Directory UMM :Data Elmu:jurnal:A:Applied Animal Behaviour Science:Vol70.Issue2.2000:

Social interactions among captive brushtail

possums (

Trichosurus vulpecula

)

T.D. Day

a,b,*

, C.E. O'Connor

a

, J.R. Waas

b

, L.R. Matthews

a a_{Animal Behaviour and Welfare Research Centre, AgResearch Ruakura, Private Bag 3123,}

Hamilton, New Zealand

b_{Department of Biological Sciences, University of Waikato, Private Bag 3105,} Hamilton, New Zealand

Accepted 1 May 2000

Abstract

A biological control strategy relying on a self-disseminating agent may provide the only affordable long-term technique for reducing brushtail possum (Trichosurus vulpecula) numbers throughout New Zealand. The objective of this study was to determine the frequency and patterns of social interactions in single and mixed-sex groups of possums, in order to identify interactions that may assist in the dissemination of biocontrol agents. Thirty-two sexually mature wild-caught possums (16 female, 16 male) were housed in captive groups (of four) in enclosures during the breeding and non-breeding seasons. Groups consisted of either all females, females and males or all males. Four types of social interactions were de®ned: threats, ®ghts, af®liative and sexual interactions. Interactions only occurred between two animals at one time and were most frequent in the non-breeding season. Within all female groups, possums readily engaged in interactions that had either an agonistic or af®liative nature. Mixed-sex groups interacted less frequently than females, but also engaged in both agonistic and af®liative interactions. In contrast, possums in all male groups rarely interacted, with only a few ®ghts and no af®liative interactions observed. Some mixed-sex dyads appeared to `associate' during the breeding period. Young were produced by three females that regularly associated with a male and one female that showed little associative behaviour. Given the different interaction patterns observed in each group type, biological control agents that rely on speci®c interaction patterns for dissemination, are likely to spread at different rates among different possum groups and in different seasons.#2000 Elsevier Science B.V. All rights reserved.

Keywords: Brushtail possum; Social behaviour; Biological control

*_{Corresponding author. Tel.:‡64-7-838-5560; fax:‡64-7-838-5727.} E-mail address: dayt@agresearch.cri.nz (T.D. Day).

1. Introduction

Brushtail possums (Trichosurus vulpecula) are Australian marsupials that were intro-duced to New Zealand in the 1840s to establish a fur trade (Pracy, 1974). They are nocturnal, mainly arboreal and omnivorous. Despite attempts to control them, possums now occupy more than 90% of the country, occurring at densities up to 20 times that found in Australia (Cowan, 1990). In New Zealand, possums seriously threaten the livestock industry as they are important vectors in the spread of bovine tuberculosis (Mycobacterium bovis; Tb) to cattle and deer (Livingstone, 1991). They also cause severe damage to native plants by selective browsing (Nugent, 1995) and adversely affect native fauna through competition, disturbance and predation (Innes, 1995). Biological control, relying on a self-disseminating control agent, may be the only option for achieving an affordable long-term reduction in possum numbers throughout New Zealand (Jolly, 1993). Some behaviours or social interactions in the possum may facilitate the spread of biological control agents.

Free-living possums are usually solitary (Winter, 1976), have widely overlapping home ranges (Green, 1984) and do not defend a territory within their range (Winter, 1976). Wild possums are suggested to spend little time on active social interaction, except during the breeding season (Winter, 1976). Interactions usually only occur between a pair of possums at one time, with groups rarely acting as a cohesive social unit (Winter, 1976). After initial interactions, dominance is maintained without further interaction by mutual avoidance of co-dominants (Winter, 1976; Biggins and Overstreet, 1978). Female possums are usually dominant to males, with older and larger possums dominating small young animals (Jolly, 1976; Biggins and Overstreet, 1978).

The social organisation and behaviour of possums have been studied in both wild and captive situations. Typically research has focused on dominance relationships (e.g. Biggins and Overstreet, 1978; Jolly et al., 1996), mating behaviour (e.g. Oldham, 1986) and ecological aspects of the possum's social organisation (e.g. Jolly, 1976; Winter, 1976; Green, 1984). No studies to date have quanti®ed the frequencies and patterns of social interactions between single and mixed sex groups of possums in different seasons. The objective of this study was to quantify the frequency and patterns of social interactions among single and mixed-sex groups of captive possums, in order to identify interactions that may facilitate or restrict the dissemination of biological control agents.

