encounters during spring and autumn

Behavioral patterns

Spring

Autumn

Useasonal

M (n=6)

F (n=6)

M (n=6)

F (n=6)

M× Ma

F× Fa

Agonistic behavior

18.5 (12.0–26.0)

11.0 (3.0–17.0)

10.5 (6.0–18.0)

6.0 (2.0–8.0)

U=3.0*

U=5.0*

Usexual

U=4.5* (M x F) s

U=3.0* (M x F)a

  

Amicable behavior

5.5 (3.0–9.0)

7.0 (5.0–11.0)

13.0 (8.0–15.0)

8.5 (6.0–11.0)

U=3.0*

NS, U=11.5

Usexual

NS (M x F) s, U=13.5

NS (M x F) a,U=6.0

  

Introductory behavior

23.5 (19.0–30.0)

18.0 (5.0–11)

18.0 (16.0–24.0)

16.0 (14.0–20.0)

U=5.0*

U=4.0*

Usexual

NS (M x F) s,U=5.5

NS (M x F) a, U=5.5

  

The significance of sexual and seasonal differences revealed by Mann–Whitney U-test is shown: *P<0.05

n number of encounters, M males, F females, s spring, a autumn. The extreme values are given in brackets

In spring, the interspecific aggressive events displayed by mice in encounters were significantly more frequent than those registered in autumn (Mann–Whitney U test: U=3.0, P<0.05 for male–male encounters, U=5.0, P<0.05 for female–female ones). However, attacks, fights, and chases were observed mainly in the male encounters. The male A. flavicollis presented significantly more offensive and less defensive behaviors than male A. agrarius (Mann–Whitney U test: U=4.5, P<0.05 for offensive behavior, U=1.5, P<0.05 for defensive one), (Table 2). The female A. agrarius often performed upright defensive postures in response to the threatening approaches of A. flavicollis females, but significant species-specific differences in offensive and defensive behaviors were not established (Table 3). Significant differences between male and female encounters were found in the frequency of agonistic events demonstrated by mice both in spring (Mann–Whitney U test: U=4.5, P<0.05), and in autumn (Mann–Whitney U test: U=3.0, P<0.05), (Table 1).
Table 2

Median and extreme values (minimum and maximum) of offensive, defensive, introductory and amicable behaviors during male-male dyadic encounters between A. agrarius and A. flavicollis, and interspecific significant differences revealed by Mann–Whitney U-test

Behavioral patterns

Median and extreme values

Spring

Autumn

A. agrarius

A. flavicollis

A. agrarius

A. flavicollis

Offensive behavior

3.0 (0–4.0)

5.0 (2.0–7.0)

1.0 (0–2.0)

1.0 (0–3.0)

U

Significant, U=4.5, P<0.05

Not significant, U=13.0

Defensive behavior

6.5 (5.0–11.0)

4.5 (2.0–5.0)

6.5 (2.0–8.0)

3.5 (1.0–6.0)

U

Significant, U=1.5, P<0.05

Not significant, U=6.0

Amicable behavior

3.0 (2.0–5.0)

2.0 (1.0–6.0)

7.0 (4.0–12.0)

5.0 (3.0–7.0)

U

Not significant, U=9.5

Not significant, U=5.5

Introductory behavior

12.0 (10.0–15.0)

10.5 (7.0–15.0)

10.0 (8.0–13.0)

8.0 (6.0–13.0)

U

Not significant, U=10.5

Not significant, U=10.0

The extreme values are given in brackets

Table 3

Median and extreme values (minimum and maximum) of offensive, defensive, introductory and amicable behaviors during female-female dyadic encounters between A. agrarius and A. flavicollis, and interspecific significant differences revealed by Mann–Whitney U-test

Behavioral patterns

Median and extreme values

Spring

Autumn

A. agrarius

A. flavicollis

A. agrarius

A. flavicollis

Offensive behavior

1.0 (0–3.0)

2.5 (1.0–3.0)

0 (0–1.0)

0 (0–1.0)

U

Not significant, U=12.0

Not significant, U=18.0

Defensive behavior

4.5 (2.0–8.0)

3.5 (1.0–6.0)

2.5 (2.0–4.0)

