Intra-family aggression and offspring expulsion in Mongolian gerbils (Meriones unguiculatus) under restricted environments

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Original investigation

Intra-family aggression and offspring expulsion in Mongolian gerbils (Meriones unguiculatus) under restricted environments By Elke Scheibler, R. Weinandy and R. Gattermann Institute of Zoology, Martin Luther University, Halle, Germany Receipt of Ms. 22.4.2004 Acceptance of Ms. 28.12.2004

Abstract Mongolian gerbils live in families consisting of a founder pair, to which reproduction is mainly restricted, and the offspring. They are described as cooperative breeder in which males and offspring act as helpers. Family dynamics have not been systematically investigated, particularly concerning the long-term consequences of periods of aggression. In a conceptual framework, promoting factors were investigated for the outbreak of aggression and its consequences on the families and on the individual level. Moreover, previously defined and described integrated (IFMs) and expelled family members (EFMs) were further characterized by frequent measurements of body mass and body composition. Six families were monitored for at least 1.5 years under controlled laboratory conditions. Regularly, the family composition and the individual state of each family member were inspected. In case of agonistic interactions, aggression periods were characterized by onset, number, duration, number of expelled animals and family size. First aggression period has been occurred 247.8737.7 days post-founding. As a consequence, family size was reduced significantly from 18.771.8 to 17.571.8 animals; the number of females decreased too from 10.671.8 to 9.771.8 females per family. All Mongolian gerbils experienced 2.470.2 aggression periods per life. All EFMs had a reduced body mass increase during aggression periods compared with integrated ones. Expelled males had a lower body mass than their integrated siblings; there was no such difference in females. In each aggression period, 2.670.2 adult animals per family were expelled. There was no sex-specific expulsion rate. Mainly founder females acted as aggressors (in 60% of all aggression periods). Up to three animals operated together aggressively, but mainly only one animal attacked the other family members (in 78% of all aggression periods). To conclude, animals of both sexes were excluded due to changes in family structure and an increased family size. Furthermore, females were expelled due to competition for exclusive reproduction. Males with lower body mass were more prone to be expelled, whereas in females no morphometrical characteristics favour the expulsion. r 2005 Elsevier GmbH. All rights reserved. Key words: Meriones unguiculatus, expulsion, body composition

1616-5047/$ - see front matter r 2005 Elsevier GmbH. All rights reserved. doi:10.1016/j.mambio.2004.12.002 Mamm. biol. 70 (2005) 3
137–146

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Introduction Mongolian gerbils are socially living rodents found in the semi-deserts and steppes in Mongolia and Manchuria. Families are based on a founder pair, to which reproduction is exclusively restricted. Sexual maturation of daughters is suppressed (Marston and Chang 1965; Adams and Norris 1973; Payman and Swanson 1980; Clark and Galef 2001). The founder male does not have exclusive access to the breeding female; even sons and males from adjacent families copulate with the founder female (Roper and Polioudakis 1976; Swanson and Lockley 1978; A˚gren 1981, 1984). The Mongolian gerbil is known for intensive pro-social behaviour such as communal foraging, grooming, defence of the family territory and cooperative breeding (Thiessen et al. 1977; Gromov 1981, 1990; Ostermeyer and Elwood 1984; Salo and French 1989; Weinandy and Gattermann 1999). Family members are identified by a family odour, which is mainly produced by the ventral gland of high-ranking family members such as founders (Thiessen et al. 1971). Aggression against non-family members is well known and interpreted as defence of the family territory (Ginsburg and Braud 1971; Reynierse 1971; Thiessen and Yahr 1977; Le Guelte et al. 1987; Gromov 1990). Moreover, intra-family aggressive behaviour has also been observed in the Mongolian gerbil. Although a sophisticated analysis is still lacking, the competition for reproductive access has been found as a major trigger (Roper and Polioudakis 1976; Swanson and Lockley 1978; Clark and Galef 2001). In order to further elucidate family dynamics, we previously suggested that there are three social categories in family groups based on aggressive interactions and parameters indicating stress: (1) founder pairs remained in their family and reproduced; (2) integrated family members (IFMs) remained in their natal family but did not reproduce; (3) expelled family members (EFMs) were attacked (Scheibler et al. 2004). Animals in these categories were further characterized by their body mass and body composition, because the parameters were developed to