2. Materials and methods

2.1. Subjects and housing

two males and two females) were housed together in grass enclosures during the non-breeding (December 1996±February 1997) or non-breeding (March 1997±May 1997) seasons. The four groups that were housed together in the non-breeding season remained in their groups throughout the breeding season in addition to the four new groups. Each grass enclosure (size range 50±130 m2) contained suf®cient wooden dens for all animals and had two climbing logs and an ad libitum supply of pellet food and water. As far as possible, possums within each group were from the same population and were of similar age and body weight.

2.2. Procedure

Possums in each group were given a 3 cm1.5 cm eartag (yellow, red or blue; All¯ex1 New Zealand, Ltd.) to allow us to identify individual animals from a distance. Each group was observed for a 3 h period from `civil twilight' (30 min after sunset) during their ®rst night in an enclosure together, and on four further nights during the following 6 weeks. The observer was positioned behind a glass window, in an elevated central observation tower, approximately 5 m from the nearest part of the enclosures. Ten white spotlights (100 W) were used to provide suf®cient illumination in the enclosures (about 20 lx) for possum behaviour to be recorded. This light level was similar to bright moonlight and did not deter the possums from using the enclosures.

All social behaviours shown by a possum that were directed towards another possum (from less than 1 m away) were recorded. The behaviour de®nitions of Winter (1976), Biggins and Overstreet (1978), Day (1996) and Hickling and Sun (2000) were used to de®ne the observed behaviours. Each sequence of behaviours shown by a dyad (pair of possums) while remaining within 1 m, was then classed into one of four interaction types: (1) threat, which involved no physical contact (glare, vocalise, bipedal threat, swipe, lunge and chase behaviours); (2) ®ght, which always involved physical contact (boxing, pounce and ®ght behaviours); (3) af®liative (touch, food share and allogroom behaviours); and (4) sexual (mating) interactions. Each interaction began with an `approach' by one possum and ended with one animal `leaving' (Day, 1996). The frequency and patterns of interactions were compared, during the breeding and non-breeding seasons, for the three group types: (1) all female; (2) mixed-sex; and (3) all male. Within each group, the interactions of each type of dyad (female±female, male±female, male±male) in both seasons were also compared (six dyads per group, four groups in non-breeding season, eight groups in breeding season, 72 dyads in total). All of the female possums were examined at 14-day intervals for evidence of pouch young, to help determine if mating had occurred (i.e. outside the observation period).

2.3. Statistical analysis

mean interaction frequencies and their standard errors were calculated. For individual interaction types, standard errors could not be calculated, as the individual cage variation in interaction frequency was too large to average the standard error terms. Therefore, standard errors of the differences between seasons or group types are presented. The Wald test for ®xed effects (Wald statistic; Genstat 5 Committee, 1993) was used to determine which factors had signi®cant effects on interaction frequencies.

For each possum within each group type the probability of it being involved in an interaction of a speci®c type in a speci®ed season was modelled. A quasi-independence test was used for each dyad to determine whether that dyad performed speci®c interactions more or less frequently in either season than would be predicted by random interactions (Larntz and Weisberg, 1976). More interactions than predicted in the quasi-independence test would suggest some non-random `association' between the possums in that dyad, whereas fewer interactions would suggest some `separation' (although not necessarily deliberate) between the dyad. All statistical analyses were performed using the Genstat 5 statistical analysis package (Release 3.1; Lawes Agricultural Trust, Rothamsted Experi-mental Station).

3. Results

All of the social behaviours were seen in each of the three types of possum dyad, except for the `food share' and `allogroom' behaviours, which were never observed in male±male dyads. All interactions occurred between only two possums at one time. A total of 726 interactions were observed in this study, of which 60% were threats, 21% were ®ghts, 19% were af®liative and <1% were sexual.

