The Impact of Olfactory Stimulation on the Behavior and Hormone Levels of the African Lions at the Detroit Zoo

Jourdan RingenbergCZAW ResidentSession II 2014

The Impact of Olfactory Stimulation on the Behavior and Hormone Levels of the African Lions at the Detroit Zoo

IntroductionAfrican lions (Panthera leo) are found in the open woodlands of Sub-Saharan Africa with a habitat covering a wide range of mixed areas of thick bush, scrub, and grass. An obligatory carnivore, their diet consists of medium to large ungulates (i.e. buffalo, zebra, wildebeest, waterbuck); small rodents and birds; young rhinos, elephants, hippos; and giraffes (McDade 2003). Lions typically are nocturnal hunters, with peak activity levels between 21:30-22:30h and 2:00-4:00h (Wilson et al. 2009). Activity levels also increase in the early morning and late afternoon during the cooler hours of the day. To allow for proper digestion and to avoid the heat of the day, lions spend 20-21 hours resting per day (Estes 1991). Resting periods may be interrupted by brief bouts of activity when engaging in social behaviors or hunting (Wilson et.al. 2009). After stalking their prey to a close range, they make a short dash to catch prey and kill by suffocation, clamping their jaws on the prey’s windpipe or muzzle (McDade 2003). Both male and females work together to catch prey, often alternating who catches prey based on prey size, large and small, respectively. Lions, social animals that live in prides of four to six individuals on average, keep territories anywhere from eight to 200m2 (McDade 2003). During the dry season when water sources are scarce, lions may need to travel further distances to find food, often inducing the need to scavenge.

In captivity, zoos are faced with the challenge of inducing the hunting and scavenging behaviors instinctive to a lion, often failing to satisfy the need to utilize these natural behaviors. One study stated that since a natural environment only requires big cats to spend a portion of their daily life stalking and killing prey, the “single greatest period of intensive activity and energy expenditure is during the hunt for food” (Baker 1997). Wild conspecifics often spend three to four hours a day hunting and scavenging for food where they may be forced to travel long distances and utilize their senses to aid in their search. As animals in captivity no longer have the need to provide their own nourishment, there subsequently is an absence of food-finding behaviors and sensory stimulation. While this provides more “free” time, not filling this time with another stimulating activity or behavior could impact the welfare of the animal. The absence of these species-specific behaviors removes the necessity to use sensory input and also poses the potential to replace this time with inactivity or stereotypic behaviors. Mason stated that behavioral inflexibility may indicate an “inadequate ability to suppress natural activities that a captive environment makes impossible” (Mason 2010). This could be detrimental to captive species welfare, as it has the potential to cause chronic frustration and may induce coping methods such as stereotypic behavior or an increased level of inactivity.

The inability to express species-specific behaviors such as hunting, scavenging, and using sensory cues to locate food could result in a prolonged negative behavioral and physiological response in captive lions. An animal motivated to perform a behavior pattern in a situation, but unable to do so, becomes frustrated (Mason 1991). A repetitive situation that produces chronic frustration may lead to a negative physiological or behavioral response that can be deleterious for the animal (Mason 1991). The presence of prolonged frustration in any animal presents an opportunity to develop a coping strategy. A stereotypy is one behavioral response in which an


animal can cope with prolonged frustration (Mason 1991). The most commonly seen stereotypy in big cats is pacing (Mason 2010, Breton 2014); however, upon initial observation of the lions at the Detroit Zoo, pacing seldom is seen. The lack of pacing in the lions suggests that the inability to perform natural behaviors either does not cause a negative behavioral response or that the lions are substituting that time with a different behavior. Initial observations of these lions indicate a high level of inactivity; suggesting that inactivity, or a lack of behavior, may be their form of substitution. However, it is important to note that since the peak activity levels of their wild conspecifics occur in the late night and early morning hours, it is possible that the lions at the Detroit Zoo are active during times when we are not observing them.