2.0 (0–4.0)

U

Not significant, U=10.5

Not significant, U=13.0

Amicable behavior

4.5 (1.0–7.0)

3.0 (0–5.0)

3.5 (2.0–6.0)

4.5 (3.0–8.0)

U

Not significant, U=11.5

Not significant, U=10.5

Introductory behavior

9.5 (9.0–20.0)

8.5 (3.0–12.0)

9.0 (6.0–11.0)

7.5 (5.0–10.0)

U

Not significant, U=11.5

Not significant, U=10.0

The extreme values are given in brackets

In autumn, the amicable contacts between males were significantly more frequent than those displayed by mice in spring (Mann–Whitney U test: U=3.0, P<0.05). However, the amicable behavior demonstrated by females remained infrequent during both studied periods. The occurrence of introductory behavior displayed by males and females of both species in their interactions was high in spring as well as in autumn. Nevertheless, in spring the events of introductory behavior were more frequent than those in autumn (Mann–Whitney U test: U=5.0, P<0.05 for male–male encounters, U=4.0, P<0.05 for female–female ones).

Attraction–avoidance to odor cues

In spring, males of both species showed an attraction to opposite-sex conspecific donors (t=2.28, P<0.05 for A. flavicollis; t=2.30, P<0.05 for A. agrarius, respectively), whilst the females were indifferent (Table 4). At the end of the breeding season both male and female A. agrarius and A. flavicollis displayed an attraction to same-sex conspecific donors (t=2.77, P<0.05 for male A. flavicollis, t=2.80, P<0.05 for female A. flavicollis; and t=3.5, P<0.05 for male A. agrarius, t=2.32, P<0.05 for female A. agrarius, respectively), but indifference to opposite-sex conspecific odors (Table 4).
Table 4

Category of responses of male and female A. agrarius and A. flavicollis to conspecific and heterospecific odors from the same and the opposite sex in spring and in autumn

Subjects

Donors

A. flavicollis

A. agrarius

Spring

Autumn

Spring

Autumn

M

F

M

F

M

F

M

F

A. flavicollis

 M

Indifference

Attraction

Attraction

Indifference

Avoidance

Indifference

Indifference

Indifference

t = −1.71

t=2.28*

t=2.77

t=1.25

t = −2.62*

t = −1.76

t = −1.17

t = −1.80

0:6:4a

5:5:0

7:2:1

4:5:1

1:3:6

0:8:2

1:6:3

0:6:4

−1.6±0.3b

2.2±1.0

3.0±0.3

1.4±1.1

−2.6±1.0

−1.2±0.7

−1.0±0.8

−2.0±1.1

 F

Indifference

Indifference

Indifference

Attraction

Avoidance

Avoidance

Indifference

Indifference

t=1.93

t = −2.09

t=0.81

t=2.80

t = −2.58*

t = −2.9*

t = −1.98

t = −1.46

5:5:0

1 : 4 : 5

2:8:0

5:5:0

0:6:4

1:3:6

1:7:2

1:5:4

2.0±1.0

−2.2±1.0

0.6±0.7

2.8±0.9

−1.8±0.7

−2.8±1.0

−2.4±0.6

−1.8±1.0

A. agrarius

 M

Avoidance

Avoidance

Indifference

Indifference

Indifference

Attraction

Attraction

Indifference

t = −5.00**

t = −2.71*

t = −1.81

t = −1.98

t = −1.90

t=2.30*

t=3.50

t=1.06

0:6:4

0:6:4

0:8:2

0:7:3

0:7:3

4:6:0

5:5:0

3:6:1

−2.6±0.7

−2.4±0.8

−1.2±1.0

−1.6±0.3

−1.4±0.7

2.0±0.9

2.6±0.7

1.0±1.0

 F

Avoidance

Avoidance

Indifference

Indifference

Indifference

Indifference

Indifference

Attraction

t = −3.67*

t = −4.02**

t = −1.20

t = −1.71

t=1.32

t = −1.71

t=0.32

t=2.32

0:6:4

0:5:5

0:7:3

0:6:4

3:7:0

0:6:4

3:6:1

5:5:0

−2.4±0.7

−3.4±0.8

−1.0±0.9

−1.6±0.9

1.2±0.9

−1.6±0.9

1.4±0.9

−3.2±0.9

The significance of differences revealed by paired t-test is shown: P<0.05*, P<0.01**

