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Wild Cats in Captivity: On Improving Captive Environments with Regard to Biology and Behaviour BY Leandra Irene Lyniuk A Thesis Submitted to the Division of Natural Sciences New College of Florida In partial fulfillment of the requirements for the degree Bachelor of Arts in Biological Psychology Under the sponsorship of Dr. Alfred Beulig Sarasota, Florida May 2011
ii Table of Contents Table of Contents ................................ ................................ ................................ .............. ii List of Figures ................................ ................................ ................................ ................... iii Acknowledgements ................................ ................................ ................................ ........... v Abstract ................................ ................................ ................................ ............................. vi Feline Biology and Behaviour ................................ ................................ .......................... 1 General family Felidae ................................ ................................ ................................ ................. 4 Leopards (Panthera pardus) ................................ ................................ ................................ ...... 12 Lions (Panthera leo) ................................ ................................ ................................ .................. 17 Biology ................................ ................................ ................................ ................................ ... 18 Pride Structure ................................ ................................ ................................ ....................... 19 Sex Ratios and Conservation ................................ ................................ ................................ 22 Lion Coalitions ................................ ................................ ................................ ....................... 25 Pride Subgroups ................................ ................................ ................................ ..................... 27 Dispersal of Offspring & New Pride Formation ................................ ................................ .... 30 Inter Pride Interactions ................................ ................................ ................................ ........... 31 Communica tion ................................ ................................ ................................ ...................... 32 The Captive Environment ................................ ................................ .............................. 37 Enrichment ................................ ................................ ................................ ................................ 37 Case Study ................................ ................................ ................................ ....................... 42 Methods ................................ ................................ ................................ ................................ ..... 43 Subjects ................................ ................................ ................................ ................................ .. 43 Materials ................................ ................................ ................................ ................................ 49 Procedure ................................ ................................ ................................ ............................... 49 Data analysis ................................ ................................ ................................ .......................... 50 Results ................................ ................................ ................................ ................................ ........ 50 Discussion ................................ ................................ ................................ ......................... 66 Appendix ................................ ................................ ................................ .......................... 73 References ................................ ................................ ................................ ........................ 79
iii List of Figures Figure 1: Author with Seze at the St. Augustine Wild Reserve ................................ ....................... v Figure 2: Felidae Family Tree with Zoogeographical Regions. Taken from (O'Brien, 2005). ........ 5 Figure 3: Male (top) and female (bottom) Amur leopards. Taken by author at Jacksonville Zoo & Gardens. ................................ ................................ ................................ ................................ ......... 14 Figure 4: Lion pride with att ending male Taken from (L.P.M. 2011). ................................ .......... 19 Figure 5: Tiger using feeding pole enrichment as invented by Law (1997). Taken from (Malpass Oz Adventure. 2011) ................................ ................................ ................................ .................... 39 Figure 6: Lion enclosure map with location designations. H=hill, S=south, E=east, N=north, W=west. ................................ ................................ ................................ ................................ ......... 44 Figure 7: Leopard enclosure map with location designations. C=center, S=south, E=east, N=north, W=west. ................................ ................................ ................................ .......................... 45 Figure 8: Laini (top) and Tamu (bottom) sister lions. Taken by author at Jacksonville Zoo. ........ 46 Figure 9: Top picture: Nikolai (top) on center tree & Makarii (bottom) in center. Bottom picture: Makarii (left) & Nikolai (right) on center tree. 48 Figure 10: Graph illustra ting behaviour category frequencies across species and sexes. Notice activity is the most frequent behaviour followed by resting, stereotypy, and breeding. ................ 52 Figure 11: Graph showing species comparison of proximity while resting frequencies. P. pardus was observed resting far most frequently while P. leo was observed resting near most frequently. ................................ ................................ ................................ ................................ ....................... 53 Figure 12: Proximity while Rest ing Frequencies for P. leo. There is a difference between the sexes with females resting near and males resting far most frequently. ................................ ........ 54 Figure 13: Individual Behaviour Frequencies across all s pecies and sexes. For leopards, the female exhibited B1 most frequently and the male exhibited B11. For lions, the female exhibited B2 most frequently and the male exhibited B2. ................................ ................................ ............. 56 Figure 14: Species Comparison of Individual Behaviour Frequencies. Both leopards and lions exhibited the walk behaviour most frequently. ................................ ................................ .............. 59 Figure 15: Graph illustrating location frequencies of leopards. The female occupied the south area most frequently, while the male occupied the center area. Note that C=center, E=east, N=north, S=south, & W=west. ................................ ................................ ................................ ...................... 61 Figure 16: Graph illustrating location frequencies of lions. The female occupied the hill area most frequently, while the male occupied the south area. Note that H=hill, E=east, N=north, S=south, & W=west. ................................ ................................ ................................ ................................ ..... 62
iv Figure 17: Graph showi ng leopard behaviours by location frequencies. Notice that in the center, north, east, and west the most common behaviours are activity; while in the east the most common was resting. Note that C=center, E=east, N=north, S=south, & W=west. ...................... 65 Figure 18: Graph showing lion behaviours by location frequencies. Notice that the most frequent behaviour that occurred in the hill area was resting; while in the east, north, south, and west areas activit y behaviours were most common. Note that H=hill, E=east, N=north, S=south, & W=west. ................................ ................................ ................................ ................................ ....................... 65
v Acknowledgements I would like to thank the Jacksonville Zoo & Gardens for allowing me to conduc t research at their facility. All my Ne w College professors who have guided me through the sea of knowledge; namely my sponsor Dr. Alfred Beulig and committee members Dr. Gordon Bauer and Dr. Heidi Harley. Thank you Duff Cooper for all of the hours spent helping me analyze my data. Mom you have provided me with unconditional support and Rebecca Hackney thank you for letting me live with you over the summer while I collected data at the Zoo it was good practice for ou r future! Leo Ferretti, thank you for your patience, I love you. Julie Diaz, my dearest and oldest friend, thanks for everything. Deborah Warrick, thank you for opening your heart and facility to me, you have changed my life. To all the felines in my life, wild and domestic, you are my constant inspiration and fascination. I saved the best for last I want to thank my New College Family these have been the greatest four years of my life because of your love! Figure 1 : Author wit h Seze at the St. Augustine Wild Reserve
vi Wild Cats in Captivity: On Improving Captive Environments with Regard to Biology and Behaviour Leandra Irene Lyniuk Abstract Leopards ( Panthera pardus ) and lions ( Panthera leo ) are the wild feline species exami ned in this thesis and case study. They are considered charismatic mega fauna and popular in captivity w hile some subspecies are critically endangered in the wild. A literature review reve aled that these species may be more complex behaviour ally than previo usly thought T he conclusion was made that optimal captive habit ats need to cater to each species unique behaviour al and biological needs in order for these species to thrive in captivity Captive habitat is the last environment in which the y are supported A case study conducted at the Jacksonville Zoo and Gardens consisted of behaviour al n=2 ) and lions ( n=4 ) Data were analyzed with regard to frequencies of behaviour s and location. There were differences b etween the sexes of each species and between the species themselves. This gives supporting evidence that captive environments should be designed with regard to behaviour and biology. Individual behaviour can be used to adjust enrichment techniques and husbandry practices in order to meet the needs of the individual in the captive environment. _______________________________ Alfred Beulig, PhD Division of Natural Sciences
Feline Biology and Behaviour Wild cats in captivity are an ever increasing phenomenon. With habitat destruction and rampant hunting they are being pushed out of their natural habitats. All 36 species of wild feline are listed as decreasing in population by the I nternational Union for the Conse rvation of Nature ( IUCN 2010). The future of wild feline rests in the hands of humans in the areas that have been set aside for them. In the case of endangered felines most of that area is in captivity. There are more tigers in the United States than there are in the wild. Since the future of these species relies upon responsible management it is imperative that we learn as much as possible about them. Knowing how a cougar functions biologically and behaviourally will give us the tools to keep populations v igorous. By studying felines in the wild we can then use that information to create captive environments that are naturalistic and allow captive felines to express their full repertoire of behaviours. This thesis takes a macro look at maintaining wild fel ine species in captivity. Biology and behaviour together determine the whole animal and when attempting to preserve a species from extinction both must be considered Two species in particular were given special consideration, lions and leopards Muc h work has been done on developing and implementing good husbandry practices. Scientific advances have led us from the routine practice of keeping wild animals in tiny bare cages to providing them with naturalistic habitats through study of their species typical requirments This thesis aims to build upon that work and provide further evidence for the need to continually improve upon captive habitats.
2 A properly maintained captive population will breed well and thus survive, even if the wild population is no lon ger allowed to flourish. Captive populations also provide for the hope of reintroduction one day into now protected areas from which that species had previously been extirpated. Well managed captive populations can hold valuable genetic diversity which in the future could benefit and strengthen the wild population. Species that have been successfully reintroduced include: Arabian oryx, plains bison, California condor, Mauritus kestrel, black footed ferret, and Guam rail (Snyder, N. 1996). The reintroduction s have been successful and provide an example of the value of captive populations Tigers are in extreme danger of becoming extinct in the wild, yet the ca ptive population is flourishing profit organizat ion formed to release captive animals into formally occupied areas (savechinastigers.org). They have taken founding stock of captive south Chinese tigers and relocated them to a reserve in the hopes that the second generation onwards will have learned the necessary skills to survive in protected parks in their native China. This project has received criticism, mainly because the successful reintroduction of captive bred carnivores into the w ild has been overwhelmingly unsuccessful. Successful reintroductions of the species mentioned above in part resulted from reintroducing them into predator impoverished areas. Thus for reintroduction to be successful the wild habitat must be appropriate. However, the relocation and reintroduction of carnivores into protected parks was initially unsuccessful until the proper technique was developed through trial and error. Leopards, lions, and hyenas have all bee n successfully reloc a ted to protected parks w h ere they had previously been
3 extripated (Hayward, 2007a; Hayward, 2007b) The south Chinese tigers have a chance at successful reintroduction if they are released into areas where they will be protected from poaching, have ample prey numbers, and low pred ator density. When a top predator is removed from an ecosystem, the balance between predator and prey is skewed. The gray wolf is an excellent example of a species that was extirpated from the continental United States with unseen ramifications. With the wolf gone, prey species such as deer and elk experienced a population boom. Increased numbers of herbivores began to overgraze plant life and destroy forests. The entire ecosystem began to fail because of the overgrazing. Upon the reintroduction of the gr ey wolf into Yellowstone National Park the herbivore population was put back in check. Forests and grasslands began to recover (Ripple, W. & Beschta, R. 2003) and the overall health of herds improved. The grey wolf population within Yellowstone has expande d outside park boundaries because of the abundance of prey species in the surrounding areas. Grey wolves can now be found in several states such as Wyoming, Idaho, Montana, and Washington. The Mexican grey wolf ( Canis lupus baileyi ) had been practically ex ( US Fish & Wildlife Service. 2010 ). The remaining wild individuals were captured in 1977 and a captive breeding population was created. In 1998 eleven captive reared Mexican grey wolves were released into the Blue Range Wolf Recovery Area. The reintroduction is considered a success as at present there are an estimated 50 individuals in the BRWRA. This is one of the first successful reintroductions of a carnivore species and should be used as a model for the reintroduction of feline sp ecies.
