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Article

Continuous Video Monitoring of Zoo Cheetahs (Acinonyx jubatus jubatus) Reveals Differential Engagement Patterns for Environmental Enrichment Items Based on Sensory Category

by
Haley N. Beer
1,*,
Dustin T. Yates
1,
Trenton C. Shrader
2 and
Ty B. Schmidt
1
1
Department of Animal Science, University of Nebraska-Lincoln, Lincoln, NE 68583, USA
2
Department of Clinical Sciences, Kansas State University, Manhattan, KS 66506, USA
*
Author to whom correspondence should be addressed.
J. Zool. Bot. Gard. 2024, 5(3), 520-538; https://doi.org/10.3390/jzbg5030035
Submission received: 13 March 2024 / Revised: 15 August 2024 / Accepted: 11 September 2024 / Published: 16 September 2024
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Abstract

:
Strategically enriching the environment of zoo felids to encourage innate behaviors is essential to good welfare. To investigate how engagement differs among sensory-based enrichment, six items representing tactile (firehose log, Jolly Eggs), visual (mirror, movie), and olfactory (cinnamon, cologne) sensory categories were offered to three adult cheetah siblings. Each item was offered four times: twice during daytime hours and twice overnight (≥5 h/occasion). Static video monitoring was used to investigate engagement frequency and duration for each item and to observe grooming behaviors. Cheetahs engaged with visual enrichment more frequently (p < 0.05) and for greater (p < 0.05) periods than other items. Allogrooming occurred most frequently (p < 0.05) when the movie was provisioned at night. Tactile enrichment was only modestly engaged, with fewer but longer engagements (p < 0.05) at nighttime than at daytime. Autogrooming frequency did not vary among enrichment items but was greater (p < 0.05) at night than day. These findings showed that zoo cheetah responses to sensory enrichment items differed based on type and time of day. Visual stimuli were favored, whereas olfactory stimuli were generally ignored. This illustrates the benefit of diverse sensory-specific enrichment strategies. Such dynamic strategies can help overcome the challenge of individual preferences to encourage engagement reflective of the animal’s natural behaviors.

1. Introduction

Ethology was formalized as a scientific discipline in the 20th century, but documented observations of animal behavior have informed animal care for centuries [1,2,3]. Advances in this field benefit animals in captivity by allowing better predictions for how genetics, physiology, and experiential memory influence individual responses to environments. Research of social structures, feeding and mating behaviors, habitat selection, and interactions with specific environmental components improves the understanding of species-specific needs [4]. Likewise, understanding individual animals through observing their behaviors can improve approaches to husbandry, health care, and socialization with humans or other animals [5,6]. Empowered by greater public awareness and support for animal welfare, modern zoos have recently expanded their species preservation efforts to include maximizing animal well-being in human-controlled environments [7,8,9,10]. Institutions can formalize their commitment by accreditation from organizations like the Association of Zoos and Aquariums (AZA) and the World Association of Zoos and Aquariums (WAZA), which requires routine welfare assessments [7,8]. Quality of life for zoo-housed animals is associated with the expression of fundamental patterns of behavior, which indicate how well an individual or group is coping with their environment [9]. Welfare is broadly defined as the animal’s long-term status derived from the sum of its individual experiences. Behavioral patterns indicative of welfare can be described in terms of their valence (the positive or negative nature of the behavior) and arousal (the degree of activation) [5]. Positive valence is associated with rewarding stimuli, whereas negative valence is linked to aversive stimuli [7]. Not surprisingly, high frequencies of positive affective states like rewards or environmental control result in good welfare, while frequent negative states such as pain or fear result in poor welfare [7]. As a classic example, differences in behavioral flexibility among conspecifics influence social interactions and activity expenditures. Promoting opportunities to engage in their species’ documented behaviors can enhance flexibility, thereby improving adaptability to environmental changes such as new enclosure layouts or social group dynamics [11]. Behavioral diversity reflects the range of behaviors an animal exhibits. In most instances, positive welfare is associated with more opportunities to perform naturalistic behaviors [11]. Despite potential differences in genetics and background experiences, environments must nonetheless provide animals the opportunity to regularly perform approximations of species-appropriate activities [9]. Expanding the complexity of captive environments via strategic enrichment is perhaps the most effective technique to accomplish this objective. Environmental enrichment is a widely promoted practice in zoos because when successful, it increases the ranges of valence and arousal, which in turn reduces stereotypy in favor of appropriate positive behaviors [12].
Enrichment design may consider evolutionary relevance and the species’ known behavioral repertoire in order to promote desired behaviors with high efficacy [6,9,13,14]. Furthermore, although multiple naturalistic behaviors may be elicited by a singular approach to enrichment, it is unlikely that any single strategy could elicit all beneficial behaviors in an animal’s repertoire. Rotating enrichment items and approaches based on the broad divisions of sensory, social, occupational, physical, nutritional, temporal, animate, and inanimate enrichment holistically increases behavioral opportunities [15,16,17]. Of course, strategies within these broad categories can be tailored to the capabilities of the individual or species. For instance, an estimated 79% of captive felids exhibit stereotypic pacing due in part to the inability to hunt, and thus, benefit from enrichment that stimulates hunting behaviors [18]. For this reason, nutritional enrichment is particularly popular in big cats because it promotes predatory behaviors [19]. Simulated predation and exploration can be encouraged by presenting dietary rations, carcasses, or bones in intentionally challenging orientations, such as hanging, buried, or hidden within other objects. Food-based enrichment is convenient and effective for carnivores, but like any strategy, it may increase stereotypic anticipatory behaviors if not rotated with other enrichment methods [18]. Sensory enrichment in widely varying forms has been shown to increase natural behaviors across many different species. For instance, harbor seals showed increased activity rates when given manipulatable PVC sculptures, horses exhibited less stereotypic weaving with mirrors in their stables, and zoo-housed lions were more social when exposed to scents from natural prey [20,21]. The context for a response toward enrichment within these broad categories varies among individuals due to developmental differences [6,9,22]. Therefore, documenting an animal’s preferences for specific environmental manipulations and its success promoting species-relevant behaviors is imperative to individualized animal welfare. Many AZA institutions encourage documentation of interaction time and frequency for enrichment items to identify the more successful enrichment and to avoid items that are less effective [23]. Although not uniform among all institutions, assessing enrichment efficacy requires some variation in a rating system (e.g., 5: >5 min (multiple visits), 4: >5 min (single visit), 3: <5 min, 2: investigated briefly, 1: ignored, N: negative/aversive, or U: unknown). A common choice is the six-step framework known as the SPIDER method (Setting Goals, Planning, Implementing, Documenting, Evaluating, and Readjusting) [22,23]. Observational records can have great value, but they do not always provide the complete picture due to the time limitations of keepers and the influence of human presence on behavior [24]. Further, engagement with enrichment after dark has not been comprehensively studied, creating a gap in our understanding of nighttime behaviors in zoo-housed animals.
Cheetahs are a popular zoo species, and their frequent inactivity relative to other large felids creates particular interest in enrichment that is simple but effective in stimulating high-frequency engagement [25]. However, non-food sensory stimuli have been largely under-explored as big cat enrichment strategies in general [26]. One study testing various sensory-based enrichment reported positive behavioral changes in jaguarundi (Herpailurus yagouaroundi) offered olfactory and tactile sensory items [27]. Another study investigating the presentation of dynamic objects to lions (Panthera leo) reported fewer self-directed behaviors and more attentive behaviors [28]. Building on these few sensory enrichment studies in felids, the items selected for each category in the present study also considered cost, availability, convenience, and practicality. Additionally, we aimed to learn more about engagement patterns that are not confounded by logistical restrictions like time of day or human presence. We expected engagement of each enrichment item to vary due to individual preferences and the appeal of the targeted response. Because cheetahs have keen eyesight for locating and tracking prey [18], we hypothesized that the novel visual stimuli selected for this study would evoke the greatest frequency and duration of engagement from the three group-housed cheetah siblings compared to olfactory or tactile stimuli. Based on previous studies [28,29], we further postulated that olfactory stimuli would result in longer durations of engagement compared to tactile stimuli. Conversely, we expected the tactile items to approximate small prey, leading cheetahs to interact with them more frequently than with olfactory stimuli. We also hypothesized that the rate of engagement for each enrichment item would inversely influence autogrooming behaviors, which can indicate stress in felid species [22,28,30]. However, we hypothesized that engagement and allogrooming would be positively correlated, as such positive affiliative behaviors increased during effective enrichment in a previous cheetah study [31]. This pattern is not a definitive measure of well-being, but we expected the cheetahs in our study to exhibit a similar inverse response, where allogrooming would increase and autogrooming would decrease with the most effective enrichment items. Thus, the objective of this study was to utilize continuous video monitoring to evaluate how the frequency and duration of engagement differed among visual, tactile, and olfactory sensory-based enrichment items. We further sought to determine if these items impacted auto-/allogrooming behaviors, and whether any of these effects differed between daytime and nighttime.