M males, F females

aNumber of animals displaying attraction:indifference:avoidance

bMean difference ± SE in the number of turns toward the stimulus minus the number of turns away from the stimulus

The response of male and female A. agrarius and male A. flavicollis to heterospecific odors from same to opposite sex donor was different from that described above. In spring, mice of both species showed avoidance of heterospecific odors from a same-sex donor (t = −2.62, P<0.05 for male A. flavicollis, t = −2.9, P<0.05 for female A. flavicollis; and t = −5.0, P<0.05 for male A.agrarius, t = −4.02, P<0.05 for female A. agrarius), and also of opposite-sex donors (t = −2.58, P<0.05 for female A. flavicollis, and t = −2.71, P<0.05 for male A.agrarius; t = −3.67, P<0.05 for female A. agrarius). Male A. flavicollis were indifferent to odors from female A. agrarius. In autumn, males and females of both species displayed indifference to heterospecific odors from same-sex and opposite-sex donors (Table 4).

Discussion

The differences in responses of A. agrarius and A. flavicollis to conspecific and heterospecific odors indicate that mice of both species probably can distinguish between odor cues from their own species and from a different species. Conspecific and heterospecific odor discrimination was reported in laboratory and field studies of various other rodents (Doty 1972, 1973; Nevo et al. 1976; Stoddart 1986; Sokolov et al. 1990; Heth et al. 1996; Christophe and Baudoin 1998; Gouat et al. 1998; Maslak and Gouat 2002). The avoidance of heterospecific odor, and the increased aggressiveness between mice of both species at the beginning of the breeding season, probably corresponds with the presence of interspecific competition for habitat resources. According to personal observations in syntopic habitats of north-west Bulgaria, the populations of A. agrarius and A. flavicollis frequently reach high density during the breeding period. In many rodent species under high density, females compete for limited offspring-rearing space. For instance, Sharpe and Millar (1991) reported that in Peromyscus maniculatus borealis the habitat of the nest site appeared to be essential for the reproductive success of females. In A. sylvaticus, the possession of a nest site of good quality is also very important for the female’s fitness (Musolf 2002). The indifference to heterospecific odors and decreasing of the level of aggressiveness, and the occurrence of introductory behavior in autumn could be linked with the end of the breeding period and forming of winter associations in their populations (Montgomery 1980; Kosoj 1984; Rosakis 1999). These behavioral tendencies, in combination with the differences in responses of males and females of A. agrarius and A. flavicollis to the same-sex conspecific odors at the beginning and the end of the breeding season, confirm the hypothesis that the seasonal changes in the patterns of behavior and the responses of the striped field-mice and the yellow-necked mice to conspecific and heterospecific odor cues are linked with seasonal variations in their lifestyle in the habitats. Many rodent and shrew species that inhabit regions with a climate of strong seasonal changes during the year and have a well-defined breeding season are asocial, or form territorial family units during the breeding season, whilst during the non-breeding season they live communally (Ferkin and Seamon 1987; Rychlik 1998; Gouat et al. 2003). The conspecific interactions and responses to conspecific odors also change across the seasons (Ferkin and Seamon 1987; Simeonovska-Nikolova 2004). The present research supports the aforementioned observations. At the start of the breeding season, males and females of both species showed indifference to same-sex conspecific odors, while at the end of the breeding season they demonstrated attraction to same-sex conspecific odors. The attraction response coincides with the