4 A case study was performed that looked at the space usage and activit y budget of two big cat species, Transvaal lions ( Panthera leo krugeri ) and Amur leopards ( Panthera pardus orientalis ) at the Jacksonville Zoo and Gardens The aim of the study w as to determine the frequency of behaviours perform ed, both individually and categorically the locations in the enclosure that the subjects were utilizing and the purpose. Analyzing the activity budget allows u s to determine the percentage of time that an animal spends performing a particular behaviour. T his reveals those behaviours which are e xpressed most frequently and their importance to the well being of the animal. Space usage is analyzed to determine which areas of the habitat were used. By l ooking at space usage and activity budget together an assessment can be made of the areas used, and the use made of it by the species in question These data can be used to design better captive environments and d etermine appropriate enrichment techniques Optima l habitats will encourage breeding. A cat that has all of its physical and behavioural needs met will have less stress which leads to greater reproductive success. General family Felidae Felidae is the family name for all cats. Forty one species are recognized within this family. There are two subfamilies Pantherinae and Felinae E ight genetic lineages are recognized based on genotypical groupings, these are: (1) Panthera, Unica, Neofelis; (2) Pardofelis, Catopuma; (3) Leptailurus, Caracal, Profelis; (4) Leopardus; (5) Lynx; (6) Puma, Acinonyx; (7) Prionailurus, Otocolobus; and (8) Felis (Wozencraft, W. C. 2005) The last four linages are most closely related and form a clade within Felinae Species within Pantherinae with t he genus Panthera
5 lion P. leo jaguar, P. onca leopard, P. pardus and tiger P.tigris Unica (snow leopard, U. unica ) and Neofelis (clouded leopard, N. nebulosa, and Bornean clouded leopard, N. diardi ) complete the Pantherinae subfamily. The other 34 species in subfamily Felinae The Felidae family tree with zoogeographical regions is illustrated in Figure 1. Figure 2 : Felidae Family Tree with Zoogeographi cal Regions. Taken from (O'Brien, 2005). A common distinction between big and small ca ts are the types of vocalizations they are able to make. All felines share a similar set of basic vocalizations, with each species having its own unique differences. Spit ting, hissing, growling, snarling, and mewing are common while purring is found in all small cats and roaring is found in all big cats. Small cats are able to purr on the inhale and exhale, while big cats can only produce the sound on the exhale. This was previously thought to be due to the ossification of the hyoid bone in the small
6 cats, enabling them to purr but not roar. The partly ligamentous hyoid found in big cats enabled the opposite, the ability to roar but not purr. Based on the data available no correlation can be substantiated. However, Weissengruber et al. ( 2002) hypothesize that the ability to purr can be distinguished based on the presence or absence of a large pad of fibroelastic tissue in the vocal folds. The large pad, found in Pantherinae, inhibits the rapid twitching of the vocalis muscle which causes purring in Felinae What enables big cats to roar is the ligamentous hyoid which lowers the larynx, this gives vocalizations a lower formant frequency. Thus purring and roaring are not mutual ly exclusive in the fact that these vocalizations arise from anatomically different areas. Felines are obligate carnivores, meaning that they gain all their nutritional needs from other animal s flesh They are the only true terrestrial carnivores as species of Canidae and Ursidae are omnivorious, no species of feline can digest plant matter for nutritional gain. A number of morphological features are thought to have coevolved with this trait. First, the flexible skeleton reflects agility in quadrupe dal stalking, running, and leaping (Homberger & Walker, 2004) The forelimbs can deliver a powerful strike and the forepaws are able to manipulate prey. On each paw recurved claws give excellent grip and are retractable allowing for silent locomotion. The ligament retracts the claws into a sheath of skin at rest and extends to reveal the claw. Cats are digitigrades with five digits and a dew claw on the forepaws and four digits on the hindpaws. These traits alone point to an enhanced agility for climbing t rees and grasping prey. The skull is designed to allow for maximum leverage when shearing off chunks of meat as the jaws can
7 only move vertically. A large sagittal crest and wide zygomatic arches allows for more powerful jaw muscles (such as the masseter) which aide in gripping struggling prey. Sensitive proprioceptors in the canine teeth help guide them to the gap between vertebrae, effectively severing the spinal cord during the killing nape bite (Leyhausen, 1979) Another adaptation for meat eating is fo und on the tongue in the form of horny papillae. These tiny papillae act like Velcro a nd rasp soft tissue from bone (t hey also facilitate grooming of the fur ) Felines lack the receptor associated with the detection of sweet stimuli (Li, X. et al. 2005). T his was another evolutionary trait among many that affected their adaptation to carnivorous behaviour A shortened rostrum brings the eyes as the dominating feature of the feline face. They are located high and central, this positioning provides binocular vision. Cats rely on sight to hunt (Leyhausen, 1979) and have excellent form vision, with rods dominating the retina. They also contain enough cones to distinguish colors (though not nearly as refined as primate color vision). A tapetum lucidum reflects l ight back through the sensory receptors and allows for superior night vision. The typically pale iris contrasts with the pupil which is elliptical in shape in the small cats and rounder in the big cats. The pupil changes size in accordance with light inten sity but also in respo nse to autonomic state. Kleiman & Eisenberg ( 1973) state that the pupillary changes due to changes in autonomic state can serve a communicative purpose, with conspecifics between the pale iris and black pupil would make any changes an effective signal.
8 Felines do not rely on olfaction to sense and perceive their environment as much as canines. However, their sense of olfaction is highly developed and essential in consumatory behaviour and communic ation (Leyhausen, 1979) Leyhausen observed that w hen presented with food cats will not consume it until olfaction stimulates appe ti tive behaviour s. Felines have a Vomeronasal organ which detects pheromones. The Flehmen response is the behaviour associated with the use of the VNO and is commonly observed in social and reproductive situations. There are two main scent glands, the facial and an al, which are used for marking. Spra ying of urine is used as a communicative signal to designate territory and reproductive status. The whiskers, or vibrissae, serve as an important sense organ. They are speed, duration, and any rhythm of the deflection of a sinus hair from its normal position, and locate the point on the upper lip where the affected hair or hairs are ). In low light situations where visual stimulus is minimal the vibrissa e aide in capturing prey. The killing nape bite is directed by information from the vibrissae as well as consumatory behaviour Audition is highly developed as well though less understood. Small cats hear high frequencies quite well, most likely to hear r odent prey since felines do not make high pitched calls. During night hunts they rely heavily on audition to locate prey. Certain species rely on audition more than others. The serval ( Leptailurus serval )
9 has proportionally large ears that facilitate the l ocation of rodent prey underground and in tall grasses. Majority of feline species have a marked coat, either spotted, striped, rosette d or some combination, on a tawny background. The tail usually has a contrasting white or black tip at the end which se rves as a communicative signal (Leyhausen, 1979) Fur is dependent on habitat with northern species, such as the snow leopard, having a dense coat and tropical ones, such as the ocelot, having a sleek coat. Felidae species are found on every continent exc ept Antartica and Australia, they are most common in forested areas, and especially diverse in tropical forests. They have evolved to exploit arboreal niches as a top predator. Often smaller species are sympatric with larger ones. They will segregate thems elves either temporally, by being active at different times, or by hunting different prey animals. Felines are cryptic because they are generally solitary and nocturnal. Some species are crepuscular, having peaks of activity in the morning and evening wh en prey is vulnerable and temperatures are milder. Most species have not been studied in the wild, thus the behaviour al data available come from captive studies and from domestic cat studies. Felines typically hunt prey smaller than themselves using a char acteristic stalk and pounce technique. Being such efficient hunters cats do not need to group together, like wolves, in order to bring down prey. The exception is the lion, the only truly social felid, which may have become social in order to bring down th e large herbivores that predomina te open grasslands. According to Kleiman & Eisenberg ( 1973)
10 feeding behaviour of felids has permitted and may have promoted the development of a more or less exclusive home range use and a solitary Felid reproduction is shaped by the solitary condition. A female will go into oestrous for about a week, before and during she will leave scent marks and call in order to attract a mate. A male will only associate with a receptive f emale for a few days this leads to multiple male matings. Often litters consist of kittens from different fathers. This is because felines are induced ovulators, they must be stimulated vaginally to ovulate. This stimulation comes from penile spines which are androgen dependent. Thus the first male to mate with a receptive female may only fertilize a single egg which was released during the last day he accompanied her. This allows for the female to ch o ose the fittest male. The first male on the scene may n ot be the best, since home ranges can be quite large, the best male may not arrive within her territory for days. The males will compete with the fittest winning breeding rights. In this way the female assures that most of her kittens will come from stron g stock. Mothers rear their offspring alone after a gestation period of two months for smaller cats and up to three and a half for big cats. Commonly only three kittens are born to a litter (litters c an range from one to five). S mall litter size allows for neonates to be more developed and precocial than other carnivores such as canids. Felids are either seasonally or annually polyestrous allowing for a second breeding opportunity if the initial pregnancy fails or the initial litter is lost. This may be in part because most species inhabit tropical forest where the seasons are
11 mild and prey is abundant. This allows for the female to have ample food to provision herself and her young during pregnancy, nursing, and weaning. Offspring stay with their mother for a longer time than other mammals, with big cat mothers tolerating their offspring for years. The main reason for this is to give sufficient time for the young to learn th e necessary hunting skills. Many of the hunting behaviour s are innate but certain asp ects such as prey recognition must be taught (Leyhausen, 1979) of their grown daughters. Males disperse and must stake out a territory of their own often far from their natal home. This prevents inbreedi ng within the population. Male home ranges will overlap those of multiple females in order to promote breeding opportunities (Mizutani, 1998) Some species, such as lions and cheetahs, have a unique social system among males with littermates forming coalit ions that last a lifetime. Generally the only social bond formed in felids is the mother offspring bond, which itself is only temporary lasting until dispersal (except for lion prides) Dolphins follow a similar pattern, with the strongest social bonds for ming between mother and dependent offspring (Connor, Wells, Mann, & Read, 2000) Communication consists of auditory, tactile, visual, and olfactory signals. Vocalizations can either be used in close contact or for long distance signaling. Purring and m ewing are common close contact calls that indicate affiliation, while roaring and mating calls establish territory and reproductive status, respectively. Tactile communication mainly consists of grooming, head butting, and rubbing. Most species only exhibi t these behaviour s during reproductive episodes or are