illustrate the status of an animal, its resources and level of stress-implications (ground squirrels: Nunes et al. 1996, rats: Harris et al. 1998, murines: Breed and Taylor 2000). Changes in body composition may reflect the state of metabolic stress (rats: Zhou et al. 1999; golden hamsters: Wade et al. 1986; Meisel et al. 1990; mice: Laugero and Moberg 2000). The rapid, safe, in vivo technique of recording total body electrical conductivity (TOBEC) allows repeated determination of body composition and has been successfully applied to the Mongolian gerbil (Weinandy and Gattermann 2001). The following issues were addressed in the present investigation: (1) What are the causes for the outbreak of agonistic behaviour? (2) How can these periods of aggression be characterized? (3) What are the consequences for the families? Are there differences between the members of the social categories that explain the expulsion of some individuals but the retention of others in the family unit?

Material and methods Animals and housing conditions Six families of Meriones unguiculatus were each based on one founder pair. Females were from our laboratory breeding stock (Zoh: CRW) going back to three breeding pairs obtained from Charles River Wiga (Sulzfeld, Deutschland) in 1992. The founder males were descended from wild animals caught in 1995. Each founder pair was housed in an enclosure enriched with a sand bath as well as tree roots and limbs. Three enclosure sizes were used to produce different family densities. Two families were kept in an area of 1.5 m2, two on an area of 2.6 m2 and the remaining two on 4.3 m2. The floor of all enclosures was covered with wood shavings (Allspan Animal bedding, The Netherlands). Tap water and food pellets (Altromin GmbH Lage) were available ad libitum. Chow was supplemented with sunflower seeds, walnuts, fruits and hay. The temperature was 2573 1C and the light/dark conditions were 14:10 h (lights-on at 5 h am), the light intensity varied from 100–300 lx (light period) to 5 lx (dark period). All individuals (450 g body mass) were tagged by passive subcutaneous transponders (Trovan Ltd., UK). If there was a loss of all reproductive females, observation was broken up. Such a family group,

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consisting of males in this case, was not used and another was introduced into the enclosure. Observation periods lasted from 1.5 to 2.4 years per family.

Monitoring of families and assignment to social categories All families were monitored for at least 0.5 h daily beginning 2–3 h after lights on, i.e. between 7 and 9 am. In order to evaluate the situation as harmonious or aggressive, agonistic behaviour was recorded. The following categories of behaviour were recorded: chasing, one animal tried to escape by running while the aggressor followed close behind; biting, one animal was attacked by the aggressor which occurred after ano-genital inspection; appeasement, the appeasing animal licked the mouth of the aggressor or rubbed its backside on the ventral gland of the aggressor; keeping distance: one animal hid on or in cage structures while the aggressor patrolled the enclosure; food restriction: an aggressor keeps another animal away from food or water by biting and chasing . A ‘‘period of aggression’’ was defined as when at least one of the above mentioned behaviour patterns occurred repeatedly within one observation session and on subsequent days. The mean duration of a period of aggression was 18:4  1:3 days. The intervals without aggressive interactions were labelled as harmonious periods. In general, presentation of data started with the first aggression period and ended with the last one. Based on Scheibler et al. (2004), family members were assigned to one of three different social categories. Individuals living in their families for their whole life, without reproducing and without being attacked, were categorized as IFMs. Animals that were chased, attacked aggressively and prevented from feeding were removed for ethical reasons when such behaviour or wounds were detected. These animals were termed EFMs. The founder pair was the third group of animals. Due to their low number, their relatively higher age and their regular reproduction they were not included into the comparative analysis of body mass and body composition. However, they were included into the family characteristics such as family size, family density, sex ratio and mean age of family members.

