Male Golden Hamsters (Mesocricetus Auratus) Are More Reactive Than Females to a Visual Predator Cue

J Ethol (2009) 27:137–141 DOI 10.1007/s10164-008-0099-7

ARTICLE

Male golden hamsters (Mesocricetus auratus) are more reactive than females to a visual predator cue

M. Elsbeth McPhee Æ Amanda E. Ribbeck Æ Robert E. Johnston

Received: 22 January 2008 / Accepted: 1 May 2008 / Published online: 11 June 2008 Ó Japan Ethological Society and Springer 2008

Abstract In most species of small mammals, males are (Lima and Bednekoff 1999; Lima and Dill 1990). Time exposed to higher levels of risk than females because they spent obtaining resources is often time less vigilant, and compete for mates, travel greater distances to find and searching for resources may draw animals into high-risk procure mates, and/or defend a territory. This suggests that situations. A large body of literature convincingly shows males and females might have different responses to risky that prey species balance these conflicting goals by shifting situations, such as the presence of a predator. We tested their behavior in response to cues from predators or the responses to a visual predator cue (an owl silhouette) in presence of a predator. For example, when predation risk male and female golden hamsters (Mesocricetus auratus). was high, teal (Ana crecca) did not submerge the entire In a laboratory arena, there was no significant sex differ- front end of their body under water while foraging but ence in the latency to enter the burrow or time spent in the foraged with only their beak submerged and their eyes burrow immediately after exposure to the owl silhouette. above water level (Guillemain et al. 2007). Lizards (Lam- Males, however, were less likely to be active during the 3- propholis guichenoti, Downes 2002) and frogs (Rana sp., min period following the animal’s exposure to the silhou- Anholt et al. 2000) decreased their level of activity in ette, indicating that male golden hamsters are more wary response to the presence of predators (yellow-faced whip after exposure to an aerial predator cue than females. Most snakes Demansia psammophis, and green darners Anax studies of responses to predators or predator cues have not junius, respectively), and anolis lizards (Anolis sagrei) considered sex differences, but our results show that males shifted patterns of habitat use in response to an experi- and females may have quite different responses to predator mentally introduced predator, the curly tailed lizard cues. Further work should be done to characterize and (Leiocephalus carinatus; Losos et al. 2004). quantify sex differences in response to predators or pred- To minimize predation risk, small mammals often ator cues. choose ‘safer’ over ‘riskier’ habitats for foraging (i.e., more versus less cover; Lima and Dill 1990). A common mea- Keywords Golden hamster Á Predator response Á sure of perceived risk during foraging is the ‘giving-up Mesocricetus auratus Á Sex differences Á Visual predator density’ (GUD). Giving-up density refers to the density of a resource left in a patch when the forager quits gathering food at that location, suggesting that the potential for fur- Introduction ther gain is not worth the risk. In other words, if a forager leaves a large quantity of forage behind (i.e., a high GUD), Animals constantly balance the need to avoid predators this behavior suggests a high perceived risk. For example, with the need to obtain resources, such as food and mates common voles (Microtus arvalis) had higher GUDs in mowed (riskier) plots than in unmowed plots (Jacob and Brown 2000). Similarly, free-living fox squirrels (Sciurus & M. E. McPhee ( ) Á A. E. Ribbeck Á R. E. Johnston niger) had higher GUDs in open habitats than in dense ones Psychology Department, Cornell University, Ithaca, NY 14853, USA (Brown et al. 1992). Although house mice (Mus domesti- e-mail: [email protected] cus) and oldfield mice (Peromyscus polionotus) did not 123 138 J Ethol (2009) 27:137–141 overtly react to the introduction of predator cues, they had the actual predation of hamsters in their natural habitat, but lower GUDs in vegetated, less exposed areas (Orrock and our field work indicates that likely predators include fox Danielson 2005; Orrock et al. 2004; Powell and Banks (Vulpe vulpe), various snakes, European white stork 2004). In an experimental set-up that assessed the extent of (Ciconia ciconia), and several species of raptors and owls foraging behavior from feeding stations, Anderson (1986) (Gattermann et al. 2001; Johnston et al., unpublished observed that deer mice (P. maniculatus) and voles observations 2005–2007). Hamster bones were recovered (Clethrionomys gapperi and Phenacomys intermedius) from owl pellets collected around Elbeyli, Turkey between moved threefold farther into dense cover than into open 2005 and 2007 (Johnston et al., unpublished observations). terrain. A number of studies have demonstrated significant changes in the behavior of small mammals upon exposure Materials and methods to cues from predators. In laboratory experiments, wild- caught male root voles (M. oeconomus) decreased their Subjects general activity and showed decreased breeding behavior (i.e., decreases in approaches to females and number of We used 12 male and 12 female captive-bred golden copulations, and an increased avoidance of solicitous hamsters that were between 3 and 5 months old. All ani- females) when exposed to the urine and feces of the steppe mals were unrelated; our colony is bred to maximize polecat (Mustela eversmanni; Bian et al. 2005). Predator diversity, and we regularly include animals from the odors also caused increased vigilance and wariness in both Charles River Laboratory for such a purpose. The animals laboratory-reared European rabbits (Oryctolagus cunicu- were kept in colony rooms on a 14:10-h (light:dark) cycle, lus) tested in outdoor enclosures (Monclus et al. 2005) and with the dark phase beginning at 0900 hours. Animals were wild-caught bank voles (C. glareolus) tested in laboratory housed singly in polycarbonate cages (30.5 9 35.5 9 16 arenas (Jedrzewski et al. 1993). Studies in the wild and in cm) with wire lids and hardwood sani-chip bedding. Food outdoor enclosures with small mammals, such as gerbils, (ProLab 1000; Agway, Ithaca, NY) and water were pro- mice, and kangaroo rats, have also documented reduced vided ad libitum. activity, shifts to more dense habitats, and reduced exploitation of habitat patches by animals exposed to live Apparatus owls (Gerbillus allenbyi, G. Pyramidum: Abramsky et al. 1996; Perognathus amplus, P. baileyi, Dipodomys merri- For this experiment, subjects were transferred into a larger ami: Brown et al. 1988; Kotler et al. 1991, 1992). Plexiglas arena divided into three 30.5 9 93-cm compart- These and many more studies clearly document behav- ments by clear Plexiglas walls. To simulate a natural ioral changes in response to predator cues. In only a few of burrow/nest-chamber, each compartment had a hole in the these studies, however, have sex differences been studied. floor that gave the animals access to their home cage below In many species, males and females are faced with dif- the arena. The floor of each compartment was covered with ferent