12 seen between mother and offspring. The exception is lions where tactile communication plays an important role in pride interactions. Due to the excellent vision felids possess visual signals are quite important. As mentioned before pupillary changes can signal autonomic state. The eyes are ringed with fur of contrasting color further accent uating this area. B ody and tail postures, facial expressions and ear movements all serve communicative purposes. Leyhausen (1979) provides an excellent and thorough account of these. Even slight changes in posture are recognized and can elicit a reaction. Olfactory signals mainly come in the form of urine marking. Both sexes urinate and defecate around the bo rders of their territory and along common trails. Smaller cats that are sympatric with larger predators cover their wastes as an antipredator avoidance. Larger cats bring attention to these scent markings by leaving visual signals as well by scraping the ground. A nother olfactory visual signal is left on trees. Cats will scratch and then rub the facial scent glands, or spray, impregnating the scratch marks with the ir scent. Often trees at the bo rders of territories are recipients of such treatment and are frequentl y visited by neighboring conspecifics Leopards (Panthera pardus) Leopards are very cryptic, which partially explains why there is a stunning dearth of research on this species. They prefer forested areas over open grassland which makes them ha rder to track and see. Their spotted coat is excellent camouflage blending into the canopy; they are hard to spot even for experienced trackers. Most of the research on leopards concerns prey, hunting, and habitat assessments with data coming from kill sit e, scat samples, and pug marks. In captivity genetic and hormonal studies have given
13 insights into captive breeding strategies for endangered subspecies. Even with this limited information cognitive assessment can be made. Hunting preference and territory can indicate decision making and odd s assessment. Dispersal and kinship ties can show recogni tion of individuals and maintenance of social relationships. Complex scent marking behaviour s show highly developed communication. Preferences over time concerning prey, habitat, mate choice, conflict avoidance/confrontation indicate personality. The lack of research only serves as an incentive to learn more! Panthera pardus is the smallest species of the Panthera subfamily. They are variable in size across their range with males weighing between 66 200 lbs and females being smaller at 51 130 lbs. This variation in size is due to the multitude of habitats they can survive in. The most adaptable of the big cats they are also the most widespread, ranging from semid esert ecosystems to rainforests, to savannahs, to temperate mountain forests. Their historic range stretches from the African continent across the Middle East, into Asia, and up to the Russian far east and leopards can still be found in these areas ( U phyrk ina et al., 2001). In comparison to other felines they have relatively large skulls, long bodies, and short limbs. A larger skull allows for greater jaw strength and the long body and short limbs make them strong climbers. The greatest concentrations of le opards are found in forested areas reflecting these morphological adaptations. Leopards are well known for their beautiful coat. Rosettes of varying size adorn a golden background and a white underbelly. Differences in color and pattern arise from differen t habitats. African leopards have square rosettes while Asian subspecies rosettes are circular. Background color ranges from cream to black relative to habitat humidity. In the heavily forested tropical Malay Peninsula majority of leopards are melanis tic ( Kawanishi, K. 2010). The
14 I U C N lists the leopard as Near Threatened, with certain subspecies such as the Amur ( P. pardus orientalis ) lis ted as Critically Endangered (I U C N 2010 ). Figure 3 : Male (top) and female (bottom) Amur leopa rds. Taken by author at Jacksonville Zoo & Gardens. Leopards are so widespread because of their incredible adaptability in diet. They will consume whatever prey they can catch ranging in size from beetles to giraffe calves. Ninety two prey species have be en identified (Hayward, 2006). However, preferred prey is medium sized ungulates. Open land leopards are nocturnal or crepuscular depending on season, while woodland leopards are crepuscular or diurnal. Activity patterns depend not only on season but on th e type of prey, with hunting occurring at hours prey is most vulnerable and sympatric carnivores less active. In India where tigers and leopards coexist, there is no temporal separation of hunting behaviour s, instead each species takes
15 differently sized pr ey with tigers taking large and leopards taking medium sized prey species (Karanth, 2000) Two studies further illustrate the adaptability of the leopard. In the alpine zone of Mount Kenya diet consists mainly of rock hyrax and rodents (Rdel, 2004) and i n the prey impoverished Sanjay Gandhi National Park in India 70% of leopards diet consists of domestic dog and scavenged domestic buffalos (Edgaonkar, 2002). Leopards hunt using the stereotypical feline stalk, run, pounce technique; though in denser cover they will ambush prey. They rely on stealth for successful hunts and habitats with intermediate vegetative cover levels are favored by hunting leopards (Balme, 2007). Caching kills is common and savannah leopards are infamous for caching prey in trees. Cac hing in a tree prevents theft from other sympatric predators such as lions and hyenas. More commonly leopards will cache their kills in caves or dense vegetation rather than expend the energy required to carry it up a tree (de Ruiter, 2001) Leopards c an survive near human habitation and often go unnoticed because of because they follow the general feline repertoire of solitary condition, home range distribution, and reproductive behaviour They are solitary with home ranges of males grown daughters. They are polyestrous year round (Schmidt, 1988) and exhibit behaviour al oestrous y ear round in mild climates and seasonally in harsher ones (van Dorsser, 2007). Females call to males before and during oestrous with a charactistic sawing roar and leave chemical signals in the form of spraying (Poddar Sarkar, 2004). Litters usually number between two and four cubs. Offspring stay with their mother for three years, which is especially long for felids. After the first year they have gained the
16 necessary hunting skills to survive. The extra two years may be spent refining those skills and sco ping out their own territory. Both sexes are reproductively mature at around three years (van Dorsser, 2005; van Dorsser, 2007). Mothers may keep ties with offspring after dispersal, anecdotal evidence shows mothers and grown offspring coming together for days to hunt and socialize together (Estes, 1992) In areas were leopards come into contact with humans they are frequently termed conservation areas. In the case of transl ocation many times the efforts are unsuccessful because the area is prey impoverished or already saturated with other predators. The leopard quickly returns to its former range and meets an untimely end. It is essential that the suitability of the area is assessed in terms of numbers of suitable prey species and conspecifics. If these requirements are met r eintroduction can be successful (Hayward, 2007b). Al Johany (2007) further illustrates the n eed to identify suitable areas for conservation The people w ho live in leopard habitat are vital to conservation efforts. Local hunters and farmers can provide information on distribution and population size. Education efforts on the economic value of the leopards they live near can provide incentive to decrease po aching as a response to livestock predation. In areas with no local human population information on distribution and population size can be gained from f ecal samples The samples can effectively identify sympatric species in order to quantify numbers in th e wild but a reliable way to identify sex ratio is needed (Sugimoto, 2006) These conservation techniques are especially relevant when considering the Amur leopard ( Panthera pardus orientalis ). Amur l eopards are critically endangered in the wild with a pop ulation of only 40 individuals They have greatly reduced genetic variation and
17 are v ulnerable to inbreeding, reduced litter size, cub mortality, infectious disease, and poaching ( Uphyrkina, 2002). Genetic impoverishment resulting from inbreeding depressio n and demographic threats put this tiny population at high risk for extinction in the wild. The captive population is much more diverse and reintroduction of c aptive individuals to the wild population ca n improve population health ( Uphyrkina, 2003). This s trategy of strengthening the wild population has been proven effective in returning the Florida panther from the brink of extinction and should be considered viable for other endangered feline species. Lions (Panthera leo ) Lions, Panthera leo are the most social of felids. Thus th ey are the best species within F elidae to search for signs of higher cognition. Social animals are seen as having similar cognition to humans, since so much of human behaviour and culture is related to our sociality. Other sp e cies that are attributed with high levels of cognition have complex social systems. Dolphins live in fission fusion societies (Connor, Wells, Mann, & Read, such as lio ns, dolphins, apes, and humans, there are many long term advantages of sociality such as numerical advantage in territorial competition (Mosser & Packer, 2009). The goal of this section detail ing the behaviour and biology of lions is to examine t he wealth of literature on this species to find examples of what could be considered higher cognitive function through behaviour al observations. Proof of higher cognition can lead to better captive environments such as great ape species which receive a high level of specialized care in captivity (Davis, J. 2007) No formal studies have been done to assess cognition in wild felids. The a rticles concern ing lion behaviour that were reviewed show
18 strong evidence for higher cognition within Panthera leo Multiple facets of behaviour such as biology, pride structure, sex ratios & conservation, lion coalitions, pride subgroups, inter pride interactions, dispersal of offspring, new pride formations, and communication support this conclusion B iology Lions are the most sexu ally dimorphic species of F elidae, with males having large manes. The mane was thought by Darwin to have evolved as a protective trait. However, it is now considered to be a condition dependent signal (West et al., 2006). Males with larger, longer, and dar ker manes are preferred by females since those traits are caused by higher levels of testosterone. They tend to live longer, have greater survival after wounding and their cubs live longer. Males can be up to twice the weight of females (F unston M ills B i ggs & R ichardson 1998) weighing 330 530 lbs and be up to 10 ft long. Females weigh between 270 300 lbs and can be up to 9 ft long. Lions stand about 4 ft tall at the shoulder. During the Pleistocene subspecies of P. leo flourished across Africa, Europe, Asia, and the Americas (Yamaguchi, Cooper, Werdelin, & Macdonald, 2004) With the exception of modern Homo sapiens no other land mammal species has had a wider distribution than the lion (Kurten, B. & Anderson, E. 1980 ) Until fairly recently lions ranged over all of Africa, along the Mediterranean, and into Asia. Today, they are found only on national parks and game reserves within Africa, and within the Gir Forest National Park in India. The I U C N lists the lion as Vulnerable (I U C N 2010 ) Lions are heavily spotted at birth with the spots subsequently fading with age. Males are sexually reproductive at two years, are mature at 5 6 years of age, and can live up to 14 years. Females are also sexually mature at two years but typically do not have their
19 first lit ter till four years of age and can live up to 18 years (Mosser & Packer, 2009). In captivity both sexes can live to be over 20. Lionesses have from one to six cubs per litter and have a litter about every two years. Prides synchronize their estrus cycles a nd will suckle and rear their cubs communally (Packer & Pusey, 1983). Figure 4 : Lion pride with attending male Taken from (L.P.M. 2011). P ride S tructure Prides are made up of a group of related lionesses and their dependent offs pring. Lions live in a fission fusion society (Heinsohn & Packer, 1995) where all members are part of an inclusive group but frequently divide into temporary subgroups. Prides are associated with unrelated male coalitions or solitary males. These males ha ve exclusive breeding privileges and father as many cubs as possible within their tenure. When a resident male is usurped by a new coalition the new males will kill any young cubs they can in order to bring the females to estrus so they can in turn sire th eir own offspring.