Both stereotypic behavior and inactivity are potential ways for an animal to substitute for species-specific behaviors they may be less able to perform. However, while stereotypies allow the animal to perform some type of behavior, inactivity is a lack of behavior. Therefore, inactivity may not be as effective of a substitute as a stereotypic behavior. Researchers have found that in some species, animals that display stereotypic patterns have lower glucocorticoid levels than animals who do not display these patterns (Kuhar 2008, Duncan 1970, Barehem 1972, Wiepkema 1984, 1987, Cronin 1985, Kennes et al. 1988, Cabib et al. 1985, Sheperdson 2004). Duncan (1970) found that stereotypic pacing in domestic fowl correlated with a decrease in corticosteroid levels, and adrenal weight showed to be negatively correlated with head-flicking in this species (Barehem 1972). A study by Shepherdson and colleagues (2004) found that polar bears performing stereotypic behaviors had lower peak cortisol levels and greater cortisol level variation than polar bears that did not perform stereotypies. Wiepkema (1984, 1987) determined that older sows that perform stereotypies have no hormonal response, and veal calves showed a significant negative relationship between the severity of abomasal lesions and stereotypic tongue-playing. Conversely, in some species, the absence of stereotypic behaviors correlates with increased stress hormone levels. Young, tethered sows that perform no stereotypic behavior, versus their older conspecifics, have a chronic rise in corticosteroids (Cronin 1985). A study with voles looked at the effects that lowering cage ceilings had on their stereotypic jumping behavior. The lower ceilings removed the ability to perform this behavior and corticosteroid levels subsequently increased (Kennes et al. 1988) Responding to these changes, some voles developed a new type of stereotypy, which returned corticosteroid to normal levels (Kennes et al. 1988). Similarly, a study on mice by Cabib et al. (1985) found that stereotypies “induced by stimulant drugs” are depressed by the introduction of stressors, indicating a lack of behavior when exposed to a source of stress. While stereotypies often are construed as negative reactions to an environment, these studies suggest that for some individuals, stereotypic behaviors do provide some relief to prolonged frustration versus no behavior at all (inactivity).

While inactivity is a perceived problem in captive felids, there also is often a lack of stimuli necessary to challenge a lion to employ all senses, and according to Powell (1995) “enrichment should take advantage of as many senses as possible”. As hunters and scavengers, lions are innately predisposed to utilize their senses to search for viable food options. As primarily nocturnal hunters, a lion’s primary sense is an acute color vision that reacts quickly to darkness (McDade 2003). However, while being highly equipped visually, all senses are pertinent to a lion’s success to locate food. Olfaction is important in the life of a lion; using scent marking as


an indicator of an animal’s sex, how recently that animal was present, and its physiological state (Schuett and Frase 2001).

Many studies have focused on olfactory enrichment in captive felids to reduce inactivity and stereotypies (Baker et al. 1997, Lewis 1992, Schuett et al. 2001, Noonan 1999, Pearson 2002). A study by Baker (1997) at the Houston Zoological Gardens looked at the effect prey and adversary feces had on lion behavior. They found that the prey species Cape hartebeest (Alcelaphas buselaphus caama), Dorcas gazelle (Gazella dorcas), Grant’s zebra (Equus burchelli bohmi), greater zebra (Tragelaphus strepsiceros), nyala antelope (Tragelaphus angasi), and white–beared gnu (Connochaetus taurinus albojubatus) samples led to a significant increase in olfaction, territorial, and social behaviors between lions, including “play behavior, rubbing, and scent marking” (Baker 1997). These elevated behavior levels continued for the following 24 hours, whereas investigative behavior, a behavior used in the search for prey, was observed during sample presentation and for 48 hours following the removal of the samples. Other studies have found that zebra feces elicits higher activity levels and behaviors such as scratching, tracking, sniffing, rolling, and social behavior versus no scent presentation that showed very low activity levels and no social behavior (Schuett and Frase 2001, Noonan 1999). The introduction of scents (such as cat nip, peppermint oil, rosemary, all-spice, cinnamon, and chili powder) to large felids have all shown to increase activity levels and behaviors such as rolling, rubbing, solitary play, and allo-grooming (Lewis 1992, Schuett et al. 2001, Pearson 2002).

The relationship between cortisol, activity levels, and olfactory enrichment has been poorly studied. Rafacz and colleagues (2014) looked at the hormonal and behavioral response to odor cues as enrichment in captive African wild dogs (AWD: Lycaon pictus), one dominant and one subordinate individual. They presented three odor cues: a competitor (lion), a natural prey (Grant’s gazelle), and an unnatural prey (cattle). Both AWDs showed a significant increase in activity with the presentation of the gazelle cue; and while not significant, activity levels increased during and post presentations of the lion and cattle cues. The dominant AWD demonstrated significantly lower fecal glucocorticoid metabolite (FGM) after the lion cue than before, while the subordinate AWD demonstrated higher FGM after the gazelle cue than before. While the relationship between FGM and activity level was inconsistent, researchers attribute these results to the interaction of the different social ranks.