2. Materials and Methods

2.1. Animals and Experimental Design

All experimental procedures were authorized and in accordance with ethical guidelines set by Lincoln Children’s Zoo Institutional Animal and Care and Use Committee. This work was performed at Lincoln Children’s Zoo (40.800573° N–96.6795° W), Lincoln, NE, USA, from November 2021 to March 2022. The subjects of this study were three captive-born 4-year-old female cheetah (Acinonyx jubatus jubatus) littermates housed together since birth. These cheetahs were kept as a group in a multicompartmental enclosure consisting of a cement indoor area, a covered cement outdoor area, and an uncovered earthen outdoor area. The indoor area of the enclosure was comprised of two 2.9 × 3 × 3 m rooms separated by a vertical door that was generally closed only for cleaning. The rooms had stone masonry back and side walls and wire mesh front walls. Each was furnished with straw bedding on elevated wooden platforms and with naturalistic wooden tree trunks. Indoor areas were not publicly accessible. Human-controlled doors allowed cheetahs access to the adjacent outdoor holding space (2.9 × 3.3 × 3 m) enclosed by chain-link fence. The cheetahs were given access to this area day and night, as long as ambient RealFeel® (AccuWeather, Ferguson Township, PA, USA) temperatures were above 0 °C. Cheetahs were also given access to a smaller outdoor grassy exhibit (12.2 × 28 m) containing boulders and elevated areas every other day, temperatures permitting. This area was visible to the public. Cheetahs had intermittent, supervised access to the adjacent outdoor holding areas when RealFeel® temperatures were between 0 °C and −9 °C and were kept indoors during colder conditions. Cheetahs were offered ad libitum access to water and were each fed a total of 900 g of meat per day (Premium Canine Diet, Central Nebraska Packing, Inc., North Platte, NE, USA), divided between feedings scheduled for 0900 and 1600. The feeding regimen was consistent with Lincoln Children’s Zoo standard protocols for cheetah care, which are based on AZA recommendations.