20 Tenure periods average two years (Estes, 1992) ; just enough time to sire and see offspring to maturity. Pride structure varies according to habitat. Plains prides are smaller and more closely associate with their male coalitions, while woodlands prides are larger and associate less frequently with their male coalitions. Between lionesses there is no hierarchy or social ranking, this is thought advantageous to their style of communally suckling and raising cubs. Plains prides experience a hierarchy between the resident males and the lionesses male lions eating first, the females second, and the cubs last. This strategy is harmful to cubs, many die of starvatio n within their first year. Woodlands males almost exclusively hunt for themselves, thus eliminating the harmful repercussions to their cubs (F unston et al., 1998). Lionesses are known for doing most of the hunting while the males sit around waiting for di nner. This misconception about lion society is widely publicized in popular culture. Males must find a balance between protecting their offspring from other infantcidal males and ensuring their cubs get enough food. While within plains prides it is true th at lionesses hunt more frequently and their males scavenge off their kills quite often but in bringing down large prey such as buffalo or hunt for themselves. They a lso have been known to scavenge off other predators kills, including hyena, leopard, and cheetah. Plains males protect their offspring directly by accompanying the pride. Accompanying their pride not only protects the cubs, but also the females against ot her
21 males and non pride females. Accompaniment protects the pride from hyenas which will they outnumber them. Hyenas will not steal pride kills when males are present. Woodlands males take a different approach. The denser habitat ma kes it easier for males to hunt the large prey they favor, since buffalo favor woodlands over plains. These males indirectly protect their pride by patrolling their territory, scent marking, and roaring. These actions discourage other males from entering t style of pride protection has several advantages over accompaniment. First, it prevents other males from coming into contact with their cubs and females. Second, it protects the resources within the territory. Lastly, the possibi lity of the patrolling males taking over a neighboring pride and thus siring more cubs is increased. Since the males do not accompany the pride they cannot scavenge off them, leaving more food for the cubs, which further increases their survival. Males are better hunters in woodlands areas because there is prey large enough and they benefit from the added cover. In open plains they cannot chase down prey as effectively, especial ly since they do not hunt in large groups as females do, so they must rely on th eir pride to hunt. Woodlands lions are more efficient hunters and do not need to rely on their pride for food. Woodland territories are typically smaller and thus easier to patrol. Funston et al (1998) suggest three hypotheses for the different pride str uctures found in plains and woodlands; hunting success, territory and pride defense, and hyena density. Using these three hypotheses that are based on behaviour al data I think that they providence evidence for some level of higher cognition. Lions are abl e to assess territory quality and judge whether they can efficiently hunt for themselves. They are able to assess the size of their territory and judge whether they can efficiently patrol it. They
22 have some concept of numerosity relevant to their pride siz e versus neighboring prides (more evidence for this later), as well as the number of other males in the area and the number of hyenas that are within their territory. S ex R atios and C onservation Sex ratios greatly influence pride structure. This aspect of pride structure differs according to environment and human hunting pressures. Three to one in favor of females, is considered the best ratio for a healthy population. Harsh habitats are characterized by low prey density and high hunting pressure. In an o verhunted population the ratio is cl oser to 1:6 which correlates with a high infanticide rate. Since lion habitat is now restricted to parks and game reserves conservation is closely linked to sport hunting. Most parks are bordered by game reserves which attract tourists and hunters looking for lions. Lions from within the parks are attracted into the game reserves by baiting (Yamazaki, 1996) or by the territory left when resident males are shot (Loveridge, Searle, Murindagomo, & Macdonald, 2007). Lions a re also reintroduced into game reserves (Kilian, P.J. Bothma, J. du P., 2003). Hunting brings in the income needed to maintain these areas as important wildlife habitat. The game reserves must find a balance between conservation and running a business. The sport hunting of lions is the biggest money maker for game reserves (who charge $130,000 per hunt) (Loveridge et al., 2007). Sex ratios are a way for parks and game reserves to assess the health of a hunted lion population. Male depopulation has many effects. In prides that have no resident male they frequently lose kills to hyenas. This is one way that male depopulation affects the entire population. Resident males territory usually encompasses the prides territory. In over
23 hunted populations males in stead establish a home range that overlaps several prides territories, but does not encompass them all. This means that the males cannot patrol or accompany their prides leaving them vulnerable. More male cubs are born in areas that have low male densities This compensates for the high male off take but ultimately damages the population, since low numbers of reproductive females cause a population to decline. When a resident male is killed within a game reserve, his vacancy is filled by another male who m igrated from a protected park. This type of immigration from protected areas negatively affects the effectiveness of parks in protecting the species. If males are constantly being drawn out of the parks into game reserves then the park populations are bein g affected as well. In this way the low male density in game reserves extends into parks. This depletion influences the whole ecosystem. Without sufficient numbers of males, the hyena popula tion expands, prey species are a ffected, and even the landscape it self (from herbivore predation upon plants) changes. In a study led by Loveridge et al., ( 2007) they found that over half of the lions they tagged died (38 out of 62) mostly from sport hunting. Eighty two percent of the hunted lions were killed within 1k m of the park boundary. Most of the tagged adult (72%) and subadult (60%) males were killed. This shows that most of th e males in the population did not even reach maturity and the ones that did were quickly dispatched While female off take is less ( five of the 34 tagged females ) even a small decline in the female population can have devastating effects. Prides are more successful when they have more withstand high male mortality better if the female population remains stable.
24 In Zambia Yamazaki ( 1996) found abnormal social variation in a male depopulated area. Social variation is common in areas where lions are hunted for sport. Normally, subadult females join their pride. Subadults from different prides never join together to form a new pride. Prides are strictly made up of closely related females. Once a male coalition takes over a pride they only mat e with their lionesses. Prides do not accept non resident males. A naturally occurring variation to this theme is found in the Kalihari desert which is an incredibly harsh environment. There lionesses transfer between prides. Males rarely associate with fe males and instead of protecting a single pride, roam among prides. In ar eas with substantial cropping from hunting pressure lionesses from different prides will join together to form new prides and males will enlarge their coalitions after a pride takeover This type of social behaviour is abnormal and is a result of a harsh environment due to human disturbance. In Zambia male tenure periods were uneven, with some lasting days and others years. Some prides were without resident males for months at a time. T ypically a single male cannot keep a pride for more than a few months, but in Zambia an old male was resident within a pride for years. Yamazaki (1996) suggests th is was because there just were no t any younger males in the area to challenge him. Males esta Kalahari Desert lions with males roaming between prides. Lionesses accepted any male since it was rare for a pride to have a resident male. This abnormal behaviour wa s the result of overhunting and its continuation leads to inbreeding, frequent male eviction resulting in increased infanticide, and pride disruption. Lions are able to modify their
25 behaviour according to their environment, this social plasticity could be seen as an indicator of higher cognition. explored. Lions are frequently reintroduced into new game reserves. Killian and Bothma (2003) carried out a study on the social be haviour and dynamics of reintroduced lions. The lio ns used for a reintroduction were subadults that we re captured from multiple prid es who we re then placed in a smaller area within the game reserve for a few months to bond into a new pride. These lions we r e subjected to a huge social disruption in their lives wherein they must adapt to the loss of their natal pride and form a new pride from unrelated members. These forced new prides are socially unstable. Socially unstable prides experience more territory m ovement and greater mortality. Killian and Bothma (2003) found that the bond that had formed between the reintroduced lions was temporary. The pride that had formed while in the smaller area disintegrated when released into the game reserve. It was incredi bly unstable with one lioness becoming solitary for a few months before another lioness broke off from the main pride to join her. The remaining lioness then became nomadic. The two males broke off their coalition, with one joining the two lionesses and th e other with the nomad. Here we can see not only the social plasticity of lions but also the consequences of social disturbance. L ion C oalitions When subadult males are expelled from their natal pride they live as nomads. During this nomadic time they form coalitions with other subadult males. Coalitions can range from 2 9 lions with dyads or triads being most common. Larger coalitions are more successful with longer tenures (Mosser & Packer, 2009). It has been hypothesized that
26 lions are sensitive to n umerical advantages and that is why males form coalitions. When males form a coalition they stay in that coalition till one of the members die, and like dolphins (Connor et al., 2000; Wells, 2003) they do not then form a new coalition. In socially unstable populations where males are over hunted it has been observed in one lion that after the death of his coalition member he accepted a new coalition of two young male should join a coalition of males and reach a large size as possible, and then unston et al., 1998). Competing coalitions will fight viciously over a pride, a fight to the death is not uncommon. Members of the same coalition will compete among themselves over receptive females but never seriously wound each other, their fights consist mainly of swats to the face (West et al., 2006) and displays. Coalition members must cooperate in order to protect their p ride. Coalitions are based on mutualism; cooperation is not conditional on either kinship or on the behaviour of companions (Grinnell, Packer, & Pusey, 1995). Coalitions may be made up of related or unrelated individuals (Spong & Creel, 2004). Smaller coal itions are composed of unrelated individuals while in the larger ones all individuals are closely related (Grinnell et al., 1995). Grinnell carried out a study that investigated cooperation in coalitions and came to the conclusion that coalitions operate through mutual cooperation. Using playback experiments he measured the speed at which males appro ached a speaker that broadcast unfamiliar males roaring, the extent coalition males monitored each ot her during approach, and the distance they spread out duri ng approach. Neither the relatedness between members nor the behaviour of companions affected their behaviour When the
27 behaviour even if the companion was a laggard. In dense brush, whe n a companion could easily defect, the males did not monitor each other either. This shows that their cooperation is based on mutualism. If a coalition member defected during an inter coalition encounter, he would not only endanger his companion, but also himself and his pride. This study also proved that lions have a concept of numerosity. Coalitions will assess the number of intruders a judgment based on the number diff erence. When they are outnumbered they will approach the intruders more slowly. P ride S ubgroups Lionesses form subgroups within their pride. Mothers with offspring will associate with each other more frequently than with non mothers (Mosser & Packer, 200 9). Non mothers usually form their own subgroup within the pride. Some lionesses are solitary and do not often associate with other pride members. This type of fission fusion is also seen in the highly cognitive dolphin (Connor et al., 2000; Wells, 2003) w here pods are divided i nto mother, non mother, and solitary sponge carrier subgroups Larger prides have better quality territories, decreased rates of infanticide, and decreased mortality. Lionesses from large prides are more often part of a subgroup and because of this had greater hunting success and were caught in risky situations less often. A risky situation would be an instance where a lioness was alone on the edge of her prides & males and her risk of hyenas stealing her kill is greater. Thus it is advantageous not to be alone.