Morphometrical features Measurements of body mass were done weekly with a digital balance (Kerns 440-45, precision 0.1 g). Measurements of body composition were

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carried out every 4–6 weeks depending on the family situation. Measurements were taken only when the situation was harmonious and not during a period of aggression. The determination of body composition was performed using an EM-SCAN SA 3000 small animal body composition analyser (EM SCAN Inc. Springfield, IL, USA), including a base unit (No. SA3B06996) and a detection chamber (No. SA3057, chamber-diameter 57 mm). Animals were anaesthetized by transferring them into a glass container in which ‘‘Forene’’ was added (active component: Isofluran-Baxter, Baxter Deutschland GmbH, UnterschleiXheim, Germany). Animals were fully sedated after 1 min and were then placed in the measuring chamber. Two to four measurements per animal were taken over a 4–7min period, depending on the state of sedation, and the resulting mean value was used for further analyses. After measurement, animals were reintroduced into their enclosures (for further details see Weinandy and Gattermann 2001). Since body mass and body composition are age and sex specific parameters, separate calculations were performed on males and females and for different age classes.

Statistics Statistical analysis was carried out with SPSS 12.0. Normally distributed data (Kolmogorov–Smirnov: number of male EFM/AP: Z ¼ 0:291; n ¼ 40; P ¼ 0:121; number of female EFM/AP: Z ¼ 0:291; n ¼ 40; P ¼ 0:121; family size start AP: Z ¼ 0:241; n ¼ 6; P ¼ 0:2; family size end AP: Z ¼ 0:243; n ¼ 6; P ¼ 0:2; family density start AP: Z ¼ 0:235; n ¼ 6; P ¼ 0:2; family density end AP: Z ¼ 0:253; n ¼ 6; P ¼ 0:2; number of males start AP: Z ¼ 0:232; n ¼ 6; P ¼ 0:2; number of males end AP: Z ¼ 0:184; n ¼ 6; P ¼ 0:2; number of females start AP: Z ¼ 0:259; n ¼ 6; P ¼ 0:2; number of females end AP: Z ¼ 0:270; n ¼ 6; P ¼ 0:19; sex ratio start AP: Z ¼ 0:281; n ¼ 6; P ¼ 0:15; sex ratio end AP: Z ¼ 0:239; n ¼ 6; P ¼ 0:2; age of family members start AP: Z ¼ 0:267; n ¼ 6; P ¼ 0:2; age of family members end AP: Z ¼ 0:200; n ¼ 6; P ¼ 0:2; family size in HP: Z ¼ 0:295; n ¼ 6; P ¼ 0:113; family density in HP: Z ¼ 0:249; n ¼ 6; P ¼ 0:2; sex ratio in HP: Z ¼ 0:220; n ¼ 6; P ¼ 0:2; age of family members in HP: Z ¼ 0:187; n ¼ 6; P ¼ 0:2) were analysed with parametric t-tests. Results are given as mean values, the statistical measure of variance is the standard error of mean (SEM). As body mass varied within a wide range, all morphometrical data of individuals were used as non-parametric data (Komogorov–Smirnov: males (n ¼ 24): body mass: 4 weeks until expulsion: Z ¼ 0:232; P ¼ 0:002; 1 week until expulsion: Z ¼ 0:302; P ¼ 0:000; expulsion: Z ¼ 0:300; P ¼ 0:000;