selective pressures—males travel greater distances sani-chip bedding. A time-lapse video camera was placed than females in search of mates and often spend more time directly above the arena. and energy in defending a territory or in intraspecific The arena was in a separate room that was on the same competition. In contrast, females usually have smaller light cycle as the colony room. During the dark phase, the home ranges but need to meet the energetic demands of testing room was illuminated with one 25-watt red light pregnancy, birth, and lactation (Andersson 1994; Ecuyer- that was mounted on a side wall about 1.5 m off the ground Dab and Robert 2004). These differences could lead to to prevent the owl silhouette from casting a shadow. The contrasting strategies for avoiding predators. We thus room was kept at temperatures ranging between 21 and propose that because males are exposed to greater risk, 25°C. their response to cues indicating the presence of predators should be greater than that of females. Procedure To test this hypothesis, we measured the responses of male and female golden hamsters (Mesocricetus auratus)to Testing took place over 3 days. At 1200 hours on day 1, the a simulated aerial predator, an owl silhouette gliding over subjects were randomly assigned to compartments and the test arena. Golden hamsters are a classic system for placed in the testing environment. We gave the animals 3 h behavioral studies. They are sexually monomorphic, soli- to habituate to their new setting. All animals began tary, and semi-fossorial animals that naturally occur in exploring the compartment above their home cage within agricultural fields in northern Syria and southern Turkey 10 min. The test session began at 1500 hours when we put (Fritzsche et al. 2006). To date, no studies have documented a food pellet at the end of the compartment furthest away 123 J Ethol (2009) 27:137–141 139 from their burrow entrance to motivate the animals to come 18 sample points or observations per 3-min period. We out of their home cages. At that point we began recording measured (1) the number of observations per trial that an with the video camera; the camera recorded all three ani- individual was in the burrow, (2) number of observations mals simultaneously. per trial that an individual was active versus stationary, and A trial began when at least two of the three animals were (3) latency to enter the burrow, measured as number of out of their burrow and in the compartment, at which point seconds before the animal entered its burrow after release the owl silhouette was flown over the entire testing arena. of the silhouette. If one of the subjects was not out of its burrow for the presentation, we retrieved the owl silhouette after 10–15 Data and statistical analysis min and waited until the third animal was out of its burrow. This procedure was repeated until each individual had been All analyses were conducted in R (R Development Core exposed to the owl silhouette. In most cases all three ani- Team 2006). For both males and females, responses to the mals were out for the first presentation. There were a few owl silhouette for the three behavioral measures did not trials, however, where the silhouette was flown a second change over trials. Thus, for each animal we pooled the time, and the original animals were still out of the burrow, data across the three trials and calculated a mean value for resulting in two presentations for these individuals. No data each individual. Because of the small sample size, male/ were collected on the second exposure: because responses female comparisons were made with the nonparametric did not attenuate over time (see below), we do not believe Wilcoxon test. These tests compared males and females on this affected the results. three measures: latency to enter the burrow after exposure Further trials using the methods described above were to the silhouette, number of observations in the burrow, and performed at 0900 hours on days 2 and 3, resulting in at number of observations active in the test chamber. Five least three exposures per animal. The animals were females and two males did not enter the burrow within 3 returned to the colony room after the final test. The testing min of the owl presentation so they were excluded from the arena was washed with a 1:10 Nolvsan/water solution and latency analysis. All hypothesis tests used a = 0.05 as the wiped with 50% ethanol to remove any scents left by the criterion for statistical significance. subjects. At 1200 hours, three new individuals were placed into the compartments for the next round of testing. The stimulus, designed to mimic a gliding owl, was Results traced from a great gray owl (Strix nebulosa) specimen at The Field Museum of Natural History in Chicago, Illinois. There was no significant difference between males and The tracing was reduced 50% and used to create a silhouette females in latency to enter the burrow (Fig. 1a; W = 97, cut out of black matteboard approximately 53 9 30 cm. p = 0.16) or number of observations in the burrow (Fig. 1c; This cutout was mounted behind a curtain at a height of 2 m W = 54.5, p = 0.326) after presentation of the stimulus. above the floor of the test chamber. It was suspended from a Males and females did differ, however, in the number of wire that ran above and across the arena, dropping to a observations they were active in the test chamber (Fig. 1b; height of 1.5 m on the other side. At the beginning of a test, W = 234, p = 0.008). Males were, on average, significantly the silhouette was released by the researcher and it ran along less likely to be active in the compartment (mean obser- the wire over the arena. The silhouette was weighted so that vations active = 7) than females (mean observations it moved along the wire without stalling and crossed the active = 11) after exposure to the owl silhouette. 3.5 m space in about 5 s; as it ‘flew’, it made a slight ‘zip’ To determine whether this difference was a reflection of sound. The silhouette was removed and carried back to the a fundamental sex difference in activity regardless of start 10–15 min after the flight. Thus, the animals only saw context or a difference in response to the predator, we the silhouette in a forward motion. Very little information is compared activity levels in a control group of animals that currently available on hamster vision and acuity under red had not been exposed to the silhouette. In this case, males light, but we assume they were able to see the stimulus and females exhibited similar levels of activity (W = 19.5, because some individuals moved their head and apparently p = 0.464). tracked visually the silhouette as it flew overhead. Data were collected from the videotapes for a 3-min period beginning with the instant the silhouette was Discussion released. Observations were made every 10 s within the 3-min period. At the start of each 10-s interval, the We tested the prediction that males would be more observer noted the animal’s location and behavior responsive than females to predator cues. Our results sup- (instantaneous sampling; Altmann 1974), making a total of port this prediction—males were less likely to be active 123 140 J Ethol (2009) 27:137–141

