Choice or opportunity: are post-release social groupings influenced by familiarity or reintroduction protocols?
K. E. MOSEBY,D.T.BLUMSTEIN,M.LETNIC and R . W EST
Abstract The conservation benefits of maintaining social Introduction groupings during and after animal translocations are un- clear. Although some studies report improved post-release any conservation reintroductions fail (Wolf et al., survival, others found no discernible influence on reintro- M ; Fischer & Lindenmayer, ; Short, ; duction success. Understanding the effects of social group- Moseby et al., ) and protocols have been developed to ings is difficult because release methods can influence the improve reintroduction success (Batson et al., ) and re- animals’ ability to maintain social groups. We explored duce stress in translocated animals (Teixeira et al., ). this relationship by first studying whether release protocols Recent research suggests that release protocols should be influenced post-release cohesion in the communal burrow- tailored to particular species and sites (Moseby et al., ing bettong Bettongia lesueur, and then investigating ) and that selection of these protocols should be based whether maintenance of social cohesion conferred any on the biological needs of the animals and their response to post-release advantage. We released bettongs into a small the release. Previous studies have focused on factors such as ( ha) and large (, ha) area and compared the propor- size and composition of the release group (McCallum & tion that maintained social groupings in the different Timmers, ), provision of supplementary food or settings. The proportion of bettongs sharing with previous water, delayed vs immediate release (Letty et al., ; ě ů warren co-occupants was higher than expected by chance in Mat j et al., ), and the location of source populations both areas, however, a significantly higher proportion of (Bright & Morris, ; Soorae, ). bettongs maintained social groupings in the small (%) For social species, maintaining social bonds may be compared to the large release area (%). This suggests essential for successful translocation (Shier, ; Batson bettongs prefer to maintain social groupings but are unable et al., ). Social disruption could cause higher stress, to locate members of their group in large release areas. greater post-release dispersal and delayed breeding in Bettongs that did maintain social groupings showed no dif- gregarious species. Conversely, maintaining social or family ference in reproductive or health outcomes compared to groups could increase survival, reduce post-release stress, those that formed new social groupings, suggesting no bene- and promote faster establishment and breeding. Animals fit to reintroduction success. We conclude that release pro- thought to require social groupings for survival, including tocols can influence post-release cohesion, but that greater large predators that hunt in packs, are often held together cohesion does not necessarily confer advantages to group- prior to reintroduction to enable social bonds to form living animals. To test the importance of social cohesion, (e.g. lions Panthera leo: Hayward et al., ; wild dogs further research on reintroductions should compare post- Lycaon pictus: Davies-Mostert et al., ; Gusset et al., release parameters for animals released using protocols ), but the importance of pre-release housing is rarely that do and do not facilitate maintenance of social tested empirically (but see review in Shier, ). groupings. Results from studies that manipulate social groupings during reintroductions are mixed; releasing individuals in Keywords Australia, bettong, Bettongia lesueur, release social groups had little benefit in New Zealand saddlebacks protocols, social networks, translocation Philesturnus carunculatus (Armstrong & Craig, )or Australian tammar wallabies Macropus eugenii (Kemp et al., ). Social organization did not affect dispersal in white-tailed deer Odocoileus virginianus (Jones et al., ). However, studies on black-tailed prairie dogs
K. E. MOSEBY* (Corresponding author), M. LETNIC and R. WEST Centre for Cynomys ludovicianus (Shier, ), brown treecreepers Ecosystem Science, School of Biological, Earth and Environmental Sciences, Climacteris picumnus (Bennett et al., ) and black-eared University of New South Wales, 2035 Sydney, Australia E-mail [email protected] miners Manorina melanotis (Clarke et al., ) suggest that releasing animals in familiar groups helps maintain social D. T. BLUMSTEIN Department of Ecology and Evolutionary Biology, University of California, Los Angeles, USA cohesion and aids establishment and survival after release. *Also at: Arid Recovery Ltd., Roxby Downs, Australia. Similarly, the failure of rock hyrax Procavia capensis reintro- Received September . Revision requested December . ductions in South Africa was thought to be caused by failure Accepted January . to maintain social groupings after release and rock hyraxes
