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Fitness Costs of Neighborhood Disruption in Translocations of a Solitary Mammal DEBRA M. SHIER∗ AND RONALD R. SWAISGOOD Division of Applied Animal Ecology, San Diego Zoo Institute for Conservation Research, 15600 San Pasqual Valley Road, Escondido, CA 92027-7000, U.S.A.

Abstract: Translocation is used to reestablish wild populations of animals, but translocation projects often do not meet their objectives because postrelease mortality of animals is high. One reason for translocation failure is that the behavioral or ecological requirements of released animals are unmet. Maintaining foundergroup social relationships during release can affect reestablishment of social species. Solitary territorial species with stable neighbors (restricted dispersal and lifetime occupation of a home range) of the same species may also benefit from the maintenance of these social relationships during translocation. We translocated Stephens’ kangaroo rats ( Dipodomys stephensi), a solitary species listed as endangered under the U.S. Endangered Species Act, with and without neighboring kangaroo rats. We compared the settlement (establishment of a stable home range) decisions and fitness of kangaroo rats between the 2 treatments. Kangaroo rats translocated with neighbors traveled shorter distances before establishing territories, had higher survival rates, and had significantly higher reproductive success than kangaroo rats translocated without neighbors. Number of offspring was 24-fold higher for kangaroo rats translocated with neighbors than those translocated without neighbors. Differences in behavior following release may partially explain differences in survival between the 2 groups. Immediately following release, animals translocated with neighbors fought less and spent significantly more time foraging and digging burrows than animals translocated without neighbors. Our results indicate that even for solitary species, maintaining relationships among members of a translocated group of animals can influence translocation success. This study is the first empirical demonstration of the fitness consequences of disrupting social relationships among territorial neighbors.

Keywords: familiarity, fitness, founder group, kangaroo rat, settlement, social behavior Costos sobre la Adaptabilidad de la Disrupci´ on Vecinal en Translocaciones de un Mam´ıfero Solitario

Resumen: La translocaci´on es utilizada para restablecer poblaciones silvestres de animales, pero los proyectos de translocaci´ on a menudo no cumplen sus objetivos porque la mortalidad de animales despu´es de la liberaci´ on es alta. Una raz´ on del fracaso de la translocaci´ on es que no se cumplen los requerimientos conductuales o ecol´ ogicos de los animales liberados. El mantenimiento de las relaciones sociales del grupo fundador durante la liberaci´ on puede afectar el restablecimiento de especies sociales. Las especies territoriales solitarias con vecinos estables (dispersi´ on restringida y ocupaci´ on de un rango de hogar de por vida) de la misma especie tambi´en se pueden beneficiar del mantenimiento de esas relaciones sociales durante la translocaci´ on. Translocamos ratas canguro (Dipodomys stephensi), una especie solitaria enlistada como en peligro en el Acta de Especies en Peligro de E.U.A., con y sin ratas canguro vecinas. Comparamos las decisiones de asentamiento (establecimiento de un rango de hogar estable) y la adaptabilidad de ratas canguro entre dos tratamientos. Las ratas canguro translocadas con vecinos viajaron distancias m´ as cortas antes de establecer territorios, tuvieron mayores tasas de supervivencia y tuvieron significativamente mayor ´exito reproductivo que las ratas canguro translocadas sin vecinos. El n´ umero de cr´ıas fue 24 veces m´ as alto en las ratas canguro con vecinos. Las diferencias conductuales despu´es de la liberaci´ on pueden explicar parcialmente las diferencias

∗ email

[email protected] Paper submitted November 11, 2010; revised manuscript accepted June 1, 2011.