2.2. Environmental Enrichment

Six different environmental enrichment items were evaluated in this study. Two items were selected to represent each of the three sensory categories: tactile, visual, and olfactory. Tactile sensory items were the firehose log and Jolly Egg pet toys shown in Figure 1a. The firehose log was a 91 × 15 × 15 cm woven rectangle that was hand-crafted by zoo staff from repurposed heavy-duty firehose. It was moderately rigid, beige in color, and weighed approximately 2 kg. The color, shape, texture, and deadweight loosely resembled a freshly killed small prey animal. The Jolly Eggs (Jolly Pets, Streetsboro, OH, USA) were oblong (i.e., egg-shaped) hollow plastic balls designed to engage predatory instincts. Their large diameter (~30 cm) and erratic movements when batted made them difficult to capture or lift from the ground, which loosely resembled a small prey animal in flight. Jolly Eggs were offered in pairs, with each a different color. Tactile items were initially placed in the center of the indoor room so cheetahs could choose whether to engage. Visual sensory items were the adjacently placed mirror and the tablet showing a movie, which are depicted in Figure 1b. These items were positioned just outside the enclosure for animal safety. The wood-encased repurposed furniture mirror (122 × 152 cm) was placed at ground level and positioned vertically against the enclosure’s wire mesh front wall. The mirror was chosen to mimic moving objects, which attract the focus of cheetahs’ adapted vision. The movie shown on the tablet was the 2011 DisneyNature release African Cats, which was recommended by a partner zoo for its vivid natural imagery. This selection was intended to leverage the cheetahs’ highly concentrated photoreceptors and wide field of view. It was presented on a 12.9-inch iPad Pro (3rd Generation, Cupertino, CA, USA) vertically positioned at ground level 1 m from the wire mesh front wall. The movie was presented without sound. Olfactory sensory items were the cinnamon and cologne sources shown in Figure 1c. Ground cinnamon (McCormick, Baltimore, MD, USA) was dispensed by sprinkling small amounts (<1 g) on the floor surface just inside the front wall, just in front of the bedding structure, and just below the water source. Cinnamon is readily available, inexpensive, and has been reported to increase levels of enrichment-directed behaviors in other felids [25,29]. The Obsession cologne (Calvin Klein, New York, NY, USA) was similarly dispersed in small volumes (<0.1 mL/area). It was chosen based on previous studies that found it promoted exploration behaviors like bunting and rubbing in wild big cats [30]. Each enrichment item was offered four times in total: twice during daytime hours and twice during overnight hours. Items were offered in a randomized order, and there was a minimum interval of 4 weeks between repetitions of the same item. Enrichment items were installed following feeding and daily cleaning of the indoor holding areas. The exact timing of installments varied due to keeper schedules, but daytime installments occurred between 0900 and 1100 and nighttime installments occurred between 1600 and 1800. Enrichment items were removed and replaced at the next scheduled cleaning, and thus were available for a minimum of five hours during each presentation.

2.3. Behavioral Assessment

The frequency and duration of enrichment engagement, autogrooming, and allogrooming events (Table 1) were determined from overhead video footage. Downward-facing cameras (4TB Smart Bullet Cameras, Lorex Security Camera Systems; Linthicum, MD, USA), were installed on the ceilings of the indoor pens, 5.4 m off the floor so that the entirety of the indoor pen was in view. This positioning allowed us to capture behaviors occurring in and around the areas where enrichment items were offered. Specifically, this included the entirety of the enclosure where the enrichment was placed as well as the adjacent indoor enclosure accessible by the cheetahs, but not the outdoor areas. Continuous footage from the time of enrichment installment to its removal was recorded to a secure cloud network for later assessment. Recorded footage for each installment was randomly assigned to be reviewed by individuals of an eight-member observation panel (5 females and 3 males, aged 22 to 48 years of age) comprised of volunteer graduate students and faculty members from the University of Nebraska-Lincoln Department of Animal Science. Before observations were recorded, individuals underwent comprehensive training created by the investigators and zoo personnel. Observers reviewed a tutorial video featuring multiple examples of what should and should not be considered engagement for each enrichment item and on how to identify auto-/allogrooming. They also received detailed written instructions on how to document and log the predetermined behavioral descriptors for enrichment engagement and grooming, as illustrated in Figure 2. Observers used all-occurrence sampling methods to document engagement, autogrooming, and allogrooming behaviors in each assigned video. Using video timestamps, observers recorded the time at which each behavioral event began and ended. This allowed quantification of frequency, mean time, and total time for each behavior of interest. Each observer assessed six installments that were stratified by item and time of day and then randomly assigned. To validate consistency of observations among different observers, the primary investigator reviewed a randomly selected 15% of the behavioral events logged by each observer as well as two randomly selected 5 min periods per installment for which no events were logged. The overall inter-observer consistency was 90.3% ± 2.2% (Mean ± SE). Details of observer consistency are described and reported in Supplementary Table S1.

2.4. Statistical Analysis

Each enrichment item was offered on four separate occasions, which were analyzed as technical replications. Because the same set of group-housed cheetahs were used, replication was treated as the experimental unit. Data were assessed for the fraction of time expressing each behavior per hour observed. Data were analyzed for normalcy by Shapiro–Wilk tests. When found to be parametric, these data were analyzed via ANOVA using the mixed procedure of SAS (SAS Institute, Cary, NC, USA) to determine the effect of the enrichment item, with replicate treated as the random effect. The mean duration of each behavioral event was analyzed by the mixed procedure of SAS for the effects of enrichment, time of day (i.e., daytime vs. nighttime), and their interaction. Time was considered a repeated measure. For nonparametric data, original ANOVA were replaced with ANOVA performed on ranked sums of the data. LS means and standard errors are presented for all tables, and the statistical tests used are indicated in the legend. Rank sums for non-parametric data are included in Supplementary Tables S2 and S3. The frequency of occurrences for each behavior was analyzed by chi-squared tests using the frequency procedure of SAS to assess the effects of the enrichment item and time of day. Fisher’s exact tests were substituted when expected values for any response were less than 5. Means were considered different at p ≤ 0.05 and tend to be different at p ≤ 0.10. The correlation procedure of SAS was used to determine associations between enrichment engagement and grooming behaviors by sensory category (tactile, visual, olfactory) and time of day (daytime, nighttime, overall). Pearson correlation coefficients were calculated between enrichment engagement time and each of autogrooming, allogrooming, and total grooming. These data were found to be normal by Shapiro–Wilk tests. All data are presented as means ± standard error except for behavioral frequencies, which are presented as the total number of occurrences.

3. Results

3.1. Frequency of Behavioral Expression

3.1.1. Enrichment Engagement

Differences (p < 0.05) in the frequency of engagement among enrichment items and between times of day are summarized in Table 2. For the firehose log, daytime interactions were observed 17 total times (1.26/hour), and nighttime interactions were observed 9 total times (0.31/hour). For Jolly Eggs, daytime interactions were observed 24 total times (1.85/hour), and nighttime interactions were observed 16 total times (0.58/hour). For the mirror, daytime interactions were observed 84 total times (10.50/hour), and nighttime interactions were observed 117 total times (4.33/hour). For the movie, daytime interactions were observed 100 total times (16.67/hour) and nighttime interactions were observed 9 total times (0.34/hour). For cinnamon, daytime interactions were observed 14 total times (1.17/hour) and nighttime interactions were observed 29 total times (1.05/hour). For cologne, no daytime interactions were observed, and nighttime interactions were observed 8 total times (0.30/hour).