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weekly body mass increase in aggression periods: IFM (n ¼ 20): Z ¼ 0:196; P ¼ 0:043; EFM (n ¼ 28): Z ¼ 0:128; P ¼ 0:2; relative fat mass: 4 weeks until expulsion: Z ¼ 0:120; P ¼ 0:2; expulsion: Z ¼ 0:186; P ¼ 0:07; relative body water: 4 weeks until expulsion: Z ¼ 0:115; P ¼ 0:2; expulsion Z ¼ 0:164; P ¼ 0:095; females (n ¼ 39): body mass: 4 weeks until expulsion: Z ¼ 0:188; P ¼ 0:001; 1 week until expulsion: Z ¼ 0:157; P ¼ 0:017; expulsion: Z ¼ 0:118; P ¼ 0:118; weekly body mass increase in aggression periods: IFM (n ¼ 11): Z ¼ 0:147; P ¼ 0:2; EFM (n ¼ 56): Z ¼ 0:114; P ¼ 0:07; relative fat mass: 4 weeks until expulsion: Z ¼ 0:124; P ¼ 0:2; expulsion: Z ¼ 0:128; P ¼ 0:2; relative body water: 4 weeks until expulsion: Z ¼ 0:126; P ¼ 0:118; expulsion: Z ¼ 0:098; P ¼ 0:2; males: body mass: IFM (n ¼ 10): Z ¼ 137; P ¼ 0:2; EFM (n ¼ 15): Z ¼ 0:250; P ¼ 0:003; relative fat mass: IFM: Z ¼ 0:243; P ¼ 0:183; EFM: Z ¼ 0:177; P ¼ 0:2; relative body water: IFM: Z ¼ 0:242; P ¼ 0:185; EFM: Z ¼ 0:152; P ¼ 0:2; females: body mass: IFM (n ¼ 10): Z ¼ 165; P ¼ 0:2; EFM (n ¼ 33): Z ¼ 0:099; P ¼ 0:2; relative fat mass: IFM: Z ¼ 0:234; P ¼ 0:2; EFM: Z ¼ 0:234; P ¼ 0:2; relative body water: IFM: Z ¼ 0:224; P ¼ 0:2; EFM: Z ¼ 0:224; P ¼ 0:000). All values of body mass were used a non-parametric ones. These data were given as median values and the interquartile-range as the measure of variance; and were analysed with nonparametric w2 -tests, Mann–Whitney U tests and Wilcoxon tests. The number of animals contributed to various parameters is given in the text and the graphs; due to the experimental set-up it is not equal across all calculations. Differences were accepted at Po0:05: In the graphs the level of significance was expressed by asterisks: **Po0:01 and ns=not significant.

Results Triggering factors for the outbreak of aggression Family level All periods of aggression were analysed with regard to potential triggering events. The main trigger was the loss of a founder female, which occurred in 25% of these periods. Harmonious family life was reinstated only after replacement of this female by another successfully reproducing female from the family group. In contrast, the loss of a founder male was less influential as only 5.0% of all aggression periods occurred after

the loss of the founder male and 2.5% of the harmonious periods happened after this event without any consequences. Another potential trigger for aggressive periods was reproductive competition, as a concurrence for exclusive access to reproductive success by giving birth of own young. Cases in which daughters were gravid or gave birth to litters were observed 8% of the time just before aggressive periods and never during harmonious periods. The exclusive position of the founder female was endangered by such a gravid or breeding daughter. The reproductive competition that had this effect was competition from a daughter. Nevertheless, the overthrow and displacement of a founder female was a rare event which occurred only once. In all other cases the founder female attacked the competing daughter vigorously. After expulsion the daughter’s pups were sometimes adopted by the mother or rather by the founder female, who acted as aggressor. Family size and density, sex ratio and mean age of adult family members within the six families investigated were evaluated as potential triggers. There were no significant differences for any of these traits between periods of aggression and harmonious periods. Mean family size was 18:6  2:0 animals per family during harmonious and 18:7  1:8 at the start of aggression periods (T ¼ 0:27; ns). Family density was 7:8  1:4 animals/m2 during aggression periods in contrast to 7:7  1:3 in the rest of the time (T ¼ 0:07; ns). Both the sex ratio (harmonious: 1 : 1:4  0:3; aggression: 1:1:5  0:3; T ¼ 0:37; ns) and the mean age of adult family members (harmonious periods: 33:4  1:4 weeks; aggression periods 33:5  1:3 weeks; T ¼ 0:058; ns) did not differ. Individual level Physical trait of expelled and integrated family members: Body mass, relative fat mass and relative total body water was analysed in all animals of both sexes from week 26 to 40. This period was chosen in order to consider adult animals of the same age in the two social categories. The only difference we found was in the body mass of males, where IFMs (n ¼ 10) had a body mass of 78.1 g