116 Conservation Biology, Volume 26, No. 1, 116–123  C 2011 Society for Conservation Biology DOI: 10.1111/j.1523-1739.2011.01748.x

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en la supervivencia entre los 2 grupos. Inmediatamente despu´es de la liberaci´ on, los animales translocados con vecinos pelearon menos y emplearon significativamente menos tiempo forrajeando y escarbando madrigueras que los animales translocados sin vecinos. Nuestros resultados indican que aun con especies solitarias, el mantenimiento de relaciones entre vecinos de un grupo translocado de animales puede influir en el ´exito de la translocaci´ on. Este estudio es la primera demostraci´ on emp´ırica de la consecuencias de la disrupci´ on de las relaciones sociales entre vecinos territoriales sobre la adaptabilidad.

Palabras Clave: adaptabilidad, asentamiento, conducta social, familiaridad, grupo fundador, rata canguro

Introduction Translocation is defined as relocating wild animals from one site to another to create, reestablish, or augment wild populations for the purposes of conservation (IUCN 1998). Over the last 20 years, there has been an exponential increase in the number of translocations in response to habitat fragmentation and loss and decreases in habitat quality (Armstrong & Seddon 2007; Seddon et al. 2007). For a large number of species with low mobility, habitat fragmentation limits dispersal, reduces probability of recolonization, and increases probability of extirpation (Newman & Pilson 1997). In fragmented landscapes, translocation may serve the purpose of natural dispersal (IUCN 1998; Armstrong & Seddon 2007). Translocation spreads the risks of demographic and environmental stochasticity over many populations and can be used to manage the genetics of local populations (genetic rescue) (Tallmon et al. 2004). The use of translocation is expected to increase in response to a rapid environmental change. Assisted migration is an emerging, albeit controversial, strategy to relocate species outside their historical range—generally to higher elevations or latitudes—to mitigate species extirpations due to climate change (McLachlan et al. 2007; Hoegh-Guldberg et al. 2008). Translocation is 1 of 4 strategies used to facilitate the adaptation of components of ecological systems and human society to changes in climate (Mawdsley et al. 2009). Translocations are often conducted without controls or proper experimental designs, and therefore few empirical data exist to evaluate and improve the technique. Many translocations have not succeeded (Griffith et al. 1989; Beck et al. 1994; Wolf et al. 1998). Translocation mortality is highest in the first days to weeks following release, as animals decide where to settle and traverse unfamiliar areas in search of resources. Mortality during this establishment period has long been attributed to the behavioral responses of translocated animals (Kleiman 1989). Translocated animals often travel long distances from release sites, with many postrelease movements exceeding typical dispersal distances (Stamps & Swaisgood 2007). If release-site habitat is of sufficient quality for the target species, fitness of released animals should be highest at the release site. Long-distance postrelease move-

ments increase the cumulative probability of exposure to predators and aggressive, unfamiliar conspecifics (Linklater & Swaisgood 2008) and may divert time and energy from finding or creating shelter, such as burrows (Shier 2006). Thus, larger than mean travel distances to settlement (establishment of a stable home range) after release may reduce survival (Moehrenschlager & Macdonald 2003; Stamps & Swaisgood 2007). For social species, intact social relationships among members of a founder group can facilitate settlement and adjustment to the novel environment (Shier 2004; Pinter-Wollman et al. 2009) and increase survival by reducing dispersal distances and predation on newly released animals (Shier 2006). Few translocations consider the effects of disturbing intraspecific source-site social relationships among solitary, territorial animals. Territorial animals respond less aggressively to neighbors, especially those that defend territories, than to unfamiliar animals, a phenomenon known as the “dear enemy” effect (Ydenberg et al. 1988; Temeles 1994). Neighbor animals that defend territories may compete for different resources than animals that are new to the area (e.g., mates but not food; Temeles 1994). Alternatively, neighbors may compete less with each other than with strangers simply because they are familiar with one another (Ydenberg et al. 1988). Once the relationship between neighbors is established, reduced aggression allows conservation of time and energy and reduces the risk of injuries. Regardless of the mechanism, translocated animals may invest substantial time in establishing stable relationships with neighbors. If translocation disrupts these relationships, released animals may expend time and energy to negotiate relationships with new neighbors that are needed for other functions, such as reproduction. We used the solitary and aggressive Stephens’ kangaroo rat (Dipodmys stephensi) to evaluate the effects of retention of neighbor relationships on translocation success. Stephens’ kangaroo rat is a nocturnal, granivorous, and semifossorial heteromyid rodent that defends territories from intruders and footdrums (strikes its feet on the ground) to advertise its presence (Randall 1984, 1989a, 1989b; D.M.S., unpublished data). Research on other species of kangaroo rats indicates these animals are capable of neighbor recognition and that species vary in their tolerance and probability of mating with neighbors versus strangers (Randall 1989a).