The number of threat interactions observed in each group type was affected by both the season and the type of group in which the interaction occurred (p<0.01; Table 1). Threat interactions were most common in the non-breeding season (p<0.001) and occurred most often in all female groups (p<0.05; Table 1). Fight interactions were not signi®cantly more common in one type of group than another, but were signi®cantly more frequent in the non-breeding season (p<0.001; Table 1). In contrast, af®liative interactions did not differ statistically in frequency with season, but were signi®cantly more common in female groups than in mixed-sex groups, and in mixed-sex groups than male groups (p<0.05; Table 1). Only a small number of sexual interactions were observed in the mixed-sex groups and pouch young were found in only four of the eight females housed in mixed-sex groups during the breeding season. No homosexual behaviour was observed during this study. The total number of interactions in each group was also affected by both the season and the group type (p<0.01). Interactions were more frequent in the non-breeding season (p<0.001; Fig. 1) and were more common in all female or mixed-sex groups than in groups of all males (p<0.05; Fig. 2).

Within the groups, some of the mixed-sex dyads interacted more frequently (associated) than was expected by independent interaction patterns during the breeding season (p<0.001), and less frequently than expected (separated) in the non-breeding season (p<0.01). This was mainly due to the occurrence of more af®liative interactions than expected in the breeding season (p<0.001) and fewer than expected threat interactions in the non-breeding season (p<0.05). Single-sex dyads did not appear to `associate' with or `avoid' each other more than expected by random interaction patterns. However, single-sex dyads housed in mixed-sex groups, interacted less frequently than expected

Table 1

Mean number of threat, fight and affiliative interactions (during all observation periods per season) in all female, mixed-sex or all male groups during the non-breeding and breeding seasonsa

Group type Season Interaction type

Threat Fight Affiliate All female Non-breeding 128.0 39.2 18.1

Breeding 18.9 4.9 27.5

Mixed-sex Non-breeding 54.5 20.6 4.9

Breeding 27.0 10.5 6.0

All male Non-breeding 10.0 5.9 1.0

Breeding 5.4 6.2 0

Effects Season <0.001 <0.001 N.S. S.E.D.b _{0.65 0.46 1.35}

Group <0.05 N.S. <0.05 S.E.D.b _{0.24 0.32 0.29} a_{Significant season and group type effects were tested using the Wald test for fixed effects.}

b_{S.E.D.ˆAverage standard error of difference between seasons or groups.}

in the breeding season (p<0.001), because the possums were involved in more mixed-sex dyad `associations'.

4. Discussion

This study has shown that possums housed in different types of groups have distinctive social interaction patterns, which are in¯uenced by the sex of the possums involved and the season in which they interact. Interactions involved only two animals at one time. Winter (1976) also observed that only two possums interacted at once in wild populations, and suggested that groups of possums rarely act as a cohesive social unit. Threats (60% of interactions) and ®ghts (21% of interactions) were most frequent in this study. Hickling and Sun (2000) found that aggressive encounters were more common than other types of interactions in wild possums, with 36% of interactions resulting in physical contact.

Fig. 2. Adjusted mean number of interactionsSEM observed in female (Nˆ2), mixed sex (Nˆ4) and male (Nˆ2) groups. Significant group type differences were tested using the Wald test for fixed effects; (*) indicates

p<0.05.

Table 2

Number and percentage of possum dyads that never interacted during the breeding and non-breeding seasons Season Dyad type Number

of dyads

Number not interacting

Percent not interacting (%) Breeding Female±female 16 2 13

Male±female 16 3 19

Male±male 16 6 38

Non-breeding Female±female 8 0 0

Male±female 8 0 0

The total number of interactions between possums in this study differed in the three group types. Previous studies have suggested that interactions between females are very rare (Winter, 1976; Hickling and Sun, 2000), but our data suggest that in the non-breeding season, interactions were most frequent in groups containing all females and least frequent in all male groups. Males tend to temporally and spatially separate to a greater degree than females, with less overlap of home ranges and greater dispersal (Green, 1984; Efford, 1991).