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that were not familiar with each other dispersed further fol- lowing release (Wimberger et al., ). Understanding the benefits of social groupings can be difficult because release methods may influence the ability of animals to maintain social groups. Releasing animals in social groups may not lead to group persistence after release because of post-release panic dispersal, new interactions with other conspecifics at the release site, post-release stress behaviour, or the absence of suitable shelter sites that can support the size of the social group. For example, although saddlebacks were released in social groups in New Zealand, they failed to maintain pair bonds after release, which could have been a direct result of the hard release method used (Armstrong & Craig, ). To examine the benefits of social groups, we need to compare groups of animals that are released using methods that do and do not facilitate the maintenance of social groupings. Thus, to understand the importance of social cohesion, we must consider the influence of release protocols on the main- tenance of social groupings. In this study, we first tested the influence of release protocols on the maintenance of social groupings by releasing the burrowing bettong Bettongia lesueur into large and small release areas and comparing the proportion that maintained social cohesion. We then tested whether maintenance of social groupings conferred any post-release advantage by measuring health and repro- ductive parameters in groups that did and did not maintain social groupings. The burrowing bettong is a social marsu- FIG. 1 Map of the Arid Recovery Reserve showing the source population (Main Exclosure) and the large release site (Red Lake pial, categorized as Near Threatened on the IUCN Red List, Expansion) where bettongs were reintroduced. The small ha which lives in warrens consisting of related females and a release pen is located in the centre of the Main Exclosure. The dominant male (Sander et al., ). Bettongs are reported location of the Reserve in Australia is shown on the inset map. to have a weak dominance hierarchy, with older females oc- cupying the upper ranks and young males the lower (Sander was reintroduced in from Western Australia and the et al., ). Burrowing bettongs are small (c. . kg) macro- population is now estimated at several thousand individuals. podids that feed on seeds, stems and roots of a variety of The Reserve is divided into six paddocks. Rabbits plants (Bice & Moseby, ), and the only macropod to Oryctolagus cuniculus, feral cats Felis catus and red foxes live exclusively in burrows (Short & Turner, ). Under Vulpes vulpes have been removed from four paddocks semi-captive conditions bettongs have been found to use totalling , ha. The remaining two are experimental several warrens but both sexes have one or two preferred paddocks containing rabbits and controlled densities of warrens where they spend –% of their time during cats (i.e. cats are added to or removed from these areas to the day (females % of time in one warren, males %of maintain a certain density; Moseby et al., ), but no time in one warren; Sander et al., ). In the wild, warren foxes. Burrowing bettongs were first reintroduced to the fidelity is usually high; females were found to use a mean of , ha Main Exclosure and now occupy all four feral . warrens over months (Finlayson & Moseby, ). animal-free exclosures. Bettong abundance has increased since release and in we translocated bettongs between the feral animal-free Main Exclosure of the Reserve and the Study area , ha Red Lake Expansion, one of the two experimental paddocks within the Reserve. We conducted experimental releases at the Arid Recovery Reserve near Roxby Downs in northern South Australia (Fig. ). The entire , ha reserve is fenced with a cat, Methods fox and rabbit-proof netting fence and four threatened mammal species have been reintroduced into the Reserve We first tested the influence of release protocols on the since (Moseby et al., ). The burrowing bettong maintenance of social groupings by studying the social
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cohesion of burrowing bettongs released into the large warren (– days, mean days). During this period, fenced , ha Red Lake paddock and a smaller ha release bettongs were also located during the day, and then followed pen. We then determined whether the maintenance of for up to nights to record the distance moved from their social groupings affected body mass, body condition and diurnal warren. This distance was averaged across all bet- reproductive condition in the large release area. tongs tracked at night to estimate the size of a bettong’s neighbourhood; i.e. the linear distance from a resident warren where bettongs would probably be familiar with Influence of release protocol: small release area