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(interquartile range 17.9) and the EFMs (n ¼ 15) showed a lower body mass of 65.5 g (interquartile range 9.7; Mann–Whitney U test: U-value: 75; P ¼ 0:02). Animals of both categories showed an increase in body mass during ontogeny, but there was no difference in the course of the growth curves of these two categories (Repeated ANOVA/ Pillai Spur: body mass: F ¼ 7:896; df ¼ 18; P ¼ 0:029; body mass*category: F ¼ 0:804; df ¼ 18; P ¼ 0:7). Relative fat mass was 13.6% (interquartile range 16.2) in IFM and 13.3 (interquartile range 6.1) in EFM and did not differ (Mann–Whitney U test: U-value: 42; ns). The same was found in relative total body water of IFM (60.2%, interquartile range 11.3) and of EFM (60.3%, interquartile range 4.5; Mann–Whitney U test: Uvalue: 43; ns). No differences were found in any of the morphometrical data of female IFMs and EFMs: body mass of IFM (n ¼ 10) was 62.6 g (interquartile range 9.9) and EFM (n ¼ 33) had 63.4 g (interquartile range 12.4). As in males, there was no difference in the growth curve for females that were integrated for their whole life and those that were expelled (repeated ANOVA/ Pillai Spur: body mass: F ¼ 3:249; df ¼ 18; P ¼ 0:025; body mass*category: F ¼ 0:657; df ¼ 18; P ¼ 0:8). IFM showed a relative fat mass of 12.5% (interquartile range 5.7), while it was 11.5% (interquartile range 5.2) in EFM. Relative total body water was 60.8% (interquartile range 4.0) in IFM and 61.7% (interquartile range 3.7) in EFM. Characterization of intra-family aggression Over the entire period of observation (1.9 years) there were 6:7  1:2 aggression periods were observed per family (summing up to 40 aggression periods within the six families). The first aggression period was observed 247:8  37:7 days after the founding male and female were paired. In the course of each of the agonistic encounters, 2:6  0:2 animals were expelled, which corresponded to 16:9  2:9% of the initial number of animals. There was no sex-specific expulsion rate (1.0 males and 1.6 females per aggression period; w2 ¼ 0:14; ns). Every 51:5  12:6 days an aggression period occurred with a mean duration of

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18:4  1:3 days. Therefore, aggressive interactions covered a time of 17:4  3:2% in a family’s life. Although the final expulsion of family members occurred after a varying length of time, the underlying process of expulsion followed similar principles. Initially, a segregation of family members took place in which some were separated or removed themselves and subsequently rested alone. Next, an increase in aggressive behaviour was displayed by the females of the founder pair and an increase in appeasement behaviour was shown by the offspring towards the aggressors, independent if the young were attacked or not. Elevated locomotor activity and biting attacks eventually indicated the aggression periods. The level of aggression varied among the aggressors and hence influenced the families and their dynamics distinctively. Aggressors During all periods of aggression, only 15 out of 156 animals acted as aggressors. The majority of them were females (66.7%). In 50% of all aggression periods, the aggressive females were pregnant or lactating. Pup mortality during aggressive periods was 69:9  8:0%: The assignment of the aggressors to the different social categories was: female FPA 60%, female future EFM 7%, male FPA 13% and male future EFM 20%. Since the mean age was 49:7  5:0 weeks when they initially acted as aggressors, they were older compared to the EFMs (33:7  1:6 weeks, n ¼ 105). Per aggression period, up to three animals acted together aggressively versus the others (in 2.5% of all aggression periods); just one aggressor was observed in 77.5%, and two animals in 20.0%. Consequences of aggression As expected on family level, the aggression periods led to a significant decrease of family size and density (Table 1). Neither the sex ratio nor the mean age of family members was influenced by aggressive interactions. On individual level body mass changes were measured at the beginning and at the end of each of the aggression periods. Data were not