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Stephens’ kangaroo rat is native to open grasslands and sparse coastal sage scrub in Riverside and San Diego counties, California (U.S.A.). Seed predation and soil disturbance by Stephens’ kangaroo rat strongly affect the vertical structure and composition of the plant community (Brown & Heske 1990; Goldinggay et al. 1997). They are prey to diverse taxa, including bobcats (Lynx rufus), coyotes (Canis latrans), rattlesnakes (Crotalus spp.), foxes (Vulpes spp.), weasles (Mustela spp.), and owls (Tytonidae and Strigidae). Since 1970, habitat fragmentation and loss of habitat to agriculture and suburban development have been the most direct causes of the decline of Stephens’ kangaroo rat. In 1971, the California Department of Fish and Game (CDFG) listed Stephens’ kangaroo rat as threatened under the California Endangered Species Act because a substantial amount of habitat throughout its range had been lost. In 1988, the U.S. Fish and Wildlife Service classified Stephens’ kangaroo rat as endangered under the U.S. Endangered Species Act. Translocations of kangaroo rats have been ineffective. Although many translocations have been conducted with several species of kangaroo rats (e.g., Williams et al. 1993; O’Farrell 1994, 1999; Montgomery 1997, 2004; Spencer 2003; Davenport 2007; Germano 2010), there have been no documented cases in which a kangaroo rat translocation has successfully established a viable population that persisted over the long term. A translocation of 599 Stephens’ kangaroo rats in 1992 yielded no surviving animals 11 months following release (O’Farrell 1994). Survival following a translocation of the species in 2002 was estimated at 40% 4 months after release (Spencer 2003), and no individuals from the release group persisted at the release site 1 year after release. Factors that affect the success of kangaroo rat translocations are virtually unknown, but current methods do not take into account the species’ social relationships. Kangaroo rats are trapped and moved without regard to individuals’ associations with neighboring kangaroo rats. We sought to determine whether maintaining neighbor groups may be more effective than translocating animals without regard for the species’ social relationships.

Methods Study Site and Subjects We studied Stephens’ kangaroo rats on and adjacent to the Southwestern Riverside County Multispecies Reserve in southern California (33◦ N, 117◦ W, mean elevation 472 m) in 2008 and 2009. In 2008 we selected a single 3.24-ha site on the reserve within the historical range of Stephens’ kangaroo rat for release of the first group of translocated animals. We selected the site on the basis of soil type (deep well-drained soils of sandy loam texture),