Interactions occurred less frequently in the breeding season than in the non-breeding season. This decrease in frequency may be an artefact of how we quanti®ed interactions: a greater proportion of af®liative interactions (generally of long duration) and fewer threat and ®ght interactions (shorter duration) were observed in the breeding season. Thus, although interaction frequency differed, it is unlikely that the total time spent interacting decreased in any of the groups during the breeding season. Further studies investigating the duration of interactions would be required to clarify this. Studies on wild possum populations suggest that interactions are restricted almost exclusively to the breeding season (Jolly, 1976; Winter, 1976). Therefore, it is likely that the number of threat and ®ght interactions observed in the non-breeding season during this study was arti®cially high, because possums could not always avoid each other by temporal or spatial separation, in the con®ned area available.

The difference in interaction frequency between seasons was greatest in the all female groups. The number of threat and ®ght interactions between females decreased and the number of af®liative interactions increased during the breeding season. Previous studies have suggested that female±female interactions are usually the most aggressive in nature (Biggins and Overstreet, 1978; Hickling and Sun, 2000), which may have accounted for the large number of threats and ®ghts observed in the non-breeding season. Jolly (1981) suggested that female possums become more tolerant of other animals (especially males) during the breeding season. As females are usually dominant to males (Winter, 1976), this tolerance may have also accounted for the reduction in threat and ®ght interactions in the mixed-sex groups during the breeding season.

Some possums in this study always avoided interacting with other possums, with male± male dyads most likely to avoid interacting, especially during the breeding season. Mutual avoidance between possums has been described previously (Winter, 1976; Biggins and Overstreet, 1978), and often occurs as a result of temporal separation between individuals (Jolly, 1976). In a study of social behaviour at bait stations (a valuable food resource), an average of 7.8 possums visited each bait station per night, but each visitor only interacted an average of 1.4 times (Hickling and Sun, 2000). Possums appear to `take-turns' when using common resources (Biggins and Overstreet, 1978; Henderson and Hickling, 1997). Therefore, although the home ranges of wild possums may overlap extensively (Green, 1984), the possums within overlapping areas rarely interact (Winter, 1976).

behaviours that have not been well documented between adult possums were observed in this study: `food sharing' and `allogrooming'. These behaviours were only observed between females or in mixed-sex dyads. However, both of these behaviours have also previously been observed between mothers and their young (Winter, 1976; Day, unpub-lished data). Several of the male±female dyads were associated during the breeding season. Associations between males and females (consort relationships) have been observed in wild possums, and usually occur for a 30±40-day period before mating occurs (Winter, 1976). In this study, three of the female possums that produced offspring were associated with a male before they produced offspring (for between 20 and 50 days), although another female that successfully bred showed no evidence of associative behaviour. Other females also showed associations with males, but did not produce offspring.

Because males and females tended to interact more with each other in the breeding season, those possums had fewer single-sex interactions over the same period. Most interactions between males in wild populations occur in the vicinity of oestrus females (Winter, 1976), but in this study there was no evidence of increased interaction between males during the breeding season. As there were two males and two females in each mixed-sex group, there may have been little competition for mates.

5. Conclusion

The different patterns of interactions observed in each group type and season have implications for the spread of self-disseminating biological control agents. While the actual frequencies of each interaction type in this study cannot be used to suggest how rapidly a biological control agent may spread, the patterns of interaction between groups and seasons are important. It is suggested that the `ideal' biological control system for possums would be based around a sexually transmitted virus that induces permanent sterility without suppressing reproductive cycles (Cowan, 1996). This is because possums' sexual contact rate would remain high as possum density reduced (male possums actively seek females for mating) and multiple matings following sterilisation may actually increase contact rate (Barlow, 1997). However, this study has shown that af®liative interactions are also common during the breeding season, especially in `associated' pairs of female possums. Af®liative interactions involve close physical contact between animals and may provide several routes of transmission (e.g. oral, direct body-to-body contact). Therefore, a biological control system that does not rely only on mating, but does rely on social interactions during the breeding season, may also prove to be effective (Day et al., 1998).

Acknowledgements

`civil twilight' times over the experimental period. Allan Pearson provided helpful comments on an earlier draft of the manuscript.

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