formation of same-sex winter associations. Probably, two factors motivate this response. On one hand, associations provide more advantages in the form of energy- and water-saving, and on the other hand adult mice stop reproducing. The indifference response coincides with the period when males and females are less attracted to the scent of the other same-sex conspecifics. However, this response seems to be in contradiction with the presence of intraspecific aggressiveness found in A. flavicollis, A. sylvaticus, and A. agrarius during this period (Hoffemeyer 1973; Montgomery 1978; Gurnell 1978; Čihákova and Frynta 1996; Frynta et al. 1995), because the aggressive interactions suppose competition between conspecifics. Therefore, it could be suggested that the level of intraspecific competition in the studied populations is not high, or that mice responded indifferently to same-sex conspecific odors because they are habituated to them in the habitats. The results from the attraction–avoidance test indicated that at the beginning of the breeding season only males showed attraction to conspecific odors from the opposite sex, whilst females were indifferent to their own species’ odors of the opposite sex. When the animals respond differently to the stimulus depending upon the sex, sex-specific differences in urine odor are demonstrated. Sex-specific differences in urine odor have been described for many rodent species as well (Daly et al. 1978; Heth et al. 1996; Ferkin et al. 1995). The response of males in the present study could indicate that chemical communication between the sexes for reproduction is more important than for competition between same-sex individuals. Equally, the fact that females were indifferent to their own species’ odors of the opposite sex suggests that assessing male quality during the breeding season is more unimportant than any potential female–female competition. The preference for the smells of opposite-sex animals often is correlated with mating preference (Huck and Banks 1982;Newman and Halpin 1988; Egid and Brown 1989; Krakow and Matuschak 1991; Patris and Baudoin 1998). It is considered that in promiscuous species, male traits such as body weight or dominance are not crucial in mate choice decisions because promiscuity leads to relatively equal individual reproductive success (Musolf 2002). On this base, the indifference of females to conspecific odors from the opposite sex could be explained against the background of the promiscuous mating of the wood mice (Bartmann and Gerlach 2001; Musolf 2002) and the striped field-mouse (Baker et al. 1999). On the other hand, there are data that responses of adult male and female mammals to the odors of animals of the opposite sex can be modified by kinship and familiarity (Barnard and Fitzsimons 1988). Besides, female preference may be context- rather than species-dependent. For instance, Agrell (1997) found that female field voles M. agrestis preferred dominant males when density was low, and showed no preference when male density was high. So, further field and laboratory studies are required to clarify better the olfactory preferences of the striped field-mouse and the yellow-necked mouse to own species’ odor of the opposite sex according to their mating system and reproductive strategies. Nevertheless, the present study demonstrated some of the proximate mechanisms that maybe control their relationships in wild populations. It would be concluded that A. agrarius and A. flavicollis individuals respond to conspecific and heterospecific odors in a way which corresponds to their social life and the changing seasons. Although A. flavicollis seems to be more aggressive than A. agrarius, probably the avoidance response of striped field-mice and yellow-necked mice to heterospecific odors during the breeding season could serve as a spacing mechanism, or means to avoid aggressive encounters between two species in syntopic habitats.