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slope (3 times and either was observed entering the burrow at the trap location or was observed chasing other kangaroo rats away from the burrow (behavioral criteria). We continued trapping until no unmarked kangaroo rats were observed in the study area (mean = 29.4 captures/individual, range 5–62). We mapped territory locations and assigned neighbor relationships to animals with adjacent territories (i.e., no other animals in between). In the 2 weeks preceding the translocation, we retrapped all previously marked animals and newly emergent young. Because Stephens’ kangaroo rat is sedentary, for each of these 64 animals, the first trapping location was within the individual’s territory. Thus, for the remaining 35 animals for which we did not have data on territory that met our behavioral criteria, we used initial capture location to assign and map territory location on our study site and to determine spatial relationships among neighbors. We brought the kangaroo rats to be translocated into a temperature-controlled facility (maintained between 15.5 and 29.4 ◦ C) adjacent to the release site to fit each animal with a VHF radiotransmitter backpack modified for use with kangaroo rats (Holohil BD-2C; Shier 2009). For the backpack harness, we modified a figure-8 design used for small passerine birds (10–200 g) (Rappole & Tipton 1991); the loops of the figure 8 wrap around the animal’s front legs and the transmitter sits across the animal’s back. We monitored each kangaroo rat for 24 hours to ensure that it was able to move and forage normally prior to transfer to acclimation cages at the release site. Translocation We translocated 54 kangaroo rats from 2 source locations into acclimation cages in 4 quadrats (0.32 ha each separated by 60–100 m) during early September of 2008. We assigned animals to 1 of 2 treatment groups: translocated with neighbors (translocated with all members of neighboring groups) and translocated without neighbors. Twenty-six were translocated with neighbors into quadrats A (n = 12, 5 adult males, 4 adult females, 3 juveniles) and D (n = 14, 6 adult males, 4 adult females, 4 juveniles). Twenty-eight kangaroo rats were translocated without neighbors into quadrats B (n = 14, 6 adult males, 4 adult females, 4 juveniles) and C (n = 14, 6 adult males, 4 adult females, 4 juveniles). We replicated this design in early July of 2009 at the other release site with 45 kangaroo rats. Twenty-two were translocated with neighbors into quadrats A (4 adult males, 3 adult females, 3 juveniles) and D (4 adult males, 4 adult females, 4 juveniles), and 23 were translocated without neighbors into quadrats B (4 adult males, 4 adult females, 3 juveniles) and C (4 adult males, 3 adult females,

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5 juveniles). The number of adults, juveniles, males, and females translocated into each quadrat reflected proportions among these classes trapped at the source sites. We matched age distribution and sex ratios between quadrats and released kangaroo rats with and without neighbors on the same night to ensure that release timing did not confound the results. For the animals translocated with neighbors, we replicated relative source-site social and spatial relationships at the release site, placing individuals in acclimation cages mimicking the relative spatial pattern of territories at the source site. During the 1-week acclimation period (methods adapted from Shier [2006]), we fed all animals supplementally with a blend of seeds and lettuce daily. At the end of the acclimation period we removed the aboveground portion of the acclimation cages. We observed the behavior of a random subset of kangaroo rats (n = 74/99; 37 per treatment) during the first 2 nights after release. We conducted 10-minute observations. We randomly selected an individual and sat approximately 5 m from its acclimation cage. We began the observation period when the individual emerged from its acclimation cage. During observations, we quantified the amount of time spent foraging (placing vegetation in mouth with forefeet) and frequency of fight initiation (chase, lunge, and spar or engage in a locked battle). We located the animals once daily (while animals were inactive) via VHF radiotelemetry signals for the first 2 months and once per week during month 3 (mean number of locations per individual 54.5; range 2–64) to determine burrow and home range establishment and to distinguish between dispersal and survival where possible. We counted burrows by walking the release site along the lines of a 10 × 10 m grid and locating burrows within 5 m of the line. We used a Global Positioning System (GPS) receiver (Garmin ETrex; Garmin, Romsey, Hants) with a mean recording error of 6 m and range 1–9 m to document the position of each burrow established on the release site 1 week and 1 month following release to assess how long it took the translocated kangaroo rats to dig burrows during the settlement period. Because animals translocated with and without neighbors were released into individual acclimation cages in different quadrats at a single site each year, we used trapping data and behavioral observations to determine the identity of the animal in each burrow. We retrapped all animals over 2 weeks, 3 months after release, to remove transmitters. Once transmitters were removed, we estimated translocation success by trapping all ear-tagged kangaroo rats that remained at the release site, their offspring, and any recruits at the site 1 week of each month throughout the rest of the year. Kangaroo rats have a short generation time, and following the 2008 translocation we observed a decrease in survival of translocated animals beyond 6 months and a concomitant increase in reproductive success as measured by

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emergence of offspring from burrows. Thus, for 2009, we assessed survival at 1 month with telemetry data and retrapped released animals, their offspring, and recruits for 1 week at 3 and 6 months after release.

and the number of burrows that were established over the 2 study periods. These analyses were conducted in PASW Statistics (version 18 for Windows; SPSS, Chicago, Illinois).