3.1.2. Autogrooming

Differences (p < 0.05) in the frequency at which cheetahs engaged in autogrooming among enrichment items and between times of day are summarized in Table 3. For firehose logs, daytime autogrooming was observed 35 times (2.59/hour) and nighttime autogrooming 45 times (1.55/hour). For Jolly Eggs, daytime autogrooming was observed 70 times (5.38/hour) and nighttime autogrooming 45 times (1.63/hour). For mirrors, daytime autogrooming was observed 7 times (0.88/hour) and nighttime autogrooming 42 times (1.55/hour). For movies daytime autogrooming was observed 14 times (2.33/hour) and nighttime autogrooming 10 times (0.38/hour). For cinnamon, daytime autogrooming was observed 25 times (2.08/hour) and nighttime autogrooming 13 times (0.47/hour). For cologne, daytime autogrooming was observed 40 times (3.33/hour) and nighttime autogrooming 24 times (0.89/hour).

3.1.3. Allogrooming

Differences (p < 0.05) in the frequency at which cheetahs engaged in allogrooming among enrichment items and between times of day are summarized in Table 4. For firehose logs, daytime engagement was observed 33 times (2.44/hour) and nighttime engagement 21 times (0.72/hour). For Jolly Eggs, daytime engagement was observed 40 times (3.08/hour) and nighttime engagement 30 times (1.09/hour). For mirrors, daytime engagement was observed 11 times (1.38/hour) and nighttime engagement 13 times (0.48/hour). For movies, daytime engagement was observed 5 times (0.83/hour) and nighttime engagement 2 times (0.08/hour). For cinnamon, daytime engagement was observed 37 times (3.08/hour) and nighttime engagement 17 times (0.62/hour). For cologne, daytime engagement was observed 22 times (1.76/hour) and nighttime engagement 16 times (0.59/hour).

3.2. Time Devoted to Behaviors

The fraction of time that cheetahs were observed to be engaging with the offered enrichment item was greater (p < 0.05) for the mirror and movie than for the other enrichment items, as shown in Figure 3. The respective fractions of time for which cheetahs engaged with the firehose log, Jolly Eggs, cinnamon, and cologne did not differ from each other. The fraction of time spent autogrooming did not differ due to the type of enrichment being offered, as shown in Figure 4. However, cheetahs spent a smaller (p < 0.05) fraction of time allogrooming when provided the movie compared to the other enrichment items.

3.3. Duration of Behaviors

An enrichment item × time of day interaction occurred (p < 0.05) for the mean length of time for enrichment engagement events. During daytime periods, enrichment engagements were longer (p < 0.05) in mean duration for the movie and the mirror than for all other items, as shown in Figure 5. The mean duration of engagement was greater (p < 0.05) for the firehose log than the Jolly Eggs and was greater (p < 0.05) for both tactile items than for either olfactory item. In fact, no daytime engagements were observed for cologne. During nighttime periods, enrichment engagements were greater (p < 0.05) in mean duration for the firehose log and movie than for the other items. Nighttime engagements were greater (p < 0.05) in mean duration for the firehose log, Jolly Eggs, cinnamon, and cologne, shorter (p < 0.05) in mean duration for the mirror and did not differ in mean duration for the movie compared to duration of nighttime engagements of the same item. Enrichment engagement events did not differ in mean duration due to the elapsed time from introduction for the firehose log, Jolly Eggs, cinnamon, or cologne. Although mean duration of engagement events differed (p < 0.05) due to elapsed time from introduction for the mirror and movie, there did not appear to be a discernable pattern within these differences.
An enrichment item × time of day interaction was observed (p < 0.05) for allogrooming but not for autogrooming. The mean duration of autogrooming events did not differ based on the enrichment item provided. However, autogrooming events were greater (p < 0.05) in mean duration at night than during the day, as shown in Figure 6. During the daytime, allogrooming events were greatest (p < 0.05) in mean duration for the mirror and cologne and least (p < 0.05) in mean duration for the firehose log, Jolly Eggs, and movie, as shown in Figure 7. During the nighttime, allogrooming events were greater (p < 0.05) in mean duration for the firehose log and movie than for all other items. Compared to daytime, nighttime allogrooming events were greater (p < 0.10) in mean duration for the mirror and cologne but did not differ in duration between daytime and nighttime for any other items. Pearson correlation coefficients are presented in Table 5. Positive correlations were observed between nighttime engagement with visual stimuli and autogrooming (r = 0.94; p = 0.06), allogrooming (r = 0.91, p = 0.09), and overall grooming activities (r = 0.95; p = 0.04). No other significant correlations between enrichment engagement and grooming behaviors were observed.