28 There are many theories for why lionesses form prides. One is that they must cooperatively defend a territory in order to protect their cubs from infanticide and procure instead of dispersing and why a territory will stay with a pride for generations. Another is that females form prides in order to protect themselv es from attack by conspecifics (Heinsohn & Packer, 1995). Inter pride aggression is the leading cause of lion mortality after humans. I believe the best explanation is a combination of these theories, where lion sociality evolved from a need to defend a pr ey rich territory against infantcidal males and neighboring prides who would jeopardize the rearing of their cubs to adulthood. Prides use complex cooperative strategies in order to defend their territory (Heinsohn & Packer, 1995). When confronted with th e roars of a neighboring pride some lionesses will lead the attack while others lag behind. The leaders recognize the laggards and laggards will change their behaviour depending on the odds. Within prides there is no social hierarchy, no female ranks above another and size does not indicate dominance. Thus laggards are not necessarily smaller or bigger than leaders. Whether a lioness is a leader or laggard is not dependent on what her mother is. Being a laggard during an inter pride con frontation has no cor relation with the level of hunt participation. Leaders take a bigger risk than laggards and this risk is increased by the distance the laggard lags behind. Lionesses that consistently lag behind are recognized as laggards. When a leader is paired with a la ggard she will approach more slowly and monitor her lagging suggests that they have the cognitive ability to implement score Packer, 1995). Even though lea ders recognize laggards they do not punish them, this
29 shows that prides are mutually cooperative. Laggards may benefit temporally by not getting injured in a fight but their overall success is dependent upon the whole pride. If they lag too far behind and one of their pride mates is killed, the whole pride is at a disadvantage. During confrontations lionesses form different subgroups; unconditional leaders, unconditional laggards, conditional cooperators, and conditional laggards. Unconditional leaders alw ays lead the attack, regardless of the odds. Unconditional laggards always lag behind. Conditional cooperators are laggards who will join the leaders when they are most needed (when they are outnumbered). Conditional laggards lag even farther behind when t he odds are against them. This behaviour bold personality types are more likely to lead while lionesses with shy personality types are more likely to lag behind. There have been no studies done on wild lion personality, however, the behaviour al data points towards the strong probability that lions have distinct personalities. An indicator of personality in animals is that their behaviour is constant over time and across situations. Lionesses develop the tendency to either lead or lag as juveniles (Heinsohn, Packer, & Pusey, 1996). When the adults move to confront an invading pride the juveniles follow behind the adults. The positions in which the juveniles arrange themselves mirrors that of the adults with some juveniles lagging behind others. These leading and lagging positions are non random and are consist from the time they first participate through adulthood. Juveniles also have a concept of numerosity. They can assess the numbe r of pride mates against intruders and make a judgment according to the odds (Heinsohn et al., 1996).
30 More evidence for personality in lions is found when looking at hunting behaviour Lionesses will consistently occupy the same roles during a hunt (Stan der, 1992). Certain lionesses always occupy the center position, while others always occupy the wing position. Center lionesses stalk a short distance then lie watching the prey and other lionesses move into position. The wing lionesses stalk further aroun d back of the prey and chase it into the ambush of the centers. Lionesses in some prides will change their preferred hunting position according to the presence, absence, or position of a pride mate. This suggests individual variability. This also provides some evidence for joi nt attention. Griffin ( 1984) has theorized that lions take conscious advantage of the positions of pride mates and coordinate their stalking patterns. Lionesses cooperatively hunt prey by a division of labor with the wings chasing the prey into the centers ambush position. When lionesses hunt in their preferred position the chance of the hunt being successful is increased. D ispersal of O ffspring & N ew P ride F ormation All species that live in a group have dispersal of offspring. This e nsures that the group does not grow too large for its territory to support it and inbreeding does not occur Subadult male lions disperse at about two years of age. Subadult females will stay with their natal pride for life. There are five circumstances in which subadult females will disperse and form their own pride (VanderWaal, Mosser, & Packer, 2009). First is when the pride is too large. There is a habitat specific threshold for dispersal. When intra pride competition is too high about half of the subad ult females will disperse to form their own pride. Lionesses are sensitive to the pride size of their neighbors and are less likely to disperse when surrounded by many unrelated neighbors. Second is when subadult females too young to breed are evicted by a n incoming male coalition. The subadults are
31 old enough to escape infanticide and are forced to form their own pride. Third is when mothers of young cubs disperse during a takeover in order to avoid the infanticide of her cubs. In this case her sudadult da ughters are old enough to breed and they and the new coalition form a pride (Hanby & Bygott, 1987). Fourth is when non mother and mother subgroups fission into separate prides. Lions live in a fission fusion society and sometimes a pride will fission perma nently forming two new prides. The fifth among the pride. I nter P ride I nteractio ns Inter pride interactions are a core aspect of lion sociality. The more closely related a pride is to its neighbor the more tolerant it is, resulting in le s s aggression and more shared territory (Spong & Creel, 2004; VanderWaal et al., 2009). Unrelated p rides fight over territory. One of the greatest causes of lion mortality is inter pride aggres sion. It is suggested that male s will kill females of another pride in order to tip the balance in favor of their own females (Mosser & Packer, 2009). Lions are s ensitive to numerical advantages in inter pride confrontations (Spong & Creel, 2004). A smaller subgroup will not approach a larger trespassing group until they have recruited more pride mates. This suggests that lionesses asses the odds of a fight in rela tion to the pride mates she is currently with and the pride mates she is recruiting. This is especially interesting considering certain lionesses are leaders and laggards. A lioness may then, besides assessing numerical differences, asses her relative prid e strength depending on if her current companions are leaders or laggards.
32 When lionesses are confronted with intruders near a territory boundary they approach slower. This may be because the intruders are closer to their territory and thus could recruit from their pride more easily This would tip the balance against the lionesses and influence their assessment. Females are more likely to roar when the odds are against them and McComb suggests that roaring is an attempt to recruit (McComb, Packer, & Pusey 1994). Response to intruders is influenced by social factors. Lion sociality may have influenced Panthera leo numerical assessment. C ommunication Lion s must be able to communicate with each other to facilitate group living. Roaring is the most iconic symbol of the lion. Of all the felines lions have the loudest roar. A roar is low pitched and delivered in bouts lasting 30 60 seconds (Grinnell & McComb, 2001). Roars begin with a few moans which progre ss to loud roars and end in a series of grunts. Lions are largely nocturnal thus roaring is an efficient means to communicate with vocalization is used to advertize territory maintain contact with cohorts, and attract mates. Lions are especially sensitive to the effects of listeners. Since males and females advertize their territory by roaring a roar can be seen as a serious threat. Nomadic male coalitions never roar, even wh en the members become separated. This is because roaring would advertize their location to resident males who would aggressively respond. Roaring while in the territory of another male will invite an attack from the resident male (Grinnell & McComb, 2001) Whenever resident males hear an unfamiliar male roar they quickly approach with intent to kill. If a resident male is not within his territory he will not approach. This indicates that males roar when they are resident with a pride and are
33 on their pride my coalitions will ro that roaring is a flexible behaviour that signalers may adjust according to the 2001). Lions are a ble to identify individuals on the basis of their roars (McC omb, Pusey, Packer, & Jon Grinnell, 1993). Lionesses with cubs are able to distinguish between the roars of their resident males and those of unfamiliar males. Cubs may also be able to make this d or were responding to the behaviour s of their mothers. When lionesses and cubs hear the roar of their resident male they remain calm and are undisturbed. When they hear the roar of an unfamiliar roar they become agitated. If the cubs are at least four and a half months old the pride will rapidly retreat, if the cubs are younger the pride will stand its ground and fight off the intruding male. Lionesses can also distinguish b etween the roars of their pride mates and those of unfamiliar females. Upon hearing the roars of unfamiliar females from a different pride the pride will approach the location. Cubs follow their mothers and if they are old enough will participate in terri torial defense (Heinsohn et al., 1996). Lionesses will defensively move towards cubs in response to unfamiliar male roars but do not when they hear the roars of their resident males or the roars of unfamiliar females. By distinguishing between roars a lion ess is able to make a decision between fight or flight.
34 Lions also have a vast repertoire of other sounds, such as grunts, moans, oows, snarls, and intensity. Li ons also use scent as a mode of communication. Lions extensively scent mark their territory. Scent also alerts cohorts to reproductive status. Lions use the Flehming response to gain information about pheromones Socialization among pride mates is overwhe lmingly tactile. Body language is highly developed and expressive. One of the strongest social behaviour s is head rubbing and licking. Lions will rub their head against another lion and engage in face licking after feeding, a fight, long separation, and in almost any other social context. Head rubbing and licking can be compared with primate grooming. Males will rub and lick their coalition partners to reassert their bond. Females rub and lick their pride mates and cubs constantly. Head rubbing and face lic king is so important to lion sociality that it influences mortality. Ousted males often die from infection of seemingly minor wounds to the head, presumably because they do not have a coalition partner or pride mate to lick and clean it (West et al., 2006) Lions have not been studied with respect to their cognition as much as dolphins or bono bos, however, examination of behaviour al evidence will reveal many similarities between lions and these highly cognitive species. By reviewing multiple behaviour al ar ticles I have come to the conclusion that lions have a degr ee of cognition higher than that which is curren tly attributed to them Through this research I see evidence for the possibility of numerosity, joint attention, recognition of the individual, compl ex communication systems, and the ability to make judgments according to the situation at
35 hand. I believe the potential for significant cognitive studies is there someone (hopefully me) just has to look for it! This evidence for a higher level of cognitio n is essential for creating an optimal captive environments for lions. In order for a captive population to be succ essful biological and behaviour al needs must be met. Modern larger enclosures ensure that they have enough space to ex ercise but frequently ignore behaviour al needs. It is rare to see an intact pride in captivity. Most offspring are whisked away to other institutions because of space issues. Thus a proper pride of r elated females can never form. Worse the offspring are frequent ly paired with unrelated individuals and forced to cohabitate. The bonds between unrelated individuals are transient as has been shown with populations of reintroduc ed lions (Hayward, 2007a; Kilian, P.J. Bothma, J. du P., 2003; Trinkel, 2008) In captivity with no oppor tunity to disperse this leads to extreme aggression. Zoos frequently must separate lions into on and off exhibit shi fts to prevent them from injuring each other. A female may not accept a male for breeding because she has no pride to help in the rearing o f her offspring. Cubs are frequently hand reared and denied the opportunity to learn from their mother. They never learn how to be a lion and thus do not act appropriately when introduced to other lions. C aptive habitats need to provide for the behaviour al repertoire of lions, which means they must allow for natural prides to form. Game p Wild Animal Park is an example of captive habitat that has allowed the formation of naturalistic prides. Instead of remov ing offspring in captive habitats males should be rotated among institutions mimicking the takeovers of coal i tions in the wild. When pride size is too large to sustain, the pride should be split naturalistically with young non mothers forming a new pride.
