adaptation - characteristics of life. types of adaptation
The Impact of Olfactory Stimulation on the Behavior and Hormone Levels of the African Lions at the Detroit Zoo
1. Jourdan Ringenberg
CZAW Resident
Session II 2014
The Impact of Olfactory Stimulation on the Behavior and Hormone Levels of
the African Lions at the Detroit Zoo
Introduction
African 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
2. Jourdan Ringenberg
CZAW Resident
Session II 2014
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).
3. Jourdan Ringenberg
CZAW Resident
Session II 2014
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.
4. Jourdan Ringenberg
CZAW Resident
Session II 2014
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.
Methods
The 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
5. Jourdan Ringenberg
CZAW Resident
Session II 2014
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.
6. Jourdan Ringenberg
CZAW Resident
Session II 2014
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 None
12
Zebra
2 Zebra
3 Zebra
4 Zebra
5 Zebra
6 Zebra
7 Break
8 Peppermint
9 Peppermint
10 Peppermint
11 Break
12 Break
13 Peppermint
14 Peppermint
15 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.
7. Jourdan Ringenberg
CZAW Resident
Session II 2014
Session Time Interval
1 10:00-12:00
2 12:00-14:00
3 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 Analysis
Activity 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 Results
It 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.
9. Jourdan Ringenberg
CZAW Resident
Session II 2014
Ethogram for African Lion
Instantaneous 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
Locomotion
Walk/Run Cat moves from one location to another with an apparent goal
Jump/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 cleaning
Stretch Cat extends part(s) of its body to full length
Not 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.
10. Jourdan Ringenberg
CZAW Resident
Session II 2014
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 Display
Cat 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
11. Jourdan Ringenberg
CZAW Resident
Session II 2014
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).
14. Jourdan Ringenberg
CZAW Resident
Session II 2014
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.):
15. Jourdan Ringenberg
CZAW Resident
Session II 2014
________________________________________________________________________________
_
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:
________________________________________________________________________________
________________________________________________________________________________
__
References
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16. Jourdan Ringenberg
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Zoo Atlanta. Journal of Applied Animal Welfare Science. 15: 313-328.
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Skibiel, A.L., Trevino, H.S. & Naugher, K. (2007). Comparison of several types of enrichment
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