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influenced by the respective age, since these attacks occurred at different times in each animal’s life. The mean change of body mass in aggression periods is shown in Fig. 1. Male IFM had the highest body mass change and their body mass changed by 1.3 (interquartile range 2.5) g per week. In male EFM (n ¼ 28) it was 0.6 g per week (interquartile range 1.4). The difference between the categories was significant (Mann–Whitney U test: U-value 152.5, P ¼ 0:008). There was no such difference in females (Mann–Whitney U test: Uvalue 209.5, ns); IFM females (n ¼ 11) had an increase of 1.8 g per week (interquartile range 2.4), and EFM females (n ¼ 56) had 0.6 g per week (interquartile range 2.0). EFMs (n ¼ 105) experienced in the mean 2:1  0:1 aggression periods, which means that they experienced one aggression period without being attacked and in a later one they were expelled. An investigation of body mass and body composition during the last 4 weeks of life is presented in Table 2 for those expelled. There was no change in either males or females (Wilcoxon: males: body mass: Z-value 0.106; ns; relative fat mass: Z-value 0.597, ns; relative body water: Z-value 0.686; ns; females: body mass: Z-value 0.937; ns; relative fat mass: Z-value 0.803, ns; relative total body water: Z-value 1.675; ns). Animals expelled showed no change in body mass within the last week before expulsion. Male EFM had a body mass of 65.7 g (interquartile range 12.9) 6–8 days before being expelled and 65.1 g (interquartile range 9.5) (n ¼ 24; Wilcoxon: Z-value 1.9; ns) when they were removed. The expelled females showed a mean body mass of 66.7 g (interquartile range

15.1) 6–8 days before being expelled and 64.6 g (interquartile range 13.9) at expulsion (n ¼ 39; Wilcoxon: Z-value 1.80; ns).

Discussion The purpose of the current long-term laboratory study was to further elucidate the causes and consequences of intra-family aggression in the Mongolian gerbil in order to reveal the underlying mechanisms and the possible functions of these patterns of behaviour. Three factors were described and evaluated as possible triggers for agonistic interactions among the family members. As expected due

6

weekly body mass increase (g)

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4

**

2

0

-2 male IFM

male EFM

female IFM

female EFM

Fig. 1. Weekly change of body mass (g) in aggression periods in males and females. Given are medians (interquartile range). Males: IFM (n ¼ 20), EFM (n ¼ 28; Mann–Whitney U test: U-value: 152.5) and females: IFM (n ¼ 11), EFM (n ¼ 56; Mann–Whitney U test: U-value: 210). The two asterisks **indicate Po0:01:

Table 1. Family trait at start and end of aggression periods in the six families. Given are mean values 7 standard error of mean. Trait

Size (n) Density (n/m2) Sex ratio Age of members (weeks)

Start

18.771.8 7.871.4 1.570.3 33.571.3

End

17.571.8 7.371.3 1.470.3 33.471.5

Paired-samples t-test T-value

Significance

2.993 2.983 1.176 0.066

P ¼ 0:03 P ¼ 0:03 NS NS

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Table 2. Body composition of the expelled males (n ¼ 24) and females (n ¼ 39) within the last 4 weeks until expulsion. Given are the medians (interquartile range). Body composition

Body mass (g) Relative fat mass (%) Relative total body water (%)

Expelled males

Expelled females

4 weeks before expulsion

Day of expulsion

4 weeks before expulsion

Day of expulsion

66.2 (17.5) 11.7 (11.1) 63.1 (8.8)

65.1 (9.5) 10.7 (10.3) 62.2 (5.0)

63.0 (9.6) 11.2 (9.8) 64.3 (7.2)