conspecifics. Twenty-five radio-collared bettongs were then captured and translocated with other individuals in In February bettongs were captured at five warrens October and monitored for up to months after in the Northern Expansion paddock and moved c. km to release. an ha, predator- and rabbit-free release pen in the Main During translocation, individuals were identified as Exclosure paddock (Fig. ). Warrens in the Northern warren co-occupants, neighbours or strangers based on Expansion were km apart and bettongs were released the following criteria: warren co-occupants were individuals after dark at the same location within the ha release pen. captured at the same warren on the night of translocation; The release pen previously housed bettongs, but all bettongs neighbours were individuals captured at warrens within the were trapped and removed from the pen weeks before the neighbourhood distance of their warren; strangers were in- trial. There were six warrens in the release pen at the time of dividuals captured at warrens outside their neighbourhood. bettong removal but bettongs dig their own warrens within a To increase the chance of animals captured at the same war- few days if suitable shelter sites are not available. ren being warren co-occupants rather than bettongs from To determine post-release social groupings, traps were adjacent warrens attracted to trap bait, we checked traps set at each active warren or single entrance burrow (n = ) within h of sunset when bettongs first emerged from within the release pen at and weeks after release. Traps their warrens and trapped multiple warrens in a neighbour- were set immediately in front of warren entrances and hood simultaneously so that animals were likely to enter a checked within hours of sunset, to decrease the chance trap at their own warren. of catching bettongs from other burrows. The number of In March, June and October (– months after ini- bettongs sharing a warren after translocation was compared tial release) warrens identified via radio-tracking of collared to the proportion expected by chance, using a Fishers bettongs within the new translocation area in the Red Lake Exact test. Expansion were trapped using the same methods as during translocation. The number of warren occupants was com- Influence of release protocol: large release area pared with the number of occupants recorded from warrens containing bettongs prior to the move. A total of warrens A total of bettongs were translocated from the Main were trapped over an -month period; warrens in March Exclosure to the Red Lake Expansion over nights in , eight warrens in both March and October , in October . Animals were captured using groups of June and in October . All individuals captured eight Sheffield cage traps set at warrens for – nights. at the same warren were assumed to belong to the same Cage traps were baited with a mixture of peanut butter and social group. rolled oats. Warrens were –, m apart in an area of The proportion of bettongs found sharing warrens after , ha. All bettongs captured at a warren in a night were release was compared with the proportion expected by moved during the same night and multiple warrens were chance, to determine if bettongs exhibited a preference for trapped per night. Bettongs with pouch young . mm maintaining social groupings. The number of burrow long were not moved but released at point of capture. sharers expected by chance was calculated as the average Animals were transported km from the Main Exclosure number of burrow co-occupants after the move, divided to the Red Lake Expansion and released in the dark. All by the total number of bettongs moved, multiplied by the bettongs were released at the same site near the centre of number of original animals recaptured after the move. the Red Lake Expansion (Fig. ). Capture bags were placed The proportion of recaptured individuals sharing in the on the ground and untied, and bettongs were allowed to small release pen was also compared with the proportion move off when ready. sharing in the large release area using a Fishers Exact Test. To examine the social organization of bettongs in the To determine if social organization was broader than the study area, we radio-collared bettongs in the Main individual warren level, we compared the distance between Exclosure prior to translocation ( g VHF core brass all pairs of bettongs before and after translocation using the collars, Sirtrack, Havelock North, New Zealand). Bettongs distances between warrens where individuals were trapped were radio tracked at least once per week for up to before and after release. Individuals sharing a warren were weeks, to record warren use and determine their resident considered to be m apart. We found no more than two