36 Hunting is another huge part of lion behaviour which captive environments do not adequately provide. Numerous enrichment techniques that stimulate hunting and foraging behaviour s can improve habitat quality (M arkowitz, Aday, & Gavazzi, 1995. Jenny, S & Sc hmid, H. 2002., Law, G. et al. 1997. Mellen, J. & She pherdson, D. 1997. Wooster, D. 1 997. Bashaw, M. et al. 2003. McPh ee, M. 2002. Shepherdson, D. 2003. ) Law et al. have d eveloped multiple feeding techniques which stimulate stalking and chasing behaviour s such as the feeding pole (Law, G. et al. 1997 ) Caching food effectively stimulates foraging ( Wooster, D. 1997. ) Feeding of whole prey stimulates natural feeding behaviour s as well as proper skeletal growth ( McPhee, M. 2002. ) The release of live prey in to the habitat is a great form of enrichment (as long as no injury comes to the predator and the prey is not subjected to undue suffering) This can be done either off exhibit or after hours in order not to offend more sensitive members of the public. Howe ver it could be done as part of an educat ional program that would effectively illustrate the hunting prowess of the lion (see hunting techniques previously mentioned). It has been shown that the feeding of live prey to carnivores has mixed support In Swit zerland and the UK the on exhibit feeding of live prey was not supported but the feeding live prey off exhibit was (Cottle,L. et al. 2010 Ings, R. 1997 ) In the United States zoo visitors suppor ted the feeding of live prey on exhibit (McDole, E. 2007) Wh ile zoos must cater to the sensitivities of visitors privat e sanctuaries and parks have greater freedom to feed live prey to carnivores as enrichment without criticism.
37 The Captive Environment Humans have been keeping wild animals in captivity for aroun d 5 ,0 00 years. T he initial purpose has changed from a show of power and wealth, to entertainment, to the current goal of species preservation. There are many types of facilities that keep wild animals in captivity and each has different goals and missions. Because of these differences there is a great deal of infighting among facilities. They all have the same basic goal : to keep wild felines healthy in captivity for future generations. In order to ensure a future for endangered felines they need to work to gether and share resources. Zoos and breeding centers conduct valuable research and uphold pr udent breeding criteria. Rescue facilities and sanctuaries allow for larger numbers of species to be supported and can act as genetic reservoirs for conservation b reeding programs. Parks and reserves protect wild populations and provide for research opportunities into naturalistic conditions in captivity. Improvements to the captive environment must be ongoing and focus on providing the best husbandry possible. Unde rstanding species biology and behaviour is an ongoing process. Ideas on proper dietary requirements, veterinary care, husbandry practice, and enrichment techniques are constantly changing and evolving. Enrichment is the most exciting development to happen in the animal care field in the last 4 0 years. Endles s opportunities to enhance the lives of captive wildlife abound re quiring insight and creativity. Enrichment The AZA (American Zoo & Aquarium Association) developed a working definition of enrichment in enrichment is a process for improving or enhancing zoo animal environments and care
38 behaviour (Shepherdson, 2003) Technique s can be loosely divided into three categories. Feeding, of which some examples are carcass feeding, foraging, puzzles, and training. Habitat, which can incorporate plants, levels, complexity, and activity. Social, where the presence or absence of conspec ifics or other species influences behaviour A good enrichment technique should incorporate at least two categories but that does no t mean it needs to be complicated.
39 Figure 5 : Tiger using feeding pole enrichment as invented by Law ( 1997). Taken from ( M alpass Oz A dventure 2011) Law et al (1997) have invented some incredible techniques. The feeding pole, illustrated in Figure 4, is an effective enrichment both behaviour ally and physically. Big cats use a short powerful burst o f energy when they hunt and bring down prey. The feeding pole consists of a telephone pole that has a peg at the top where a large chunk of meat can be hung. The tiger must run up the pole, grab the meat, and climb back down.
40 This enrichment incites hunti ng behaviour s that frequently are not expressed in captivity such as stalking, running, leaping, are climbing. For small felids a swing pole feeder can elecit similar hunting behaviour s. Habitats for smaller felids are often fully enclosed, thus a terra co tta plant pot can be attached to the roof with small pieces of meat put inside. In order to get the meat the feline must climb a branch close to the pot and stick its paw behaviour expressed b y smaller felids (Leyhausen, 1979) These enrichment techniques not only stimulate hunting behaviour s but provide opportunities for the cats to express great bursts of activity and energy. Keeping captive predators active is important in managing their wei ght. Often if a cat is too heavy its fecundity is very low. Odors are commonly used as enrichment because they are easy to administer. Different odors can elecit different behaviour s. Shuangying (2008 ) provided Amur leopards with three different odors whi ch stimulated different responses. Odors of prey species, sympatric carnivores, and spices are effective. Felines respond to a multitude of spices as they do to catnip rubbing and rolling on the scented object and exhibiting increased marking behaviour s. (Markowitz, Aday, & Gavazzi, 1995) Even older animals who have lived in relatively stimulus free habitats who seem unresponsive can be brought to greater activity levels and behaviour al repertoires through these techniques. Frequently abnormal negative behaviour s such as stereotypical pacing can be reduced by providing enrichment (Jenny & Schmid, 2002) The feeding of intact carcasses and presentation of live fish are proven to reduce stereotypic pacing (Ba shaw, 2003; McPhee, 2002)
41 Habitat complexity is another way to improve a captive animals welfare (Law, 1997) Concrete flooring is now considered less hygienic and has a higher incidence of paw and joint injuries. Natural substrates are now preferred and allow for behaviour s such as digging and scratch marking. Plantings not only look appealing to zoo visitors they provide cover and shade. More cryptic species need many places to hide and providing natural vegetation provides security. Most felids are agi le climbers thus the vertical space in an enclosure should be utilized as much as possible. L arge and complex artificial tree s can give arboreal species a more natural setting. In most zoos male female pairs are kept in the same exhibit because of public d esire to see them side by side and lower costs of building and maintaining a single enclosure. However, this forced pa i ring goes against the felid solitary social system. As a result many pairs lose interest in breeding which may only be revived if separat ed for a period (Law, 1997) However, some species can be kept in social groups. Tigers kept in groups exhibit less stereotypical behaviour s than those kept isolated (Jenny & Schmid, 2002; A. Miller & Kuhar, 2008; L. J. Miller, Bettinger, & Mellen, 2008) In order to assess the e nvironmental enrichment needs of a species, it is necessary to determine its natural history and behaviour al biology
42 Case Study Felines are one of the most complex and specialized mammals. They have always held a mystery and fas cination to humans. Due to habitat destruction and relentless hunting the future of wild felines is in the hands of humans in captive environments. In order to ensure a future for these fascinating animals we must learn all we can about them in order to p rovide an optimal habitat. It was the goal of this study to observe space usage and activity budget of two species P. leo krugeri and P. pardus oreintalis With the s e data we can further improve captive environments thus ensuring the future of the amazing cats. Previous work on activity budget and space usage of wild cats in captivity influenced my study design (A. Mallapur, Qureshi, & Chellam, 2002; A. Mallapur, 2002; Pitsko, 2003) Charismatic megafauna are species that are generally large, flashy, and popular with the public which conservationists use to garner support (Barney, E et al. 2005). Species such as pandas, polar bears, and tigers are popular in captivity because of the physical appeal they bring to visitors. Lions have long been a staple in z oos. The male lion is an impressive sight alongside a pride of lionesses. Another essential from the cat These Panthera species rank as charismatic megafauna and are com mon in captivity as a crowd pleaser and ambassadors for conservation of their natural habitats. Lions and leopards are the center point of this thesis and case study because of their popularity and status. These species are important tools for education an d as a result deserve the best care possible. While humans have been keeping exotic animals in captivity for 5,000 years (Kisling, V. 2001) it is not until recently that much research had been devoted to
43 good husbandry. By better understanding the idiosy ncrasies of these species human caregivers can provide an optimal captive environment. Methods Subjects Two species of Panthera served as subjects, Transvaal lions P. leo krugeri (n=4 2.2.0 ) and Amur leopards P. pardus or ie ntalis (n=2 1.1.0 ) for a total of six subjects Both species were fed six days a week with one day being a fast day. Water was available ad libitum. The lions and leopards were housed in habitats that consisted of on and off exhibit enclosures. The on exhibit enclosures were larger, l andscaped, and allow for public viewing of the animals. The off exhibit enclosures were secure kennels w h ere the animals were kept at night or when not available for public viewing. The lion on exhibit enclosure was a rectangular shape of about one acre, b ordered on two sides by a moat, on one side a small pond and viewing areas, the off exhibit enclosure in the back, a hill with a cave in the center, and was scattered wi th multiple large oaks. The off had one large kennel on one side and four smaller kennels on the other, and two covered outdoor runs were accessible via the smaller kennels (see Figure 6 ).