Notes

Acknowledgements

I wish to thank Maria Miladinova for her help in the laboratory experiments and the two referees for their comments and recommendations for improving the standard of the present manuscript.

References

  1. Andrzejewski R, Babinska-Werka J, Gliwicz J, Goszczynski J (1978) Synurbization processes in population of Apodemus agrarius. I Characteristics of populations in an urbanization gradient. Acta Theriol 23:341–358 Google Scholar
  2. Agrell J (1997) Experimental testing of female mating strategies in microtine rodents. In: Abstracts of the Seventh International Theriological Congress, Acapulco, Mexico, p 5Google Scholar
  3. Baker RJ, Makova KD, Chesser RK (1999) Microsatellites indicate a high frequency of multiple paternity in Apodemus (Rodentia). Mol Ecol 8:107–111CrossRefPubMedGoogle Scholar
  4. Barnard CJ, Fitzsimons J (1988) Kin recognition and mate choice in mice: the effect of kinship, familiarity and social interference on intersexual interaction. Anim Behav 36:1078–1090CrossRefGoogle Scholar
  5. Bartmann S, Gerlach G (2001) Multiple paternity and similar variance in reproductive success of male and female wood mice (Apodemus sylvaticus) housed in an enclosure. Ethology 107:889–899CrossRefGoogle Scholar
  6. Bimova B, Karn R, Pialek J (2005) The role of ABP in reproductive isolation between two subspecies of house mouse: Mus musculus musculus and Mus musculus domesticus. Biol J Linnean Soc 84:349–361CrossRefGoogle Scholar
  7. Brown LE (1966) Home range and movement of small mammals. Symp Zool Soc Lond 18:111–142Google Scholar
  8. Brown LE (1969) Field experiments on the movements of Apodemus sylvaticus L. using trapping and tracking techniques. Oecologia 2:198–222CrossRefGoogle Scholar
  9. Brown RE (1979) Mammalian social odors: a critical review. Advan Study Behav 10:103–162Google Scholar
  10. Čiháková J, Frynta D (1996) Intraspecific and interspecific behaviour interactions in the wood mouse (Apodemus sylvaticus) and the yellow-necked mouse (Apodemus flavicollis) in a neutral cage. Folia Zool 45:105–113Google Scholar
  11. Cockel J, Ruf T (2001) Alternative seasonal strategies in wild rodent populations. J Mammal 82:1034–1046CrossRefGoogle Scholar
  12. Cox TR (1984) Ethological isolation between local populations of house mice (Mus musculus) based on olfaction. Anim Behav 32:1068–1077CrossRefGoogle Scholar
  13. Cox TR (1989) Odor-based discrimination between non-continuous demes of wild Mus. J Mammal 70:549–556CrossRefGoogle Scholar
  14. Christophe N, Baudoin C (1998) Olfactory preferences in two strains of wild mice, Mus musculus musculus and Mus musculus domesticus, and their hybrid. Anim Behav 56:365–369CrossRefPubMedGoogle Scholar
  15. Daly M, Wilson MI, Faux SF (1978) Seasonally variable effect of conspecific odors upon capture of deer mice Peromyscus maniculatus gambelli. Behav Biol 23:254–259CrossRefPubMedGoogle Scholar
  16. Dickman CR, Doncaster CP (1986) The ecology of small mammals in urban habitats. I Populations in patchy environmental. J Anim Ecol 56:629–640Google Scholar
  17. Dixon AK, Fisch HU (1989) The ethopharmacological study of drug induced changes in behaviour. In: Blanchard RJ, Brain PF, Blanchard DC, Parmigiani S (eds) Ethoexperimental approaches to the study of behaviour. Kluwer, Dordrecht, pp 451–473Google Scholar
  18. Doty RL (1972) Odor preferences of female Peromyscus maniculatus bairdi for male mouse odours of P. m. bairdi and P. Leucopus noveboracensis as a function of estrous state. J Compar Physiol Psychol 81:191–197CrossRefGoogle Scholar
  19. Doty RL (1973) Reactions of deer mice (Peromyscus maniculatus) and white-footed mice (Peromyscus leucopus) to homospecific and heterospecific urine odours. J Comp Physiol Psychol 84:296–303PubMedCrossRefGoogle Scholar
  20. Egid K, Brown JL (1989) The major histocompatibility complex and female mating preferences in mice. Anim Behav 38:548–550CrossRefGoogle Scholar
  21. Ferkin MH, Seamon JO (1987) Odor preference and social behavior in meadow voles, Microtus pennsylvanicus: seasonal differences. Can J Zool 65:2931–2937Google Scholar