4. Discussion

In this study, we found that cheetahs exhibited different engagement patterns toward specific sensory categories of environmental enrichment. Most notably, the cats engaged with enrichment items designed for visual stimulation about four-fold more frequently than items designed for tactile or olfactory stimulation. However, engagements with items designed for visual stimulation lasted about twice as long on mean. The type of enrichment provided did not appear to affect autogrooming patterns and only modestly influenced allogrooming behaviors. Additionally, we observed that the patterns for enrichment engagement and grooming behaviors were not uniform between daytime and nighttime periods. Moreover, the nature of these time-of-day differences was enrichment-specific, as engagement and allogrooming events were fewer in number but longer in duration at night for several but not all items. Previous literature on cheetahs and other species shows that varying environmental cues provide broad benefits for animal welfare by encouraging specific behaviors [20,32,33,34]. The observations from the present study indicate that such environmental variability can be accomplished with a robust and dynamic rotation of enclosure-enriching items that span the different sensory categories. They also illustrate the importance of understanding and documenting the benefits and limitations of individual enrichment approaches.
Sensory enrichment items designed for visual engagement, and to a lesser extent, tactile engagement, were effective in promoting engagement from this group of captive cheetahs. Cheetahs are known to be visual hunters [35], and thus their greater interest in the two items from the visual sensory category would seem to align well with this evolutionary trait. In fact, previously reported histological analyses of the brain showed that cheetahs have more robust neuronal development in the visual processing centers of the cerebral cortex than other big cats [35]. It is therefore reasonable that behavioral attention characterized by direct eye contact and intentional proximity was high for items that were chosen specifically to provide visual stimulation. Although engagement was always characterized by attention and focus on the item, the nature of this attention evolved over the timeframes that the mirror was present. When first presented to the cheetahs, we observed an initial aversion that included darting from the area, cautiously returning after several minutes, and maintaining a distance of several meters. This response lasted for 10 to 15 min each time and was noticeably more heightened for two of the cats, although all three kept their distance initially. Subsequently, the cats maintained their frequent transitions between indoor and outdoor areas, but their demeanor was more consistent with patrolling and investigating rather than the fear-induced flight or territorial aggression described in previous studies [36,37,38,39]. Ultimately, valence toward the mirror seemed to shift to curiosity, as the cheetahs appeared on multiple occasions to be peeking behind the mirror, as shown in Figure 8. To our knowledge, there is no evidence that cheetahs recognize themselves in mirrors at first sight. However, studies in domestic cats indicate that responses to mirrors are based on individual personability, regardless of self-recognition [40,41]. Thus, the social tendencies and volatility of individual animals should perhaps be considered to determine if using mirrors is a compatible form of environmental enrichment. Although engagement with the mirror could be qualitatively characterized as the most pronounced, frequency and duration metrics show that engagement with the movie was slightly more profound, particularly during the daytime. It is not clear what impact the specific title (i.e., a documentary depicting native African terrain and animals) chosen might have had, but it seems unlikely that the attention was drawn by recognition of the images as other animals. In fact, the subdued responses to the film make it reasonable to postulate that the engagement was driven largely by curiosity for the novel moving colors. A recent study on lions demonstrated a keen attraction to animated illusory patterns, which were chosen more often and engaged for longer periods than non-animated patterns using the same colors and shapes [28]. Whatever the reason, it was clear that the video presentation provoked frequent and prolonged arousal in the cheetahs. It may be that the high incidence of investigation toward the movie, which was displayed on a standard-sized iPad, is attributable to the innate instinct of cheetahs to react to small moving objects [42]. In the wild, the poor stamina of cheetahs generally limits their hunts to one attempted attack [43], making visual acuity necessary for detecting, stalking, and chasing prey and a critical component of their hunting strategy. Although we did not observe responses to the movie that we would consider consistent with instinctive stalking or attacking, the engagement with the movie was characterized by consistent curiosity. These were similar to their later interactions with the mirror, where they chose to sit in close proximity facing the item despite having access to the entire indoor and outdoor areas.
The unique engagement patterns brought on by the individual items chosen from different sensory categories in this study reflect distinct mental perceptions of environmental cues by the cheetahs. Engagement is the first step in creating dynamic experiences within the enclosure aimed at specific sensations and, in turn, naturalistic behaviors. Most of the items assessed in this study were successful to varying extents at generating the predefined engagement behaviors for that item. For example, tactile items were designed to promote manipulative play that approximated hunting behaviors and prey subjugation. As intended, the manifested engagement included batting and chasing the erratically moving Jolly Eggs and dragging the deadweight firehose log around the enclosure by mouth. The present observations provide strong proof-of-concept evidence for the benefits of dynamic enrichment, which helps to inform follow-up studies with more intricate interpretive assessments of behavioral outcomes. As one example, we observed that engagements with tactile items occurred substantially less often and for shorter durations than engagements with visual items. We speculate that this was due to the greater natural intensity of the tactile engagements relative to the more passive visual engagements, as cheetahs have high proportions of fast-twitch skeletal muscle fibers that provide their famous speed but are also quick to fatigue [44]. Thus, the shorter and less frequent tactile engagements may not have been indicative of less interest, but rather physiological factors not measured in this study. Conversely, engagement behaviors for visual and olfactory stimuli were comparable in nature, and thus we can objectively conclude that the greater frequency and duration of the visual stimuli indicated they were more effective in provoking engagement. In fact, enrichment designed for olfactory stimulation produced surprisingly low apparent interest and engagement from these cheetahs. Previous studies in other big cats reported strong responses to novel scents, including the ground cinnamon and Calvin Klein cologne fragrances used in the present study [29,30,45]. The previously observed behaviors included exploratory sniffing, licking, and rubbing against surfaces and objects near the source of the scent, but these were only minimally expressed by our cheetahs. Both olfactory items used in our study were likely novel, as no records for these cheetahs indicate their previous use as enrichment. Findings from other studies indicated a decreased responsiveness to novel odors over a 5-day testing period due to habituation, but it is unclear if habituation influenced our results, as our study involved much shorter periods of access and longer intervals before the items were reintroduced. [29]. Although the current study did not have the capacity to highlight consistent behavioral patterns among the three cheetahs, it is also possible that the indifference toward either olfactory stimuli was due to individual preferences or confounding scents from the housing area. Likewise, engagement may have been low due to the method by which we administered the scent sources, as a previous study in zoo felids found that fragrance sources prompted the greatest interactivity when presented inside a conspicuous novel object such as a hay ball [29]. Scents in the present study were applied to existing surfaces in multiple discrete areas of the enclosures to encourage exploration. Thus, the cheetahs could not have associated the scents with any specific object, novel or otherwise. Finally, the low engagement could have been related to differences in olfactory sensitivity between cheetahs and other large cats. A study of several zoo-housed big cat species found that tigers and jaguars, which are more reliant on their sense of smell for hunting, were more responsive to olfactory enrichment from cinnamon, chili powder, and cumin than cheetahs [25].
Modest associations were observed between enrichment and grooming observations in this study. Most notably, visual enrichment with the movie not only produced the greatest engagement but also resulted in greater nighttime allogrooming. Routine grooming is important in big cats because it helps maintain their fur, has a role in social bonding, and can indicate stress and welfare status [28,29,31]. This study demonstrates that grooming behaviors may be influenced by the timing and type of environmental enrichment, as cheetahs spent less time allogrooming when presented with the movie during the daytime but performed unexpectedly high allogrooming at night. Nocturnal activities in zoo-housed cheetahs have not been comprehensively explored, but the positive correlation between nighttime grooming events and engagement of visual enrichment, which did not occur during the day, indicates the timing aspect of this relationship. It is intriguing that nighttime activity patterns in captive cheetahs might not reflect those documented in wild cheetahs, which typically only alter their diurnal patterns to hunt when a full moon is present [42,46,47].