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bettongs sharing a warren after release so we only compared TABLE 1 The number of bettongs captured at warrens containing the distance between all pairs of recaptured bettongs. The radio-collared bettongs before (Main Exclosure) and after (Red distances between pairs of bettongs before and after trans- Lake Expansion) translocation. location were compared using a Mantel test (Smouse Mean sex Total et al., ) which tests for a correlation in the pairwise Before/ Mean no. of ratio warrens distance matrix for before and after translocation. The Date after bettongs ± SE (F:M) ± SE trapped Mantel test was computed in R .. using packages reshape October Before 4.27 ± 0.49 0.42 ± 0.05 30 (Wickham, ) and ade (Dray & Dufour, ). We 2014 also compared the distance between previous warren March After 3.67 ± 0.37 0.35 ± 0.05 19 co-occupants, neighbours and strangers after release using 2015 ± ± a one-way ANOVA. October After 3.44 0.29 0.31 0.05 18 2015
Influence of social groupings on post-release parameters of bettongs that maintained social groupings to %( out All bettongs captured prior to release were given a unique of bettongs). Bettongs were significantly more likely to be ear tag, sexed and weighed, and their reproductive status sharing with a previous warren occupant compared to was evaluated. Body condition was estimated using the chance when escaped co-occupants were (Fisher Exact test formula condition = cube root weight/pes length (Short & statistic = . ,P= . ) and were not included (Fisher Turner, ). These parameters were compared before Exact test statistic = . ,P= . ). and after release for bettongs that did and did not maintain social groupings in the large release area, using two-way Influence of release protocol: large release area ANOVAs. A total of bettongs from warrens were translocated from the Main Exclosure to the Red Lake Expansion over Results nights in October . Translocated radio-collared bet- tongs settled into warrens within weeks of release, and we Social familiarity located warrens in the new release area, using data from radio-collared bettongs and patrolling the area on foot. Of the bettongs radio-collared before release, ( %) These warrens were located throughout the Red Lake used the same warren over the study period, with the Expansion and up to km from the release site. Of the – remaining bettongs using different warrens a mean of bettongs translocated, were recaptured and assigned ± . SE . m apart. The mean number of warrens warren occupancy. Trapping at warrens containing radio- used by all bettongs was . , with females using a mean collared animals revealed a mean of . ± SE . bettongs ± ± of . SE . warrens and males . SE . . There was per warren prior to translocation and . ± SE . and . no significant difference between the number of warrens ± SE . at and months post release, respectively used by male and female bettongs (F = . ,df=, (Table ). There was no significant difference in the number P= . ). A total of night-time fixes were obtained of bettongs per warren (F = .,df=,P=.) or in the from radio-collared bettongs. The mean distance that sex ratio of bettongs per warren (F = .,df=,P=.) bettongs travelled at night from their diurnal warren was before and after translocation. Only warrens known to be ± – SE . m (range . , m). used by radio-collared bettongs were used in the analyses. None of the warrens trapped after release contained Influence of release protocol: small release area the same combination of occupants as prior to release. Only individuals ( pairs: female–female, male– Fifteen bettongs were captured at the five warrens trapped male, male–female) were still found to be sharing burrows during release into the small release area. After release, with a previous co-occupant after release; individuals traps were set at the warrens within the release pen and shared with new co-occupants. Although only a small per- of the bettongs were captured in nine of these warrens centage (%) of bettongs were recaptured at warrens with a (five individuals escaped the release pen by digging under previous warren occupant, the proportion of individuals the foot netting). Of the recaptured animals, (%, that maintained burrow sharing was still significantly higher female–male pairs, and male–male pair) shared warrens than that expected by chance (two-tailed Fisher Exact Test with a previous warren occupant weeks after release. Statistics = .,P=.). The results from the Mantel test Two of the recaptured bettongs did not have a previous suggest that there was no relationship in the distances burrow co-occupant to share with after release because between all bettong pairs before and after translocation. their co-occupants escaped. This increased the proportion Thus, post-release social groups were independent of
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TABLE 2 The distance between pairs of bettongs before and after re- lease for pairs from the same burrow (co-occupants), from warrens within m of each other (neighbours) and from warrens more than m apart (strangers).