64.6 (13.9) 10.7 (7.9) 62.2 (6.3)

to the prominent role of the founder or reproductive female (Swanson and Lockley 1978; Ostermeyer and Elwood 1984; Weinandy and Gattermann 1999), competition for this exclusive rank between the mother and her daughters was an unambiguous cause for the outbreak of aggression. This threat of the founder female to her position is a permanent one, and therefore she seems to stabilize her status by the expulsion of potential female rivals. Due to that, only two out of 56 nonfounder females were able to give birth. Mature females that copulated and therefore actively strived for reproductive success were attacked by the mother. As a consequence there was only one reproducing female per family. A further trigger for intra-family aggression was the loss of a founder female due to aging; that led to a radical change of the family structure. Overthrowing a founder female was just observed in cases where such an old founder female was not able to attack competing daughters. The two factors competitive females and aged founder female were necessary for the overthrow of such a dominant animal. Because both females and males were expelled and since the family size was always reduced during aggressive periods, the low number of family members appeared to be another promoting factor for aggression. This is in concordance with Hull et al. (1973), who showed that aggression and group size are positively correlated. It is possible that the expulsion of family members in the Mongolian gerbil serves for a stable family size in an optimal range. An aggressive period with the expulsion of young can be seen as result of a family size increase during the harmonious periods.

During this long-term experiment, the majority of the offspring (73%) was expelled and this strongly points to a parent–offspring conflict (Trivers 1972; Huntingford and Turner 1987). Under natural conditions, the dispersion of young is often caused by an increase of aggressive behaviour starting from the residents against offspring (Holekamp 1986; Smale et al. 1997). As described for mammals in general (Kleimann 1977, 1979), aggressive behaviour within families occurs if the maintenance of the existing social structure is threatened by the offspring. That is most probably the reason why animals will be attacked when they act as competitors. In a recent study, the assignment of the offspring into two social categories was performed on the basis of aggressive interactions (Scheibler et al. 2004). The first category was the EFMs and the majority of the animals belonged to this group. The second category, the IFMs were never attacked and did not reproduce throughout their lives. Whether such a distinction exists under natural conditions, remains open for future studies. However, the current laboratory study with its limitations (no dispersal possibilities and closed family groups) allowed us to obtain some insights into the mechanisms underlying family dynamics. In the families investigated the dynamics were mainly influenced by the females. Aggressive behaviour was sex-specific (females: 67%, males: 33%). In general, the aggressors were older and therefore heavier than those that were attacked. A high body mass is an advantageous factor for the outcome in a conflict, but for some purposes it is more useful to analyse the body

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composition (Raffel et al. 1996: female guinea pigs (Cavia porcellus); Nunes and Holekamp 1996: Belding0 s ground squirrels (Spermophilus beldingi). Moreover, body composition and migration are most probably linked, as dispersal behaviour under natural conditions mainly occurs if the animals have sufficient energetic reserves. In order to further describe the expelled and the IFMs and to evaluate the influence of aggression, body mass and body composition were both chosen as indicators for individual well-being and for estimating individual resources. Expelled males showed a lower body mass throughout their ontogeny compared to the integrated ones of the same age. Therefore, the integrated males might be more successful in agonistic interactions. A further hint for the expulsion of light males and their higher involvement during aggressive periods was shown by the more pronounced body mass increase of integrated males during aggression periods compared to the lower body mass increase of expelled ones. Moreover, integrated males were rarely involved in aggression and since they also displayed appeasement behaviour they were not attacked and chased by the aggressors. Expelled females in the current study tended to have a higher body mass throughout their lives. Concerning this it can be supposed that females were expelled due to their mature stage and therefore acted as competitors for the founder female; while expelled males displayed characteristics of low ranking family members. It was shown by others, that the individual’s experience determines its success in fights or intra-specific conflicts as a further factor in the outcome of an aggressive interaction (Hsu and Wolf 2001). Francis (1988) rated individual aggressiveness as another factor associated with dominance.

The higher level of experience and aggressiveness might be another advantage for the founder females in interactions with inexperienced lower ranking females as they experienced between five and seven aggression periods compared to expelled individuals, that were excluded after two. There were only slight differences in body composition at the end of the period of expulsion. This can be explained by the ad libitum food availability and the experimental set-up, which was designed to avoid harm to the animals. To sum up, under restricted environments three main factors emerged as probable causes of family aggression: (a) female competition for reproduction; (b) change of family structure; (c) family size. As a consequence of aggression, the number of animals within the family group was reduced. The expulsion rate was irrespective of sex and integrated and expelled animals differed only slightly with respect to body mass and body composition. Expelled males were evaluated as lightweight and were therefore more pronounced for low rank positions. Expelled females were heavier and older than the integrated ones and therefore potential competitors for the aggressor.