  22. Ferkin MH, Sorokin ES, Johnston RE (1995) Seasonal changes in scents and responses to them in meadow voles: evidence for the co-evolution of signals and response mechanisms. Ethology 100:89–98Google Scholar
  23. Fowler J, Cohen L, Jarvis P (1998) Practical statistics for field biology. Wiley, Chichester Google Scholar
  24. Frynta D, Exnerová A, Nováková A (1995) Intraspecific behaviour interactions in the striped field-mouse (Apodemus agrarius) and its interspecific relationships to the wood mouse (Apodemus sylvaticus): dyadic encounters in a neutral cage. Acta Soc Zool Bohem 59:53–62Google Scholar
  25. Gouat P, Patris B, Lalande C (1998) Conspecific and heterospecific behavioural discrimination of individual odours by mound-building mice. C R Acad Sci 321:571–575Google Scholar
  26. Gouat P, Katona K, Poteaux C (2003) Is the socio-spatial distribution of mound-building mice, Mus spicilegus, compatible with a monogamous mating system? Mammalia 67:15–24CrossRefGoogle Scholar
  27. Gurnell J (1978) Seasonal changes in numbers and male behavioural interaction in population of wood mice, Apodemus sylvaticus. J Anim Ecol 47:741–755CrossRefGoogle Scholar
  28. Halpin ZT (1986) Individual odours among mammals: origins and functions. Adv Stud Behav 16:39–70CrossRefGoogle Scholar
  29. Heth G, Todrank J (1995) Assessing chemosensory perception in subterranean mole rats: different responses to smelling versus touching odours stimuli. Anim Beh 49:1009–1015CrossRefGoogle Scholar
  30. Heth G, Beauchamp GK, Nevo E, Yamazaki K (1996) Species, population and individual specific odors in urine of mole rats (Spalax ehrenbergi) detected by laboratory rats. Chemoecology 7:107–111CrossRefGoogle Scholar
  31. Hoffemeyer I (1973) Interaction and habitat selection in mouse Apodemus flavicollis and Apodemus sylvaticus. Oikos 24:108–116CrossRefGoogle Scholar
  32. Huck UW, Banks EM (1982) Differential attraction of females to dominant males: olfactory discrimination and mating preferences in the brown lemming (Lemmus trimucronatus). Behav Ecol Sociobiol 11:217–222CrossRefGoogle Scholar
  33. Hurst JL (1989) The complex network of olfactory communication on population of wild house mice Mus domesticus Rutty: urine marking and investigation within family groups. Anim Behav 37:705–725CrossRefGoogle Scholar
  34. Hurst JL (1990) Urine marking in population of wild house mice Mus domesticus Rutty. I: communication between males. Anim Behav 40:209–222CrossRefGoogle Scholar
  35. Kosoj ME (1984) Formation of winter aggregations in striped field-mouse (Apodemus agrarius) (In Russian). Zool Zh 63:1396–1402Google Scholar
  36. Krackow S, Matuschak B (1991) Mate choice for non-siblings in wild house mice: evidence from a choice test and a reproductive test. Ethology 88:99–108Google Scholar
  37. Laukaitis C, Critser E, Karn R (1997) Salivary androgen-binding protein (ABP) mediates sexual isolation in Mus musculus. Evolution 51:2000–2005CrossRefGoogle Scholar
  38. Lehner Ph (1996) Handbook of ethological methods. Cambridge University press, CambridgeGoogle Scholar
  39. Livoreil B, Gouat P, Baudoin C (1993) A comparative study of social behaviour of two sympatric ground squirrels (Spermophilus spilosoma, S. mexicanus). Ethology 93:236–246CrossRefGoogle Scholar
  40. Mackintosh JH (1981) Behaviour of the house mouse. Symp Zool Soc Lond 47:337–365Google Scholar
  41. Maslak S, Gouat P (2002) Short-term contact elicits heterospecific behavioral discrimination of individual odors in mound-building mice (Mus spicilegus). J Comp Psychol 116:357–362CrossRefPubMedGoogle Scholar
  42. Montgomery WI (1978) Intra and interspecific interaction of Apodemus sylvaticus (L.) and Apodemus flavicollis (Melchoir) under laboratory conditions. Anim Behav 26:1247–1254CrossRefGoogle Scholar
  43. Montgomery WI (1980) Spatial organization in sympatric populations of Apodemus sylvaticus and Apodemus flavicollis (Rodentia:Muridae). J Zool Lond 192:379–401CrossRefGoogle Scholar
  44. Musolf K (2002) Verhaltensökologische Untersuchung an Waldmäusen (Apodemus sylvaticus)—behavioral ecology studies of wood mice (Apodemus sylvaticus). PhD Thesis, Faculty of Biology, University of KonstanzGoogle Scholar