44 Figure 6 : Lion enclosure map with location designations. H=hill, S=sout h, E=east, N=north, W=west. The leopard on exhibit enclosure was a rectangular shape about a quarter acre totally enclosed, with a large complex artificial tree in the center, scattered plants throughout, and was covered in vines which shaded almost the w hole area. The off smaller kennels (see Figure 7 ). The female had exclusive access to the larger kennel
45 Figure 7 : Leopard enclosure map with location designations. C=center, S=south, E=east, N=north, W=west. The lion pride consisted of two females, Tamu and Laini, and two males, Mshoni and Catali. Tamu and Laini were littermates who came from the San Diego Zoo and were born in November 2007 Catali came from the St. Louis Zoo and was born in December 2005. T he oldest lion born in August 1995, was Mshoni who was from the San Diego Zoo as well. He is the only hand reared cat in the collection The researcher was a ble to readily distinguish between the males as Mshoni had a very large and dark mane only. The sisters were harder to distinguish. Tamu had a scar on her right hip and had more scars around her face, she was also slightly heavier than Laini (see Figure 8 )
46 Figure 8 : Laini (top) and Tamu (bottom) sister lions. Taken by author at Jacksonville Zoo.
47 The lions were put out on exhibit in three diffe rent compatible groups 1 The first group consisted of Tamu and Mshoni who formed a breeding pair and had access to the exhibit whenever she was in heat. The second group consisted of Laini and Ca tali who formed a non breeding pair Lastly, Tamu and Laini f ormed a sister group. The sister group was rarely on exhibit, thus the researcher rarely had to distinguish between the two females. One of the male female pair s was usually on exhibit. The remaining two lio ns not on exhibit were kept off exhibit in the ke nnels but usually had visual contact with the on exhibit lions. The leopard group consisted of one female, Makarii, and one male, Nikolai. They both came from the Lincoln Park Zoo; Makarii was born in 2000 and Nikolai was born in 2001 Makarii was iden tifiable by her rotundness despite her smaller stature, she had a round head and a shorter tail. Nikolai was leaner and taller with a square head and long tail (see Figure 9 ) The two leopards were always on exhibit together during operating hours, with ea ch having sole access during the night on alternating days (while the other was kept off exhibit for the night ) 1 Originally Catali, Tamu, and Laini formed a small pride but aggression between Catali and Tamu resulted in her removal and subsequent pairing with Mshoni (who had been alone after the death of his brother).
48 Figure 9 : Top picture: Nikolai (top) on center tree & Makarii (bottom) in center. Bottom picture: Makarii (left) & Nikolai (right) on center tree.
49 Materials Materi als included a kitchen timer, all weather notebook brand) and writing utensils used to record data. A computer with Microsoft Excel and Statistical Analysis S oftware was used to an alyze data. Procedure An ethogram was created for each species from ad libitum observations totaling three hours per species (see Appendix page 74 & 76 ). Thirty five behaviour s were recorded coded, and categorized (see Appendix page 78 & 79 ) On exhibit enclosures where divided into five locations Observations were made using the focal animal (Altmann, J. 1 9 74 ) continuous sampling methods (Lehner, 2007) Five minute intervals of continuous sampling were done in three hour sessio ns once a day, five days a week for two months totaling 120 hours. A session was held in the morning (09:00 12:00) or afternoon (14:00 17:00). Night ti m e observations were not possible for this study. For each species approximately 20 sessions were conducted with 10 sessions per sex, with five morning and five afternoon sessions. This resulted in 30 hours of observation per species sex (i e. leopard male). Sessions were assigned randomly and inter observer reliability was tested and found to be in high agreement (98%) Observat ions focused on space usage and activity budget. Proximity while resting was also noted since it has been linked to affili a tive behaviour s (Miller & Kuhar, 2008) Data were recorded on site in an all weather notebook and later input into an Excel spreadshe et for analysis.
50 Data analysis Data were broken down a nd analyzed with regard to frequencies of : 1. Behaviour categories 2. Proximity while resting 3. Individual behaviour 4. Location 5. Behaviour s by location. It was decided to analyze the data in terms of frequencie s of occurrence (Paterson, J. 2001) where each novel behaviour that occurred in a novel location was counted once per interval. Results 1. Results showed that both leopards and lions exhibit ed activity behaviour s (highlighted in yellow) most frequently follo wed by resting behaviour s (in green). Table 1 Behaviour Category Frequencies by Species Behaviour Category Species Resting Activity Stereotypy Breeding P.P ardus 793 1094 187 0 P. leo 949 1101 51 63 Total 1742 2195 238 63 Note. See page XX of Appendix for Behaviour Category information.
51 There was a significant difference between sexes n =4,175, with females exhibiting resting behaviour s (in yellow) most frequently while males exhibited activity behaviour s (in green) most frequently as shown in Table 2 Table 2 Behaviour Category Frequencies Beha viour Category Species Sex Resting Activity Stereotypy Breeding P. pardus Female 477 394 28 0 Male 316 700 159 0 P. leo Female 551 510 36 40 Male 398 591 15 23 Note. See page XX of Appendix for Behaviour Category information. Figure 10 illustrates behaviour category frequencies graphically showing activity as the most frequently exhibited behaviour followed by resting.
52 Figure 10 : Graph illustrating behaviour category frequ e ncies across species a nd sexes Notice activity is the most frequent behaviour followed by resting, stereotypy, and breeding. 2. Proximity while resting was significantly different between species p,.0001, n =1,400, with leopards resting far from each other most fr equently and lions resting near to each other most frequently (in yellow, in Table 3) Figure 12 illustrates the species comparison of proximity while resting frequencies Table 3 Proximity while Resting Frequencies Species P.pardus P. leo Proximity Female Male Total Female Male Total Far 360 234 594 117 215 332 Near 26 12 38 297 139 436 Note. Proximity was determined as follows: Far = B1 + B3; Near = B2 + B4. See page X X of Appendix for behaviour code in f ormation.
53 Figure 11 : Graph showing species comparison of proximity while resting frequencies. P. pardus was observed resting far most frequently while P. leo was observed resting near most frequently. 1. With lions a differen ce between sexes was observed with females resting near and male resting far most frequently ( in green, in Table 3) Figure 13 illustrates the difference between sexes in lions for proximity while resting frequencies
54 Figure 12 : Proximity while Resting Frequencies for P. leo There is a difference between the sexes with females resting near and males resting far most frequently. 2. The female leopard exhibited the Resting Head Erect Far behaviour most frequently while the male leopa rd exhibited Walk behaviour most frequently ( in yellow, in Table 4 ). The female lions exhibited the Resting Head Erect Near behaviour while the male lions exhibited the Resting Head Erect Far behaviour most frequently ( in green, in Table 4 ) Figure 15 i llustrates the behaviours most frequently observed across all species and sexes. Table 4 Individual Behaviour Frequencies Species P. pardus P. leo Behaviour Female Male Female Male B1 190 147 90 167 B2 14 4 215 100 B3 170 87 27 48
55 B4 12 8 82 39 B5 63 54 74 13 B6 28 16 63 31 B7 60 117 96 115 B8 23 16 46 42 B9 6 3 12 9 B10 15 2 5 0 B11 113 235 184 148 B12 12 18 6 8 B13 7 34 4 6 B14 2 1 0 2 B15 3 3 3 0 B16 0 1 2 3 B17 2 6 17 13 B18 5 3 10 20 B1 9 1 3 0 2 B20 22 27 4 3 B21 9 9 9 25 B22 4 0 0 3 B23 0 24 2 9 B24 14 27 4 24 B25 2 3 3 1 B26 1 0 1 2 B27 51 32 43 29 B28 2 5 3 5 B29 12 1 10 10 B30 19 39 25 46 B31 3 77 1 37 B32 5 7 19 15 B33 1 7 1 14 B34 28 159 36 15 B35 0 0 40 23 Note. See page XX of Appendix for behaviour code information.
Figure 13 : Individual Behaviour Frequencies across all species and sexes. For leopards, the female exhibited B1 most frequently and the male exhibited B11. For lions, the female exhibited B2 most frequently and the male exhibited B2.
The species comparison of individual behaviour showed that both leopards and lions exhibited the walk behaviour most frequently ( in yellow, in Table 5). Figure 16 illustr ates the behaviours most frequently observed across species. Table 5 Species Comparison of Individual Behaviour Frequencies Species Behaviour P pardus P. leo B1 337 257 B2 18 315 B3 257 75 B4 20 121 B5 117 87 B6 44 94 B7 177 211 B8 39 88 B9 9 21 B10 17 5 B11 348 332 B12 30 14 B13 41 10 B14 3 2 B15 6 3 B16 1 5 B17 8 30 B18 8 30 B19 4 2 B20 49 7 B21 18 34 B22 4 3 B23 24 11 B24 41 28 B25 5 4 B26 1 3 B27 54 72 B28 7 8
58 B29 13 20 B30 58 71 B31 80 38 B32 12 34 B33 8 15 B34 187 51 B35 0 63 Note. See pag e XX of Appendix for behaviour code information.
Figure 14 : Species Comparison of Individual Behaviour Frequencies Both leopard s and lions exhi bited the walk behaviour most frequently.
3. n= 980. The fe male leopard occupied the south area of their habitat w hile the male occupied the center area most frequently ( in yellow in Table 6). Figure 17 illustrates the location frequencies of leopards. Table 6 Location F requencies Location Species Sex C enter E ast N orth S outh W est P. Pardus Female 109 68 42 142 44 Male 208 29 176 100 62 Location Species Sex H ill E ast N orth S outh W est P. leo Female 228 18 21 108 27 Male 110 19 19 197 13 Note.
61 Figure 15 : Graph illustrating location frequencies of leopards. The female occupied the s outh area most frequently, while the male occupied the center area. Note that C=center, E=east, N=north, S=south, & W=west. n= 760. T he female lions occupied the hill area of thei r habitat most frequently while the male lions occupied the south area ( in green, in Table 6) Figure 18 illustrates the location frequencies of lions.