No published study has examined the relationship between activity levels, enrichment, and cortisol levels in captive felids. While both the African wild dog and African lion are carnivores and pack species, canids have a significantly more structured social organization that is “phylogenetically more ancient and thus more highly developed” and requires greater cooperation in hunting (Rudnai 1973). As lions have a more relaxed social structure and group cooperation is less vital during a hunt (Rudnai 1973), presenting olfactory cues to lions may not produce the same relationship between hormone and activity level as it did in the African wild dogs. Additionally, the three odor cues in the AWD study were presented only once in one location behind a chain-linked fence and therefore, were not accessible by the dogs. Presenting each olfactory cue in an accessible location may mitigate any negative effects produced by social structure.


It is possible that inactivity in the Detroit Zoo lions is the result of the lack of necessity to perform species-specific behaviors, which subsequently could cause physiological side effects. The objectives of this study are to a) determine the fecal cortisol levels in the absence of a stimulus b) understand how presenting olfactory stimuli affects behavior and cortisol levels c) compare the effectivenessof two novel scents: that of a prey species and the oil of a plant that would not be encountered in a lion’s natural habitat but has been shown to increase activity levels in other captive felid studies (Schuett et al. 2001, Pearson 1999). It is expected that the presentation of both scent cues will increase active behaviors and decrease inactive behaviors, which subsequently will decrease fecal cortisol levels. It is important to note that since the peak activity levels of their wild conspecifics occur in the late night and early morning hours, it is possible that the lions at the Detroit Zoo are active during times when we are not observing them. If this is the case, the results may not show a significant difference in activity level before and after enrichment presentation. Nonetheless, the expectation is that the difference still would be evident in fecal cortisol levels.

MethodsThe Detroit Zoo is home to 1.2 African lions (Panthera leo): Simba, Bikira, and Erin. Their habitat consists of a 7500ft2 outdoor enclosure (on exhibit) and a smaller indoor enclosure. Features of the outdoor enclosure includes several trees, a grassy area with a small pool and flat rocks which can be heated, and a large rock wall in the rear of the enclosure that has alcoves and flat areas. The indoor enclosure is made up of 10 individual stalls with concrete floors, mesh barriers, an overhead chute system that allows Simba and Erin access to one another, several rotating toys, elevated platforms within each stall with ramp access to some, movable fire hose beds, and scratch boards. Due to old age and poor health, Bikira is housed separately from her two conspecifics, but still has auditory, visual, and olfactory access to them when all three lions are indoors. Simba and Erin are locked out on exhibit during the day, being let out in the morning at approximately 10:00hr and brought in any time after 17:00hr. Observations will be conducted when the lions are on exhibit, therefore, only Simba and Erin will be subjects of this project. All further reference to the lions will exclude Bikira as she is not a part of this study.

The lions are fed in the evening when they are brought in for the night. Animals are fed a standard feline diet with the addition of a carcass on occasion. Training sessions are provided in the morning, before the cats are let out, anywhere from one to six times a week, depending on the cat. Part of the lions’ diet is used as reinforcers during training sessions. The lions are trained to perform behaviors pertinent to their husbandry and medical care: tail presentation for blood draw and blood pressure, mouth open for mouth checks, as well as up, down, and side. The keepers of the Detroit Zoo lions do not use an enrichment schedule, rather providing enrichment at a random frequency. Types of enrichment used span from an array of various toys, beddings, and scents. The lions have received various scent enrichment over their time at the Detroit Zoo: a variety of spices and herbs, various perfumes, and also fecal samples from the Southern white rhinoceros (Ceratotherium simum simum) at the Detroit Zoo (L. Butler, personal communication).


Fecal samples will be collected during the three weeks prior to experimental data collection. There will be no change in the current enrichment schedule or husbandry activities, with the exception that no scent enrichment will be given outside of study conditions three weeks prior to or during data collection. Behavior, exhibit location (see Figure 1), proximity to conspecific, weather, visitor number and noise level (collected using the NoiseWatch application on an iPhone), and substrate used for inactive behaviors will be observed and recorded for 30 minute intervals. The introduction of olfactory enrichment will begin following three weeks of fecal collections. The two scents will be presented separately over a six week period. Zebra will be presented the first six weeks followed by a one week break. Peppermint oil will be presented for three weeks followed by a two week break, and presented again for another three weeks (see Table 1). Each scent will be given in the morning of the second day of observation each week and taken away at the end of that second day. As the lions’ rotation schedule is often inconsistent, it may not be possible to take out the scents at the end of the second day. In such cases, scents will be taken out as soon as possible and keepers will record appropriately. Enrichment items will be presented in the morning after the lions have entered the outside enclosure. Zebra feces and a peppermint oil-saturated piece of cardboard will be presented in separate paper bags on their corresponding days. Keepers will stand on the roof overlooking the outdoor enclosure and toss each scent bag in the same area. Each scent will have an equal number of presentations (see table 1). Observations will occur on the day before presentation, the day of presentation, and the day following presentation. A four-day break will follow in which no observations will be taken and no new scent presented. The purpose of the break is to reduce the potential continued impact of the previous week’s enrichment on the results of any given week.