Distance before Mean distance after move (m) move (m) ± SE N Co-occupants 0 2,117 ± 123 86 Neighbours 1–316 2,081 ± 90.7 169 Strangers . 316 2,250 ± 22.3 2,905
pre-release social groups (Monte Carlo test observation = .,P=.). The mean distance between pairs of bet- tongs after release was c. km and there was no significant difference in the distance between pairs of warren FIG. 2 Mean post-release distance ± SE between pairs of previous co-occupants, neighbours or strangers (F = .,df=, warren co-occupants for different times between release of the P=., Table ). first and second individual of each pair. Numbers above the bars represent the number of bettong pairs included for each bar. Comparing the small and large release areas, we found that the proportion of bettongs sharing with previous warren co-occupants in the small release pen (% when F = .,df=,P=.) suggested this was consistent including and % when excluding escaped co-occupants) between the two groups. No females had pouch young was significantly higher than in the large release area when released and nearly all females had pouch young (%) (compared to %: Fisher Exact test statistic = ., when trapped after release (Table ). A Fisher Exact test P=.;comparedto%: Fisher Exact test statistic = ., found no significant difference in the proportion of females P=.). with pouch young in females who did and did not maintain When we trapped bettongs for relocation, we were not social groupings (Fisher Exact Test Statistic = ,P. .). always able to trap all bettongs from a warren during the same night; warrens were trapped for up to nights. Discussion Thus, to investigate the potential influence of the time between the first and second individual of a co-occupant The low percentage of bettongs that maintained social pair being moved on the maintenance of social groupings, groupings after release into the large release area was unex- we compared co-occupant pairs that were moved during pected considering they live communally in warrens with the same vs different nights (, , and . nights apart). relatively high warren fidelity (Sander et al., ; Of the warren co-occupants moved during the same or Finlayson & Moseby, ). Bettongs formed new social different nights, there was a significant effect of time be- groupings soon after release, with a similar number of tween release of co-occupant pairs and their distance warren co-occupants to that recorded prior to translocation. apart after release (F = .,df=,P=., Fig. ). A Other studies have also reported a failure to maintain social Tukey post hoc test revealed that bettong pairs moved dur- bonds after release in species such as New Zealand robins ing the same night or night apart were significantly closer (Armstrong, ) and rock hyraxes (Wimberger et al., after release than pairs moved . nights apart (Fig. ). ). Burrowing bettongs use more than one burrow with- in their home range and so it could be argued that social Influence of social groupings on post-release parameters groupings may be more important at the neighbourhood ra- ther than the individual warren level. However, we found Body mass, body condition and reproductive status of that bettongs did not maintain neighbourhood associations bettongs were compared before and months after release after release; there was no significant difference in the between the individuals that maintained warren groupings distance after release of pairs of bettongs from the same vs those that did not. To exclude seasonal differences, only neighbourhoods vs unfamiliar bettong pairs. bettongs recaptured in March were included in this ana- Although the maintenance of social groupings was low, it lysis. There was no significant difference between bettongs was still higher than that expected by chance and even high- that did and did not maintain social groupings (Table ). er in the small release pen, suggesting that bettongs sought Body mass (-way ANOVA F = .,df=,P=.)and to maintain social relationships after release and that the body condition index (F = .,df=,P=.) were size of the release area influenced their ability to maintain significantly lower after release, but the non-significant inter- social groupings. This is in contrast to other species such action terms (mass F = .,df=,P=. and condition as the black-eared miner that appear to have strong group
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TABLE 3 Difference in body and reproductive condition months after release for animals that maintained social groupings vs those that did not.