  45. Newman KS, Halpin ZT (1988) Individual odours and mate recognition in the prairie vole Microtus ochrogaster. Anim Behav 36:1779–1787CrossRefGoogle Scholar
  46. Nevo E, Bodmer M, Heth G (1976) Olfactory discrimination as an isolating mechanism in speciating mole rats. Experientia 32:1511–1512CrossRefPubMedGoogle Scholar
  47. Popov V, Sedefchev A (2003) The mammals in Bulgaria—handbook (In Bulgarian). Vitosha Library, Geosoft, Sofia, pp 144–145Google Scholar
  48. Patris B, Baudoin C (1998) Female sexual preferences differ in Mus spicilegus and Mus musculus domesticus: the role of familiarization and sexual experience. Anim Behav 56:1465–1470CrossRefPubMedGoogle Scholar
  49. Patris B, Gouat P, Jacquot C, Christophe N, Baudoin C (2002) Agonistic and sociable behaviours in the mound-building mouse, Mus spicilegus: a comparative study with Mus musculus domesticus. Aggress Behav 28:75–84CrossRefGoogle Scholar
  50. Peshev Tz, Nankinov D, Peshev D (2000) The handbook of the Bulgarian vertebrates (In Bulgarian). Bulvest Press, SofiaGoogle Scholar
  51. Rudran R, Kunz T (1996) Appendix 1. Ethics in research. In: Wilson DE, Cole FR, Nichols JD, Rudran R, Foster MS (eds) Measuring and monitoring biological diversity. Standard methods for mammals. Smithsonian Institution Press, Washington and London, pp 251–254Google Scholar
  52. Rosakis A (1999) Populationsgenetische Untersuchungen an Gelbhalsmäusen (Apodemus flavicollis). Diplomarbeit der Fakultät für Biologie, Universität Konstanz, GermanyGoogle Scholar
  53. Rychlik L (1998) Evolution of social systems in shrews. In: Wójcik JM, Wolsan M (eds) Evolution of shrews. Mammal Research Institute, Polish Academy of Sciences, Białowieża, pp 347–406Google Scholar
  54. Sharpe ST, Millar JS (1991) Influence on the variation in initiation of breeding in Peromyscus maniculatus. Can J Zool 69:698–705CrossRefGoogle Scholar
  55. Simeonovska-Nikolova D (2004) Seasonal changes in social behaviour and spatial structure of Crocidura leucodon in north-western Bulgaria. Acta Theriol 49:167–179Google Scholar
  56. Simeonovska-Nikolova D (2006) Social interactions in the striped field-mouse Apodemus agrarius (Mammalia: Rodentia, Muridae). Acta Zool Bulg 58(1) (in print)Google Scholar
  57. Sokolov VE, Kotenkova EV, Ljalukchina SI (1990) Biologija domovoj i kurganchikovoj mysej. (The biology of the House mouse and Mound-building mouse) Nauka, Moscow (in Russian)Google Scholar
  58. Stoddart DM (1986) The comparative responses of mice and moles to conspecific and heterospecific odours in the field—a lesson in social behaviour. In: Duvall D, Muller-Schwartze D, Silverstein RM (eds) Chemical signals in vertebrates IV. Plenum Press, New York, London, pp 533–550Google Scholar
  59. Stopka P, Macdonald DW (1999) The market effect in the wood mouse, Apodemus sylvaticus: selling information on reproductive status. Ethology 105:969–982CrossRefGoogle Scholar
  60. Talley H, Laukaitis C, Karn R (2001) Female preference for male saliva: implications for sexual isolation of Mus musculus subspecies. Evolution 55:631–634PubMedCrossRefGoogle Scholar
  61. White AM, RR Swaisgood, Zhang H (2004) Urinary chemosignals in giant pandas (Ailuropoda melanoleuca): seasonal and developmental effects on signal discrimination. J Zool 262:231–238CrossRefGoogle Scholar
  62. Wolton RJ, Flowerdew JR (1985) Spatial distribution and movements of wood mice, yellow-necked mice and bank voles. Symp Zool Soc Lond 55:249–275Google Scholar
  63. Yalden DV (1980) Urban small mammals. J Zool Lond 191:403–406Google Scholar
  64. Zgrabszyńska E, Piłacińska B (2002) Social relations in family group of wood mice Apodemus sylvaticus under laboratory and enclosure conditions. Acta Theriol 47:151–162Google Scholar

Copyright information

© Japan Ethological Society and Springer-Verlag 2006

Authors and Affiliations

  1. 1.Department of Ecology and Protection of Nature, Faculty of BiologySofia University “St. Kliment Ochridski”SofiaBulgaria

Personalised recommendations