5. Potential Study Limitations

The findings of this study provide new insights into enrichment engagement in captive cheetahs. The investigators experienced several potential limiting factors that should be considered with these findings. Performing this study at a public zoological institution offered benefits that helped to offset the limited control over resources, daily operations, and logistical constraints. A methodological limitation common to most studies of zoo animals is the small sample size, which may or may not be representative of other captive cheetah populations. This study was also limited to females and it is possible that male cheetahs engage with enrichment differently, as spatial distributions in the wild indicate a high likelihood for differential preferences between sexes [43]. Additionally, the cheetahs in this study were group-housed littermates, which may have behaved differently than individually housed cheetahs or those with different genetic backgrounds. It is also important to acknowledge that neophobia, or a fearful reaction to novel stimuli or situations, could have influenced the engagement patterns we observed with the enrichment items used in this study [48,49]. Differences in the extent of neophobia that individual animals experience toward novel items could not be assessed here. Likewise, the animals available for this study did not allow age-specific differences to be examined. The absence of a true negative control condition (i.e., no enrichment) is not ideal but is the reality of performing research in an AZA-accredited zoo, where daily enrichment is mandated. Similarly, the research team had limited control over the human presence necessary for daily zoo operations. Staff presence and tasks (e.g., cleaning, food prep) occasionally drew the attention of the cats. However, these events were generally brief and only rarely disrupted tracked behaviors. Moreover, frequent human presence is representative of the typical zoo environment, and suspending essential activities during observation periods would have presumably influenced animal behaviors as well.

6. Future Implications

Animal behaviors, activity budgets, and grooming habits provide insight into their well-being [50,51], but are difficult and costly to monitor in person. This study demonstrates that static video monitoring can be used to assess behaviors in zoos, which eliminates confounding human presence and eases time constraints. The next step is to incorporate Animal–Computer Interaction (ACI) technology for automated monitoring of behavioral patterns in individual animals and groups. This will allow staff to assess welfare of captive animals more objectively and over greater periods of time [50]. Wearable tracking systems that attach GPS, accelerometers, and gyroscopic devices provide valuable information [51,52,53,54,55,56], but they can be restrictive and require direct human–animal contact to use. Detached systems require the development of complex algorithms, but recent advancements in this technology may ease this barrier. Machine learning is an artificial intelligence approach that uses algorithms and statistical models to train computer systems with generalized adaptable instructions [57]. These machine learning systems connect camera-detected events with programmed inferences from patterns in data, which represents an emerging strategy for perpetual non-invasive monitoring of captive animals.

7. Conclusions

Effective environmental enrichment enhances zoo animal welfare. Good enrichment strategies promote opportunities for animals to express a fuller behavioral repertoire relevant to their species by engaging specific items or cues. Enrichment items selected from wide-ranging sensory categories and approaches encourage greater diversity and duration of behaviors that are indicative of a healthy psychological and physiological state. Our study revealed that enrichment items from different sensory categories evoke unique degrees of interest and engagement from zoo cheetahs. This confirms the importance of thoroughly evaluating species-specific enrichment strategies and incorporating wide varieties of sensory inputs. The implications are that by developing dynamic experiences that encourage desired natural behaviors, animals can interact with their environment in ways that are advantageous to welfare. The cheetahs in this study expressed greater interest in visual stimuli as enrichment items, which would seem to align with their evolved sight-based hunting. Conversely, they interacted least with olfactory stimuli, which had previously worked well in other felid species. This further illustrates that enrichment experiences are best when tailored for individual animals or groups, as preferences can be influenced by genetics and background as much as by species or region of origin. Continuous, automated video monitoring is the next step in improving the status of animal-environmental interactions and the resulting behavioral patterns that result from engaging in enrichment.

Supplementary Materials

The following supporting information can be downloaded at: https://www.mdpi.com/article/10.3390/jzbg5030035/s1, Table S1: Estimated accuracy of observed behaviors in zoo cheetahs provided different enrichment items; Table S2: Non-parametric ranked sums analyses for time spent performing behaviors in zoo cheetahs provided different environmental enrichment items; Table S3: Non-parametric ranked sums analyses for average duration of behavioral observations in cheetahs provided different environmental enrichment items.

Author Contributions

Conceptualization, H.N.B. and T.B.S.; methodology H.N.B. and T.C.S.; software, D.T.Y.; validation T.B.S.; formal analysis, H.N.B., T.B.S. and D.T.Y.; investigation, H.N.B., T.C.S. and D.T.Y.; resources, T.C.S. and T.B.S.; data curation, H.N.B., T.C.S. and D.T.Y.; writing—original draft preparation, H.N.B.; writing—review and editing, D.T.Y. and T.B.S.; visualization, H.N.B. and T.B.S.; supervision, T.C.S.; project administration, T.B.S. and D.T.Y.; funding acquisition, T.B.S. and D.T.Y. All authors have read and agreed to the published version of the manuscript.

Funding

This research was funded by discretionary accounts at the University of Nebraska-Lincoln.

Institutional Review Board Statement

This study was reviewed and conducted in accordance with Lincoln Children’s Zoo’s IACUC.

Data Availability Statement

The data presented in this study are available on request from the corresponding author. Public access to the data is restricted because permission to access the private server where the information is stored is limited to individuals affiliated with zoo entities.