Data Analyses

Results

We used one-way analysis of variance (ANOVA) with a sequential Bonferroni correction (Rice 1989) to examine whether translocation with and without neighbors explained significant variance in settlement variables (days to settlement, straight-line distance to settlement location, and total distance traveled prior to settlement) and multiple logistic regression to quantify the effects of neighbor familiarity on survival. Because half the animals were translocated in neighbor groups, we used regression with a cluster function to account for potential correlations within those groups. We conducted ANOVA and multiple logistic regression in Stata (version 10 for Windows; Stata, College Station, Texas). We analyzed reproductive success (offspring that emerged per female that survived at the release site) with Poisson regression in Stata. We used one-way ANOVA to compare the number of fights initiated and duration of foraging by focal individuals in the 2 treatment groups

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A greater number of kangaroo rats translocated with neighbors settled, survived, and reproduced than animals translocated without neighbors (Fig. 1). Animals translocated with neighbors traveled shorter distances before settling (ANOVA: straight-line distance, F 1,94 = 10.65, p < 0.01, corrected alpha = 0.02; total distance traveled, F 1,94 = 5.56, p = 0.02, corrected alpha = 0.05); settled more quickly after release (days to settlement F 1,91 = 49.88, p ≤ 0.01; corrected alpha = 0.02) (Fig. 1a). Their survival was 3 times greater than animals translocated without neighbors (1 month: Wald χ 2 = 8.40, n = 99, z = 2.01, p = 0.04; 3 months: Wald χ 2 = 18.46, n = 99, z = 3.78, p ≤ 0.01; 6 months: Wald χ 2 = 6.10, n = 99, z = 2.20, p = 0.03; 12 months: Wald χ 2 = 4.89, n = 48, z = 2.11, p = 0.04) (Fig. 1b). More individuals of both sexes in the with-neighbor groups survived than survived in without-neighbor groups, but the treatment effect was

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Figure 1. Mean (SE) results of translocations of Stephens’ kangaroo rats with neighbor kangaroo rats and without neighbors: (a) straight-line distance to settlement (i.e., establishment of a stable home range), total distance traveled to settlement (mean number of meters divided by 5), and total time to settlement; (b) survival at 1, 3, 6, and 12 months in 2008 following release; (c) differences in female and male survival 6 months following release; and (d) mean number of offspring per female for all females that survived 1 year and total number of offspring produced at the release site in the first year following release.

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Discussion Our results indicate that translocating Stephens’ kangaroo rats in intact neighbor groups increases settlement, survival, and reproductive success relative to translocating animals without neighbors. Decreased time to settlement may have reduced energetic expenditure and exposure to predators and allowed animals to establish seed caches. Kangaroo rats that traveled shorter distances prior to settlement had higher survival rates than those that traveled farther. These results are consistent with the results of Moehrenschlager and Macdonald (2003), that show quick settlement increases survival and suggest that reducing the distance of postrelease movements and facilitating settlement may increase the probability of successful translocation. Familiarity is an important component in neighbor recognition, spacing of territories, and mate selection in kangaroo rats (Randall 1993). Stephens’ kangaroo rats are philopatric (young do not disperse far and often settle adjacent to their mothers; Shier 2010), which may promote long-term associations among neighbors (Randall 1993) and increase survival (Jones 1986). Neighbor recognition in some species of kangaroo rats may be a sexually dimorphic behavior (Randall 1989a, 1993). Female, but not male D. merriami, tolerate neighbors better than unknown conspecifics. Surviving females translocated without neighbors may have had fewer pups for many reasons. For example, in the absence of established social relationships with

