Designing an assay to evaluate behavioral responses to opposite-sex conspecifics in the endangered black-footed ferret (Mustela nigripes).

The endangered black-footed ferret (ferret; Mustela nigripes) is a North American carnivore that is actively managed to reestablish self-sustaining wild populations. Behavioral abnormalities have been reported in the breeding program and may be a limiting factor for the species' success. Our goal was to design and test an assay that examines the ferret's exploratory response to odor cues in the form of soiled bedding from opposite-sex conspecifics. Across two breeding seasons, males and females were tested using a T-maze that connected their home nest box to two novel nest boxes containing two different conspecific's soiled bedding. For a control, we provided two clean bedding samples. We ran linear mixed models to determine the effect of sex, type of odor cue (soiled, clean), and order of trial (first, second) on time exploring and proportion of that time spent in each behavior. Ferrets spent the majority of time in the novel nest boxes sniffing (44%), standing alert (27%) and scratching (14%). Males explored for longer than females; however, both displayed similar behaviors. Type of cue influenced behavior, with ferrets sniffing more among soiled cues than clean cues. Habituation to the assay was also observed, with less exploration and more standing alert during the second trial of the day. This study is the first step in characterizing the ferret's exploratory response and provides information regarding vital investigatory and vigilance behaviors. The continual development of this assay to further evaluate reproductive and mate choice behaviors will facilitate more successful breeding of the species.

Incorporating Research into an Undergraduate Animal Behavior Course using Zoos and Webcams.

In our nonmajors animal behavior class, we developed a semester-long research project assignment that incorporates project-based learning (PBL) and the opportunity for Course-Based Undergraduate Research Experiences (CUREs) that introduces, assesses, and applies the course concepts. This project can easily be adapted for nonmajors biology, majors biology, or other more general survey classes, including remote courses. This student-led project involves a field trip for data collection at our local zoo, additional data collection using webcams, and writing and presenting a scientific report. Students apply the scientific method to design their research project and formulate a hypothesis. Throughout the semester, students learn about different behavioral sampling methods and how to develop and use an ethogram in class using animal webcams from zoos. At the zoo, students conduct a comparative behavior project by collecting data from their main animal and two related animals using multiple trials, so students can observe differences in behavior. At the conclusion of the project, students write a report demonstrating their data analysis, graphing, explanation, and interpretation of their own scientific data. We discuss how others can design and implement PBL and CUREs in their classes and what we have learned from our experiences.

Using odor cues to elicit a behavioral and hormonal response in zoo-housed African wild dogs.

Olfactory enrichment, like odor cues, can positively affect behavior, reproductive success, and stress physiology in zoo-housed species. Our goal was to determine if odor cues were enriching to the African wild dog (AWD; Lycaon pictus), a species with a complex social structure and a highly developed sense of smell. Our objectives were to: (1) examine changes in activity levels and stress hormone physiology in response to fecal odor cues from natural competitor and natural/unnatural prey species; and (2) determine whether these odor cues could function as effective enrichment for zoo-housed AWDs. Over a 6-month period, fecal samples were collected from two males (AWD 1: dominant, AWD 2: subordinate), fecal glucocorticoid metabolites (FGMs) were validated using an ACTH-challenge, and hormones were analyzed for FGMs by enzyme immunoassay. Behavioral observations were conducted using scan-sampling, and contact and proximity were recorded. AWDs were presented with three fecal odor cues: LION (competitor), CATTLE (unnatural prey), and GAZELLE (natural prey). Only the GAZELLE cue elicited an increase in activity (10.6%) in both individuals and increased positive social behaviors with higher frequencies of affiliative, submissive, and dominant behavior. AWD 1 demonstrated lower (P < 0.05) FGMs than AWD 2 both before and after all odor cues, and FGMs decreased (P = 0.08) in AWD 2 after all cues. We conclude that exposure to natural prey odor cues may be used as effective enrichment for AWDs, and that changes in stress hormone physiology in response to odor cues may be dependent on social rank in this species.

Hormonal and behavioral patterns of reproduction in female hylobatids.

Ovarian cyclicity, reproductive behavior, and gestation length were characterized in female hylobatids using non-invasive fecal steroid analyses and behavioral data. Progestagen metabolites were quantified in fecal samples collected for 3 months from seven females housed at seven North American zoological institutions. Mean (±SEM) ovarian cycle length was 23.1±1.5 days (seven females; 22 cycles) and was similar across individuals and species (range: 15.3-27.3 days). Gestation length in white-cheeked gibbons was 191±7.0 days (n=2), and female-initiated reproductive behavior occurred throughout the ovarian cycle for each individual. This was the first study of its kind to use fecal hormone metabolite analysis in combination with behavioral observations to characterize female reproductive traits for various hylobatid species. These results contribute to our general knowledge of the basic biology of hylobatids, highlight the importance of evaluating both hormonal and behavioral information, and assist the management and breeding of zoo-housed populations of these endangered primates to support overall conservation efforts.

Hormonal correlates of paternal care differences in the Hylobatidae.

Only one of the 15 species of monogamous hylobatids, the siamang (Symphalangus syndactylus), demonstrates direct paternal care in the form of infant-carrying, providing a unique model for examining hormonal correlates of paternal care differences between siamangs and gibbons. We used behavioral data and fecal hormone analysis to investigate (1) differences in monthly percent father-infant proximity in relation to monthly fecal androgen metabolite concentrations from infant birth to the late postpartum period between siamangs and gibbons, (2) the pattern of change in fecal androgen and fecal estrogen metabolite concentrations during the 8-week peripartum period between siamangs and gibbons, and (3) the change in mean fecal glucocorticoid metabolite concentrations at 1-month postpartum from individual baseline between siamangs and gibbons. Father-infant proximity increased as androgen concentrations decreased over the postpartum period in siamangs but not in gibbons. Androgen concentrations increased around birth in siamangs during the 8-week peripartum period, but exhibited a decreasing trend around birth in gibbons. Estrogen concentrations increased from pre- to postpartum in siamangs during the 8-week peripartum period, but exhibited a decreasing trend from pre- to postpartum in gibbons. The difference in mean glucocorticoid metabolite concentrations from baseline was greater in siamangs than gibbons. Our data suggest a relationship between specific steroid hormone patterns and differences in paternal care among the hylobatids, warranting further investigation of such proximate mechanisms.