Acknowledgments

The authors wish to acknowledge the Lincoln Children’s Zoo for facilitating access to their cheetah collection. We extend a special thanks to zookeepers Emma Hazel, Sarah Johanson, Daniel Dunn, Angela Rohland, and JoHanna Lanphier for accommodating this study with your time and effort. Special acknowledgment is due to Benny Mote for aiding with camera setup and technical inquiries and to the individuals who dedicated countless hours to footage review: Rachel Gibbs, Melanie White, Zena Hicks, Pablo Grijalva, Eileen Marks-Nelson, Brooke Parrish, Storey Forester, and Avery Vieregger. Lastly, we recognize the involvement of Beth Kizer, Jone Beer, Lelanya Yates, and Charlee Schmidt, whose participation in the initial review and observation techniques went far beyond support.

Conflicts of Interest

The authors declare no conflicts of interest.

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Figure 1. Environmental enrichment items offered to group-housed zoo cheetahs. Items were chosen from three sensory category: (a) tactile stimuli: firehose log (top) and Jolly Eggs (bottom); (b) visual stimuli: mirror (top) and movie (bottom); and (c) olfactory stimuli: cinnamon (top) and cologne (bottom).
Figure 1. Environmental enrichment items offered to group-housed zoo cheetahs. Items were chosen from three sensory category: (a) tactile stimuli: firehose log (top) and Jolly Eggs (bottom); (b) visual stimuli: mirror (top) and movie (bottom); and (c) olfactory stimuli: cinnamon (top) and cologne (bottom).
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Figure 2. Enrichment engagement and grooming were documented in group-housed zoo cheetahs provided different enrichment items. The top row shows examples of (A) autogrooming (self-grooming) and (B) allogrooming (grooming of another cheetah). The 2nd row shows examples of engagement with tactile enrichment items: (C) firehose log and (D) Jolly Eggs. The 3rd row shows examples of engagement with visual enrichment items: (E) mirror and (F) movie on a tablet. The bottom row shows examples of engagement with olfactory enrichment items: (G) cinnamon and (H) cologne.
Figure 2. Enrichment engagement and grooming were documented in group-housed zoo cheetahs provided different enrichment items. The top row shows examples of (A) autogrooming (self-grooming) and (B) allogrooming (grooming of another cheetah). The 2nd row shows examples of engagement with tactile enrichment items: (C) firehose log and (D) Jolly Eggs. The 3rd row shows examples of engagement with visual enrichment items: (E) mirror and (F) movie on a tablet. The bottom row shows examples of engagement with olfactory enrichment items: (G) cinnamon and (H) cologne.
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Figure 3. Proportional time that cheetahs spent engaging environmental enrichment items. Data are expressed as the fraction of total time the item was offered. These data were found to be non-normal by Shapiro–Wilk test (W, 0.466; p < 0.01). Therefore, statistical analyses represented on this graph were performed on data ranks. a, b Means with different superscripts differ (p < 0.05). Rank sums are presented in Supplementary Figure S2. Note: Y-axes vary for data visibility.
Figure 3. Proportional time that cheetahs spent engaging environmental enrichment items. Data are expressed as the fraction of total time the item was offered. These data were found to be non-normal by Shapiro–Wilk test (W, 0.466; p < 0.01). Therefore, statistical analyses represented on this graph were performed on data ranks. a, b Means with different superscripts differ (p < 0.05). Rank sums are presented in Supplementary Figure S2. Note: Y-axes vary for data visibility.
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Figure 4. Proportion of time that cheetahs spent grooming. Data are expressed as the fraction of total time the item was offered. These data were found to be normal by Shapiro–Wilk test (W = 0.956; p = 0.35). a, b Means with different superscripts differ (p < 0.05) within each behavior. Note: Y-axes vary for data visibility.
Figure 4. Proportion of time that cheetahs spent grooming. Data are expressed as the fraction of total time the item was offered. These data were found to be normal by Shapiro–Wilk test (W = 0.956; p = 0.35). a, b Means with different superscripts differ (p < 0.05) within each behavior. Note: Y-axes vary for data visibility.
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Figure 5. Mean duration of engagements with different sensory enrichment items during daytime (top) and nighttime (bottom) periods. These data were found to be non-normal by Shapiro–Wilk test (W, 0.533; p < 0.01). Therefore, statistical analyses represented on this graph were performed on data ranks. a, b, c, d Means with different superscripts differ (p < 0.05). Rank sums are presented in Supplementary Figure S3. Note: Y-axes vary for data visibility.
Figure 5. Mean duration of engagements with different sensory enrichment items during daytime (top) and nighttime (bottom) periods. These data were found to be non-normal by Shapiro–Wilk test (W, 0.533; p < 0.01). Therefore, statistical analyses represented on this graph were performed on data ranks. a, b, c, d Means with different superscripts differ (p < 0.05). Rank sums are presented in Supplementary Figure S3. Note: Y-axes vary for data visibility.
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Figure 6. Mean duration of time spent engaging in autogrooming with different sensory enrichment items during daytime and nighttime applications. These data were found to be non-normal by Shapiro–Wilk test (W, 0.598; p < 0.01). Therefore, statistical analyses represented on this graph were performed on data ranks. a, b Means with different superscripts tend to differ (p < 0.10). Rank sums are presented in Supplementary Figure S3. Note: Y-axes vary for data visibility.
Figure 6. Mean duration of time spent engaging in autogrooming with different sensory enrichment items during daytime and nighttime applications. These data were found to be non-normal by Shapiro–Wilk test (W, 0.598; p < 0.01). Therefore, statistical analyses represented on this graph were performed on data ranks. a, b Means with different superscripts tend to differ (p < 0.10). Rank sums are presented in Supplementary Figure S3. Note: Y-axes vary for data visibility.