(Fig. 1b) after exposure to a predator than were females. There was, however, no significant sex difference in latency to enter the burrow or time spent in the burrow immediately after the owl silhouette was flown. This suggests that while males did not initially get into the burrow more quickly than females, they were more wary and attentive for the 3 min following the presentation. These results are similar to those reported by Perrot- Sinal (1996, 1999), who found that male meadow voles (M. pennsylvanicus) significantly decreased their levels of activity and spent less time in the center of an arena after exposure to fox odor, whereas females did not show similar decreases in activity. The authors suggested that these sex differences exist because males need to travel greater distances and spend more time in high-risk locations than females do and, consequently, males have a higher risk of predation (Perrot-Sinal et al. 1999). Similarly, Jedrzejewski and Jedrzejewska (1990) found that male bank voles (C. glareolus) changed their use of a 150-m2 semi-natural enclosure to a greater extent than females after a weasel (Mustela erminea) had been released into the arena for a discrete amount of time (either 24 or 2 h). Our experimental design did not allow us to determine whether the hamsters were reacting to the sound made by the silhouette as it flew over the arena or to the visual cue of the flying silhouette. In either case, these results indicate that males and females exhibited significantly different reactions to predator cues. These differences may be due to sex differences in the degree of exposure to risk: males usually have larger home ranges and travel greater distances than females, and are thus more exposed to predation, whereas females tend to stay closer to their burrow or nest and are less exposed to risk. More studies that employ quantitative measures of sex differences in responses to predators or predator cues would be valuable. Obtaining quantitative data on the actual difference in predation risk between males and females would also be beneficial. As with any study that uses captive-bred animals, these results must be interpreted with caution. All captive golden hamsters are thought to be descendants of a single brother– sister pair brought into captivity in 1930 (Murphy 1971). We must therefore consider the possibility that the observed patterns might be due to inbreeding and/or founder effects. For example, if by chance the male of the original pair had been more wary than the female, this difference could have been passed through the generations and thus explain the patterns observed in this experiment. Additionally, artificial selection over generations in the captive environment could have Fig. 1 Responses of males (n = 12) and females (n = 12) to the altered the behavioral repertoire of the subjects, thus influ- presentation of an owl silhouette. a Mean latency (in seconds) to enter the burrow (p = 0.16), b mean number of observations per trial in encing their responses to predators (Kleiman et al. 1996; which an animal was active (***p = 0.008), c number of observations McPhee 2003, 2004a, b; Millar and Threadgill 1987). This per trial an animal was in the burrow (p = 0.33). Open circles are the could possibly explain why seven of the 24 animals did not mean and bars represent 95% confidence intervals respond at all to the owl silhouette. Our results show that males 123 J Ethol (2009) 27:137–141 141 are more wary than females when presented with cues that in common voles. Oikos 91:131–138. doi:10.1034/j.1600-0706. simulate a gliding owl. 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