% with pouch young (n) Mean body condition index ± SE (n) Mean weight (g) ± SE (n) Maintained, before 0 (5) 5.04 ± 0.053 (12) 1,566 ± 17.4 (12) Maintained, after 100 (5) 4.74 ± 0.053 (12) 1,486 ± 17.4 (12) Non-maintained, before 0 (27) 5.06 ± 0.009 (69) 1,580 ± 7.2 (69) Non-maintained, after 93 (27) 4.68 ± 0.009 (69) 1,472 ± 7.2 (69)
bonds, with populations maintaining social cohesion even improved when animals were released in their social group- in soft and hard releases (Clarke et al., ). Our finding ings (Shier, ). We did not compare survival between that bettongs were significantly more likely to maintain so- groups but the time taken to form new social groupings cial groupings after release into a small compared to a large could have increased bettong vulnerability to predators release site suggests that the breakdown of social groupings and may have affected survival if we had released animals in the large release site could have been caused by an inabil- into an area with high predator densities. Taken together, ity of previous warren co-occupants to locate each other the variety of results suggests that the effects of transferring after release. Radio-collared bettongs usually settle into bur- animals in social and non-social groups are species-specific rows within days of release (Moseby et al., ), so in large and possibly related to the importance of social bonds for release areas it is probable that bettongs settled into warrens defence from predators, access to food or reproduction. with individuals that were in close proximity during the first Burrowing bettongs appeared to prefer to maintain social days after release. Our observation that co-occupant pairs groupings after release but readily formed new social group- that were moved within a few days of each other were ings with no apparent detrimental effect on long-term more likely to settle in warrens that were closer together reintroduction success. This suggests that release methods than those released . days apart supports this finding. can influence the ability of animals to maintain social Bettongs disperse up to km after release (Short & groupings but that maintaining social cohesion after release Turner, ; Moseby et al., ), which decreases the does not necessarily lead to fitness advantages. Thus the chance of intercepting warren co-occupants in the first failure of animals to maintain social bonds in some release few days after release, when warren occupancy is formed. programmes could be an artefact of the release protocol Our findings are consistent with the hypothesis that this rather than a result of the individual animals’ preference. hyper-dispersal is facilitated by the opportunity to move To understand the benefits of maintaining social groupings long distances. By contrast, the small release site may have in reintroduction programmes, future translocations should allowed bettongs to locate each other sooner and permitted first seek to examine the requirements for maintaining them to maintain social bonds. social groupings after release and then compare post-release Importantly, social group fidelity seemed to confer no parameters for groups of animals released using protocols fitness advantages; the few individuals that maintained social that do and do not facilitate maintenance of social groupings after release did no better than those that developed groupings. Only under these scenarios will it be possible new social groupings. There were no significant differences in to accurately determine the benefits of maintaining social breeding rates, body condition or body mass of animals that groupings in reintroduction programmes. maintained vs those that formed new social groupings. Thus, our results suggest that bettongs were not negatively Acknowledgements We thank D. Williams, R. Pedler, C. Lynch, P. affected by the breakdown of social groupings during reintro- Carter and Z. Richardson for assistance with fieldwork. Funding was duction and were readily able to form new social groups. obtained from an Australian Research Council Linkage Grant between These results are similar to other studies where social Arid Recovery, University of New South Wales and University of groupings were not maintained and new groupings were California Los Angeles (Australian Research Council Linkage Project LP160100270). Arid Recovery is an independent conservation initia- formed with no impact on post-release fitness correlates. tive supported by BHP Billiton, the University of Adelaide and the Experimental trials with white-tailed deer found that indivi- South Australian Department of Environment. duals translocated in social or unrelated groups did not remain with their release groups but there was no difference Author contributions Conception of the study: KM and RW. in survival probability or dispersal distance from the release Methodology design: RW, KM, DTB and ML. Data collection: RW site in familiar vs unfamiliar groups (Jones et al., ). and KM. Data analysis: RW and KM. Writing: KM and RW. All However, this is not always the case. For example, rock authors interpreted the data, contributed to drafts and gave approval hyrax reintroductions failed because of an inability to main- for publication. tain or form new social groupings following release (Wimberger et al., ) and prairie dog survival was Conflicts of interest None.
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