Acknowledgements The authors thank I. Haufe for her assistance in running the statistics, P. Fritzsche for his valuable comments on the manuscript and K. Williams and R.E. Johnston for providing helpful comments on the manuscript and revising the English. We are grateful to B. Gebhardt for her fine assistance. We thank the Federal State of Sachsen Anhalt for approving the grant (3375A/0021 M).

Zusammenfassung Innerfamilia¨re Aggression und Ausgrenzung von Familienmitgliedern bei der Mongolischen Wu¨stenrennmaus (Meriones unguiculatus) unter Laborbedingungen Mongolische Wu¨stenrennma¨use (M. unguiculatus) leben in territorialen Familien, die aus einem Stammpaar und deren Nachkommen bestehen. Da das Stammweibchen und adulte Ma¨nnchen die

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reproduzierenden Rollen einnehmen und alle anderen Nachkommen lediglich als Helfer agieren, wird diese Art als kooperativ beschrieben. Im Rahmen einer Langzeitstudie untersuchen wir Auslo¨ser aggressiven Verhaltens und die Konsequenzen auf familia¨rer und individueller Ebene. Daru¨ber hinaus wurden durch wiederholte Messungen der Ko¨rpermasse und ihrer Zusammensetzung die beschriebenen Kategorien der Familienmitglieder charakterisiert. Es wurden sechs Familien u¨ber einen Zeitraum von mindestens 1,5 Jahren beobachtet und regelma¨Xig ihre Zusammensetzung kontrolliert. Trat agonistisches Verhalten wiederholt auf, so wurde eine solche Aggressionsphase durch den Zeitpunkt des Auftretens, Ha¨ufigkeit, Dauer, Anzahl der verstoXenen Tiere und die Familiengro¨Xe charakterisiert. Aggression trat erstmals 247:8  37:7 Tage nach der Verpaarung auf, in deren Verlauf im Mittel 2:6  0:2 Tiere verstoXen wurden, wodurch die Familiengro¨Xe von anfa¨nglich 18:7  1:8 auf 17:5  1:8 Tiere pro Familie reduziert wurde. Das Geschlechterverha¨ltnis war sowohl in den Familien wa¨hrend der Aggressionsphasen als auch unter den VerstoXenen ausgeglichen. Alle Tiere erlebten im Mittel 2:4  0:2 Aggressionsphasen. Aggressoren traten hauptsa¨chlich (77%) allein auf und waren in 60% der Fa¨lle Stammweibchen. VerstoXene Ma¨nnchen zeichneten sich durch eine geringere Ko¨rpermasse gegenu¨ber den integrierten Ma¨nnchen aus, wohingegen bei den Weibchen keine Unterschiede gefunden wurden. Agonistisches Verhalten wirkte sich auf die VerstoXenen beider Geschlechter durch eine verringerte Ko¨rpermassezunahme im Verlauf von Aggressionsphasen aus. Zusammenfassend konnten die Konkurrenz um das weibliche Reproduktionsmonopol, die Vera¨nderungen in der Familienzusammensetzung sowie die Familiengro¨Xe als Ursachen fu¨r das Auftreten von Aggression ermittelt werden. Weibchen wurden aufgrund ihrer Konstitution und ihrer reproduktiven Potenz von dem Stammweibchen verstoXen, wa¨hrend im Gegensatz dazu besonders leichte Ma¨nnchen pra¨destiniert waren, ausgegrenzt zu werden. r 2005 Elsevier GmbH. All rights reserved.

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Authors’ address: Elke Scheibler, Rene´ Weinandy and Rolf Gattermann, Zoologisches Institut, Domplatz 4, D-06108 Halle/ Saale (e-mail: [email protected].)