Location will be recorded by these guidelines (all directions will be oriented from an observer’s view point facing the enclosure): Location 1 is from the left most point of the enclosure to the right most point of the pool. Location 2 is from the right most point of the pool to the left side of the large tree trunk towards the middle of the enclosure. Location 3 is from the left point of the tree trunk to the right most point of the two stalagmites. Location 4 is from the right most point of the right stalagmite to the right most point of the enclosure (see Figure 1 for visual representation).

Week Scent Given-31 None-2 None-1 None12 Zebra2 Zebra3 Zebra4 Zebra5 Zebra6 Zebra7 Break8 Peppermint9 Peppermint


10 Peppermint11 Break12 Break13 Peppermint14 Peppermint15 Peppermint

Table 1. A proposed timeline for the presentation of both olfactory enrichments.1. A negative number indicates a week that data is not collected. 2. A positive number indicates a week that data is collected.

Data will be collected on the pair of lions using an instantaneous and an all-occurrence sampling method. Instantaneous sampling will occur at one-minute intervals for activity budget behaviors (see table 3) and all-occurrence sampling will be recorded for the all-occurrence behaviors (see table 4) that occur. Each observation session will be 30 minutes in length. Three observation sessions will occur during three time intervals, respectively (see Table 2) throughout the day. Three days of observations (Tuesday, Wednesday, and Thursday) will be conducted each week for the duration of 12 weeks.

Session Time Interval1 10:00-12:002 12:00-14:003 14:00-16:00

Table 2. Proposed data collecting time intervals for a given day.

Fecal samples for each lion will be collected as often as possible (allowing at least 24 hours between each sample) starting the day of scent presentation and continuing for the following four days, with a total of five potential collections each week per lion. For the three weeks prior to data collection, fecal samples will be collected following the same schedule as the data collection period. Shown by Fuller et al. (2011), it takes approximately one day for a lion to complete a cycle of digestion. Therefore, the proposed fecal collection schedule is chosen to capture the complete realm of digestion, including before the expected effects of scent presentation and several days following. Individual samples will be marked with blue and green food coloring to distinguish between animals. This will allow for a potential total of 15 pre-study samples and 60 study samples for a total of 75 samples per lion. The proposed fecal collection schedule is preferred; however, as the lions’ rotation schedule is often inconsistent, five samples per week may not be possible. In this case, as many samples as possible will be collected. An average level in the pre-study period will be compared to average levels for each scent in the study period. Keeper staff will be responsible for collecting samples. Samples will be stored in a Ziploc bag marked with the lion name, date, and time of collection. After collection, samples will be stored immediately in a -20 degrees C freezer until they are sent to the St. Louis Endocrinology lab for analysis.

To account for extraneous husbandry variables, the keepers will complete a form each week in which they will record enrichment given, training sessions, scent time introduction and removal,


any diet additions, time the lions are let out in the morning, nights when the lions remained outside, and any additional factors of note.

Data AnalysisActivity budgets will be calculated by dividing the instances of each behavior by the total number of scans. Activity budgets will be compared between baseline and enrichment conditions (both overall and individual) using G-tests. Fecal glucocorticoid metabolite levels (ng/g) will be compared across conditions using mixed effect linear models with lion ID as a random effect and/or non-parametric statistics (Friedman’s two way ANOVA and Wilcoxon signed rank tests).

Expected ResultsIt is expected that the presentation of both scent cues will correlate with an increase in active behaviors and a decrease in inactive behaviors. Expectations are such that activity levels will be higher on the day of and following presentation than the day before presentation. Fecal cortisol levels will be higher during the pre-study collection than during study collection. Decreased fecal cortisol levels will be seen starting approximately 24 hours after scent presentation each week.