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Figure 7. Mean duration of allogrooming during the day and at night. These data were found to be non-normal by Shapiro–Wilk test (W, 0.651; p < 0.01). Therefore, statistical analyses represented on this graph were performed on data ranks. a, b, c, d Means with different superscripts differ (p < 0.05). Rank sums are presented in Supplementary Figure S3. Note: Y-axes vary for data visibility.
Figure 7. Mean duration of allogrooming during the day and at night. These data were found to be non-normal by Shapiro–Wilk test (W, 0.651; p < 0.01). Therefore, statistical analyses represented on this graph were performed on data ranks. a, b, c, d Means with different superscripts differ (p < 0.05). Rank sums are presented in Supplementary Figure S3. Note: Y-axes vary for data visibility.
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Figure 8. Evolution of behavioral responses to a mirror used as environmental enrichment in group-housed zoo cheetahs: (top) initial cautious observation marked by guarded movements and hesitant visitation; (bottom) transition to curiosity with investigative behaviors, such as attempts to peek behind the mirror in search of the source of the reflected images.
Figure 8. Evolution of behavioral responses to a mirror used as environmental enrichment in group-housed zoo cheetahs: (top) initial cautious observation marked by guarded movements and hesitant visitation; (bottom) transition to curiosity with investigative behaviors, such as attempts to peek behind the mirror in search of the source of the reflected images.
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Table 1. Categories of behaviors documented during the observation period.
Table 1. Categories of behaviors documented during the observation period.
BehaviorDescription
Enrichment engagementInteracting with the enrichment item via direct contact
(e.g., touching, rolling, sniffing, playing, catching, rubbing, carrying)
AutogroomingLicking, scratching, or nibbling own body
AllogroomingLicking, nibbling, bunting another cat
Table 2. Frequency of engagement by cheetahs among environmental enrichment items during daytime and nighttime periods.
Table 2. Frequency of engagement by cheetahs among environmental enrichment items during daytime and nighttime periods.
ItemDaytimeNighttimeTotal
FirehoseOccurrences17926
Time Observed (min)81017402550
Frequency/h1.260.310.61
Jolly EggOccurrences241640
Time Observed (min)78016502430
Frequency/h1.850.580.99
MirrorOccurrences84117201
Time Observed (min)48016202100
Frequency/h10.504.335.74
MovieOccurrences1009109
Time Observed (min)36015901950
Frequency/h16.670.343.35
CinnamonOccurrences142943
Time Observed (min)72016502370
Frequency/h1.171.051.09
CologneOccurrences088
Time Observed (min)75015902340
Frequency/h00.300.21
Chi-square value, 93.93; degrees of freedom, 5; p-value, <0.001.
Table 3. Frequency of autogrooming in cheetahs among enrichment items offered during daytime and nighttime periods.
Table 3. Frequency of autogrooming in cheetahs among enrichment items offered during daytime and nighttime periods.
ItemDaytimeNighttimeTotal
FirehoseOccurrences354580
Frequency/hour2.591.551.88
Jolly EggOccurrences7045115
Frequency/hour5.381.642.84
MirrorOccurrences74249
Frequency/hour0.881.561.40
MovieOccurrences141024
Frequency/hour2.330.380.74
CinnamonOccurrences251338
Frequency/hour2.080.470.96
CologneOccurrences402464
Frequency/hour3.200.901.64
Chi-square value, 39.79; degrees of freedom, 5; p < 0.001.
Table 4. Frequency of allogrooming among enrichment items offered during daytime and nighttime periods.
Table 4. Frequency of allogrooming among enrichment items offered during daytime and nighttime periods.
ItemDaytimeNighttimeTotal
FirehoseOccurrences332154
Frequency/hour2.440.721.27
Jolly EggOccurrences403070
Frequency/hour3.081.091.73
MirrorOccurrences113344
Frequency/hour1.381.221.26
MovieOccurrences527
Frequency/hour0.830.080.21
CinnamonOccurrences371754
Frequency/hour3.080.621.37
CologneOccurrences222648
Frequency/hour1.760.981.23
Chi-square value, 38.43; degrees of freedom, 5; p-value, <0.001.
Table 5. Correlations between total time engaged with environmental enrichment and time spent grooming in group-housed cheetahs during daytime (0900–1500) and nighttime (1500–0800) hours.
Table 5. Correlations between total time engaged with environmental enrichment and time spent grooming in group-housed cheetahs during daytime (0900–1500) and nighttime (1500–0800) hours.
Enrichment CategoryTime of DayAutogroomingAllogroomingTotal Grooming
TactileDaytime−0.63
0.37		0.49
0.51		0.04
0.95
Nighttime−0.61
0.39		−0.81
0.19		−0.73
0.27
Overall0.57
0.13		0.16
0.69		0.41
0.31
VisualDaytime0.72
0.28		−0.66
0.33		0.39
0.60
Nighttime0.94
0.06		0.91
0.09		0.95
0.04
Overall−0.02
0.97		−0.09
0.83		0.06
0.87
OlfactoryDaytime−0.39
0.61		0.24
0.76		−0.02
0.97
Nighttime−0.58
0.41		−0.39
0.61		−0.48
0.51
Overall−0.19
0.64		−0.02
0.95		−0.09
0.81
Top number, Pearson correlation coefficient (r); bottom number, p-value.
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Beer, H.N.; Yates, D.T.; Shrader, T.C.; Schmidt, T.B. Continuous Video Monitoring of Zoo Cheetahs (Acinonyx jubatus jubatus) Reveals Differential Engagement Patterns for Environmental Enrichment Items Based on Sensory Category. J. Zool. Bot. Gard. 2024, 5, 520-538. https://doi.org/10.3390/jzbg5030035

AMA Style

Beer HN, Yates DT, Shrader TC, Schmidt TB. Continuous Video Monitoring of Zoo Cheetahs (Acinonyx jubatus jubatus) Reveals Differential Engagement Patterns for Environmental Enrichment Items Based on Sensory Category. Journal of Zoological and Botanical Gardens. 2024; 5(3):520-538. https://doi.org/10.3390/jzbg5030035

Chicago/Turabian Style

Beer, Haley N., Dustin T. Yates, Trenton C. Shrader, and Ty B. Schmidt. 2024. "Continuous Video Monitoring of Zoo Cheetahs (Acinonyx jubatus jubatus) Reveals Differential Engagement Patterns for Environmental Enrichment Items Based on Sensory Category" Journal of Zoological and Botanical Gardens 5, no. 3: 520-538. https://doi.org/10.3390/jzbg5030035

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