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substantially greater for females than for males. Only 3 of 20 adult females (15.0%) in the without-neighbor group survived 6 months after release, whereas 10 of 16 adult females (62.5%) translocated with neighbors survived for 6 months (Wald χ 2 = 8.80, n = 99, sex × treatment: z = 2.16, p = 0.03) (Fig. 1c). More than twice as many surviving females reproduced in with-neighbor groups than in without-neighbor groups (Wald χ 2 = 20.83, n = 22, z = 3.32, p < 0.01) (Fig. 1d). For every offspring produced in the without-neighbor treatment, 24 were produced in the with-neighbor treatment. One year after translocation, the newly established population was in its sixth generation. Behavioral differences were apparent immediately after release. Animals translocated with neighbors initiated fewer fights (F 1,74 = 12.98, p < 0.01) (Fig. 2a), spent more time foraging (F 1,74 = 30.49, p < 0.01) (Fig. 2b), and established more burrows (1 week, F 1,99 = 16.06, p < 0.01; 1 month, F 1,99 = 9.78, p < 0.03) (Fig. 2c) than animals translocated without neighbors. For both treatment groups, survival decreased as distance to settlement increased (Wald χ 2 = 27.01, n = 99, z = −3.59, p < 0.01) (Fig. 3).

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Figure 2. Mean (SE) behavioral differences of Stephens’ kangaroo rats translocated with and without neighbors: (a) number of fights initiated, (b) time spent foraging (seconds), and (c) number of burrows established within 1 week and 1 month following release. neighbors, these females may have had difficulty finding or attracting mates. For the 3 species of kangaroo rats for which data are available, mating primarily occurs between close neighbors and appears to be facilitated by neighbor recognition (Randall 1993; Randall et al. 2002). Alternatively, females translocated without familiar neighbors may have experienced greater psychological and physiological stress, leading to reduced immunity to pathogens, poor body condition, and compromised reproduction (Dickens et al. 2010). Behavioral data may help to explain these findings. Kangaroo rats in the 2 treatment groups behaved differently immediately after release. In the first days following release, individuals translocated with neighbors

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CalFire conducted the controlled burn. G. Grether and D. Blumstein provided comments on the manuscript. M. Petelle, L. Baker, and J. Price assisted with the fieldwork. S. Marczak assisted with figure production. G. Grether, E. Fleishman, J. Randall, and one anonymous reviewer significantly improved the manuscript.

Literature Cited Figure 3. Probability of survival as a function of distance traveled to settlement (i.e., establishment of a stable home range) (logistic regression: Wald χ 2 = 27.01, n = 99, z = −3.59, p < 0.01). Shaded region indicates 95% CI. spent more time foraging and initiated fewer fights than animals translocated without neighbors. Allocating more time to foraging and less time to fighting may have allowed kangaroo rats translocated with neighbors to improve in physical condition and spend more time and energy excavating burrows and avoiding predators. Kangaroo rats translocated with neighbors excavated more burrows than rats translocated without neighbors during the first month following release. Our findings indicate that disrupting social relationships in a solitary and aggressive territorial species may reduce the probability of successful translocation. Investigators have long known that territorial animals have evolved mechanisms for social recognition of neighbors (Barash 1974). Although the potential costs of negotiating new social relationships have been discussed with regard to the evolution of territorial relationships (Temeles 1994), ours is the first empirical demonstration of effects on survival, reproduction, and behavior of disrupting social relationships with territorial neighbors. As the number of translocation programs increase in response to climate change and other factors, there is a growing need to improve translocation techniques. Understanding the role of behavior in relocation may be the key to increasing the efficacy of this conservation strategy. Attention to social relationships led to a 24-fold increase in the overall population productivity (number of offspring produced in with-neighbor vs. without-neighbor translocation) and the population continued to thrive 3 years following release. Differences of this magnitude could determine whether a translocated population establishes successfully.

Acknowledgments This work was supported by the San Diego Zoo and the Riverside County Habitat Conservation Agency. C. Moen, T. Ash, and D. Bircheff provided assistance on the ground.

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