Ethogram for African LionInstantaneous Behaviors

Behavior Category

Behavior Definition

Inactivity2

Rest Cat has all four limbs and body on ground1, eyes can be open or closed, head up or down

Sit Cat has haunches and front paws on ground, chest and forearms are upright

Stand Cat has all four paws on ground

LocomotionWalk/Run Cat moves from one location to another with an apparent goalJump/Climb Cat moves from a lower point to a higher point, or vice versa, in a

single motion

Ingest

Eat Cat lowers mouth toward food (mouth is within 6in of food), uses paw(s) to move food to mouth, inserts food into mouth, bites food with mouth, licks food with tongue, includes jaw movement after food insertion

Drink Cat lowers mouth toward water source or laps up water into mouth with tongue

Other

Excretion Cat urinates or defecates, includes vomiting Self-groom Cat licks, scratches, or bites self with the intention of cleaningStretch Cat extends part(s) of its body to full lengthNot visible Cat is not visible to observer

Table 3. Ethogram for instantaneous behaviors.

1. Ground is defined as any substrate an animal has the opportunity to be on in its enclosure: grass, rock, water, or tree limb.

2. Inactive behaviors are only recorded in absence of other behaviors; if animal is performing an inactive behavior with another behavior, the other behavior takes precedence.


All-Occurrence Behaviors

Behavior Category Behavior Definition

Stereotypic Pace Cat walks with no apparent goal; walking becomes pacing after cat completes three rotations of the walking pattern

Olfaction

Smell/Sniff Cat inhales scent from an object, area, or the air

Flehmen

Cat opens its mouth, upper lip curled back, teeth are exposed, face is scrunched, eyes are squinted or closed, tongue may or may not be out; position must be held for more than two seconds

Rub3 Cat pushes head and/or body against an object

Roll3 Cat lowers body to the ground and rotates from side to side while lying down on back

Social

Allo-groom Cat licks or scratches conspecific with the intention of cleaning

Play Cat swats, pounces, “hugs”, or jumps on conspecific

Chase Cat runs in pursuit of the other who is simultaneously running and withdrawing

Agonistic

Dominance/Threat (Strut)

Cat stands tall, shows side, walks stiffly, tail erect over back

Defense DisplayCat has flat ears, barred teeth, marrow eyes, head may or may not be turned, can be crouched or lying on back, may or may not be vocalizing

Aggression Cat slaps, grapples, or bites conspecific in a hostile manner

Object Manipulation

Paw Manipulation Cat moves non-food object between front paws

Scratch Cat has front claws protracted and moves claws against an object or substrate, sweeping paw(s) towards body

Carry Cat picks up non-food object with mouth and moves it from one location to another

Lick Cat drags tongue across non-food object; does not include grooming

Bite Cat puts mouth around a non-food object and exerts force; may be a form of play

Chew Cat grinds a non-food object with mouth

Other

Investigate Cat moves head toward an object or area to gain more information

Vocalize Cat creates any noise with its mouth(e.g. roar, hiss)

Mark Cat sprays a vertical object (e.g. on a rock) from posterior, tail raised or rubs paws on ground

Stalk Cat walks slowly with legs bent slightly, eyes focused on a specific item or conspecific


Table 4. Ethogram for all-occurrence behaviors.

3. This behavior is included in the olfaction category due to the findings of previous studies that the introduction of novel scents produces this behavior in captive felids. (Lewis 1992, Schuett et al. 2001, Pearson 2002).


Figure 1. Map of the outdoor lion enclosure representing the four possible locations.


CZAW Lion Study-Keeper Form*This sheet pertains to Simba and Erin only.

*Please fill out by the end of the week*Once completed, please return to Jourdan Ringenberg,

Stephanie Allard, or Anna Murray. Thank you!!

Please answer #1-4 for Tuesday, Wednesday, and Thursday.

1. Check if enrichment was given: T___ W___ Th___

2. Type of enrichment (describe below):

Day Type

Tues

Wed

Thurs

3. Training sessions (circle which lion): Tues S E Wed S E Thurs S E

4. Time let out (keep blank if they were already outside): Tues ______ Wed______ Thurs______

5. Wednesday: Scent enrichment given at ________ AM.6. Scent enrichment was removed (please indicate day of week and time of day):

__________________________________________________________________

Please describe the following conditions that happened this week for #7-10.

7. Diet additions, type and what day(s) (carcass given, etc.):

_________________________________________________________________________________

8. Simba and Erin stayed outside on which nights:

_________________________________________________________________________________

9. Stereotypic behavior witnessed, type and what day(s) (pacing, etc.):

_________________________________________________________________________________


10. Any unusual events that happened or other additional comments:

_________________________________________________________________________________

_________________________________________________________________________________

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The Impact of Olfactory Stimulation on the Behavior and Hormone Levels of the African Lions at the Detroit Zoo