62 Figure 16 : Graph illustrating location frequencies of lions. The female occup ied the hill area most frequently, while the male occupied the south area. Note that H=hill, E=east, N=north, S=south, & W=west. 4. Leopards most frequently exhibited resting and activity behaviour s in the center and exhibited stereotypical behaviour in the north area of their habitat (no breeding behaviour was observed) ( in yellow, in Table 7) Lions most frequently exhibited resting behaviour s in the hill area and exhibited activity, stereotypical and breeding behaviour s in the south area of their habitat ( in green, in Table 7). Table 7 Species Comparison of Behaviour s by Location Frequencies Behaviour Category Species Location Resting Activity Stereotypy Breeding P. pardus C enter 322 363 1 0 E ast 94 90 0 0 N orth 71 216 163 0 S outh 2 52 306 23 0 W est 54 119 0 0
63 P. leo H ill 527 283 0 14 E ast 19 73 0 3 N orth 25 91 0 7 S outh 340 556 51 37 W est 38 98 0 2 Note. See page XX of Appendix for Behaviour Category information. The female leopard exhibited resting, activity and stereotypy behaviour s most frequently in the south area ( in yellow, in Table 8). The male leopard exhibited resting and activity behaviour s in the center area with stereotypical behaviour s exhibited most frequently in the north area ( also in yellow, in Table 8). The female lions exhibited resting behaviour s in the hill area and activity, stereotypy, and breeding behaviour s in the south area most frequently ( in green, in Table 8 ). The male lions exhibited resting, activity, stereotypy, and breeding be haviour s in the south area most frequently ( also in green, in Table 8). Table 8 Behaviour s by Location Frequencies Behaviour Category Species Sex Location Resting Activity Stereotypy Breeding P pardus Female C enter 119 77 0 0 E ast 89 50 0 0 N orth 51 45 6 0 S outh 177 181 22 0 W est 41 41 0 0
64 Male C enter 203 286 1 0 E ast 5 40 0 0 N orth 20 171 157 0 S outh 75 125 1 0 W est 13 78 0 0 P. leo Female H ill 376 185 0 14 E ast 14 29 0 2 N orth 14 45 0 4 S outh 116 187 36 18 W est 31 64 0 2 Male H ill 151 98 0 0 E ast 5 44 0 1 N orth 11 46 0 3 S outh 224 369 15 19 W est 7 34 0 0 Note. See page XX of Appendix for Behaviour Category information. For leopards, t he most frequent behaviour that occurred in the center, north, south and west areas was activity while the east area was resting behaviour s (Table 7). Figure 19 illustrates leopard behaviours by location frequencies. For lions, t he most frequent behavi our that occurred in the hill area was resting, while the east, north, south, and west areas were activity behaviour s (Table 7). Figure 20 illustrates lion behaviours by location frequencies.
65 Figure 17 : Graph showing leopard beh aviour s by location frequencies. Notice that in the center, north, east, and west the most common behaviours are activity; while in the east the most common was resting. Note that C=center, E=east, N=north, S=south, & W=west. Figure 18 : Graph showing lion behaviour s by location frequencies. Notice that the most frequent behaviour that occurred in the hill area was resting; while in the east, n orth, south, and west areas activity behaviour s were most common. Note that H=hill, E=e ast, N=north, S=south, & W=west.
66 Dis cussion A significant difference was found between proximity while resting and species. Leopards rested far from each other while lions rested near. This fits in with previous research supporting the behavioural pref erences among conspecifics of these species. Leopards are solitary in the wild thus the subjects in this study were exhibiting naturalistic behaviour by resting far from each other Lions are the only truly social felid; in the wild conspecifics frequently rest in close proximity to each other in large groups. The data from the case study show that the captive lion subjects are exhibiting naturalistic behaviours as well. Interestingly there was a difference between the sexes in lions with regard to proxim ity while resting. The male lions were found to rest far, while the females rested near most frequently. This may be explained in terms of the pair groups of the lions when on exhibit. The observer noticed that sister pair preferentially rested near each o ther almost all the time, thus this may have affected the high incidence of female lions resting near. A factor that may explain the reason the males rested far most frequently also derives from the pair groups. In the breeding pair group the male lion Ms honi, was much older than the female Tamu, he was paired with T he observer noted that the female often attempted to initiate play, which was rebuffed by the old male who would walk away and rest far from her The non breeding pair which consisted of the other sister, Laini, and the young male, Catali, also encountered this scenario. Laini would often attempt to initiate play with Catali he would respond by moving far away from her. When the sister pair group was on exhibit they often played together befo re and after resting near each other. This leads one to ask, why would the males avoid play
67 behaviour? The researcher assumes that the extremely hot weather influenced the heavily maned males to avoid unnecessary exertion. In the case of the old male, Msho ni, avoidance of play behaviour may have also been age related. In the wild lion sisters are very closely bonded, thus the affiliative behaviours (resting near and play) between the females subjects studied supports previous research of species typical beh aviour. Contrary to what the researcher initially hypothesized the results show that both lions and leopards exhibited activity behaviours most frequently, followed by resting behaviours. These results support previous research that in the wild felines are quite active throughout a 24 hour cycle. In captivity predators are frequently under stimulated and thus exhibit a behaviour profile dominated by resting behaviours. A difference between the sexes was found with females exhibiting resting behaviours most frequently and males exhibiting activity behaviours most frequently. This may be explained in several ways. Unbeknownst to the researcher at the time of the study the female leopard, Makarii, was pregnant 2 Makarii may have exhibited disproportionally more resting behaviours due to her pregnancy (in the middle of summer) and her data may have skewed the overall female data in favor of resting behaviours. The male leopard, Nikolai, may also have skewed the overall male data in favor of activity behaviours be cause he spent the majority of his time pacing. One confound the researcher acknowledges that may have skewed the data in favor of activity behaviours is that activity behaviours consisted of both states and events, and both were counted with equal weight Duration of behaviours were also not recorded 2 Makarii gave birth to two cubs, a male and a female, on September 27, 2010. Unfortunately, the female cub died shortly after birth. The male cub was subsequently removed for hand rearing and is healthy and prospering!
68 s both were each counted as one. In future studies duration should be noted and taken into consideration during analysis to clear up this potential confound. The individual behaviour that was exhibited most frequently was analyzed to determine which behav iour each subject performed most often. The female leopard was the above speculations concerning her overall increase in resting behaviours due to her pregnancy. This also supports the species typical behaviour of wild leopards to remain high incidence of stereotypical pacing. The researcher postulates that this may be due to the speci es typical urge to patrol the boundaries of his territory. Wild leopard males can have large territories that overlap multiple females. They must patrol this territory in order to drive away other males and to assess the reproductive status of the females. most, while the most commonly. A probable hypothesis for why the lions exhibited resting behaviours mos t is that the study took place during the summer months and the heat caused the lions to avoid unnecessary activity. The researcher has already presented reasoning as to why there was a difference between the sexes in relation to proximity. the most frequently exhibited behaviour exhibited for both lions and leopards when the sexes were collapsed and species were compared.
69 The location that each subject was most frequently found in was assessed to determine space usage. The leopards were foun d to occupy different areas of their habitat. The female occupied the south area, while the male occupied the center area most frequently. This further supports the display of naturalistic behaviours in these captive leopards, as in the wild leopards are s olitary with males only associating receptive females for breeding. The researcher observed that the female leopard was defensive of her space within the enclosure and as a result the male avoided close proximity with her. uenced this behaviour as the keepers informed the researcher that previously the leopards often exhibited a ffiliative behaviours towards each other. Another reason the male may have preferred the center area is that it was the most complex area of the encl osure which allowed for many scent marking opportunities. The lions were also found to occupy different areas of their enclosure. The females occupied the hill and the males occupied the south area most frequently. The difference can be explained similarl y as to why the lions exhibited a difference in proximity while resting. The hill area is the preferred location in the lion habitat as it is elevated and shaded, thus providing a cool lookout point. The females dominated this preferred area; if the males wanted to avoid the play behaviours of the females they had to find a different area within the enclosure. Leopards most frequently exhibited resting and activity behaviours in the center area. This may be because this was the most complex area of their e nclosure, with a large artificial tree, and thus promoted activity behaviours like jumping and scent marking. The center area was a good area for resting because it was the most shaded area and was most likely the coolest place to escape the heat it also was the furthest area from the public
70 viewing areas and afforded the leopards some isolation from the public. Stereotypical pacing occurred most frequently in the north area of the enclosure and was exhibited almost exclusively by Nikolai the male leopard. Lions most frequently exhibited resting behaviours in the hill area this area was elevated and shaded thus providing an optimal cool vantage point. Activity, stereotypical, and breeding behaviours were most frequently exhibited in the south area of the enclosure. The researcher noted that besides the hill area the south was the second most shaded area of the enclosure. The lions preferred this area for exhibiting these behaviours because it provided a respite from the summer heat. Stereotypical pacing oc curred most would pace in front of the entrance in the presence of keepers before they were let into the kennels for the night. These results show that the subjects use d ifferent areas of their enclosures for different purposes. The s e data can be used by the Jacksonville Zoo and other institutions to improve their enclosures and husbandry practices. Each subject demonstrated a distinct activity budget and space usage prof ile. Further studies can determine how constant these animal in the collection. From there enclosures, husbandry practices, and enrichment techniques can be tailored t o the individual improving quality of life The San Diego Zoo while males preferred objects they could scent mark on. The male leopard, Nikolai, can provide an excelle nt research opportunity Now the Zoo knows definitively that he exhibits a high occurrence of stereotypical pacing behaviour and they can quantify
71 exactly how frequently he paces. In order to attempt to decrease this behaviour keepers or researchers can in stitute enrichment techniques to try to divert his behaviour towards more appropriate activities. Enrichment such as a cardboard box filled with hay and spices may encourage hunting behaviours such as stalking, running, pouncing, biting, scratching, etc. The efficacy of the newly instituted enrichment techniques can be gauged with further behavioural observations. The observations can then be compared with the results of this study to determine scientifically if Nikolai has exhibited a reduction in pacing. The improvement of captive habitat with regard to species biology and behaviour can decrease stereotypical behaviou rs and increase breeding success in captivity. Individual behaviour enr ichment techniques and husbandry practices in order to meet the needs of the individual in the captive environment. Observational information collected from well managed captive populations can increase our knowledge of feline behaviour which can benefit f ield researchers working with wild populations (Law, 1997). Behaviour al research on wild leopards is scarce but information about their species typical behavioural repertoire can be gained through studies of captive specimens. Considerable changes in the attitudes towards the keeping of wild animals in captivity have been made over the past 50 years. Concern for animal welfare has become widespread among cultures and affected the way institutions care for their animals (Kirkwood, 2003). Husbandry technique s are always improving as science progresses and new discoveries are made in animal behaviour Just a couple decades ago enrichment was seen as superfluous, now it is an integral part of proper management. Animal caregivers should
72 always be creating new te chniques and never become complacent about the welfare of the animals under their care. Wild populations are diminishing, soon for some species like the tiger, the only future they will have left is in captive environments in the care of humans. It is our responsibly to make those conditions the best possible. Education of the public through outreach programs can inspire people to take action in the conservation of wildlife. Education programs are especially effective when presented to young children who Environmental interpretation can involve strategies as simple as an illustrative poster presentation on native wildlife to a complex and well rehearsed live presentation of exotic animals. Ham (1992) defi interpretation involves translating the technical language of a natural science or related animal care facilities, from zoos to rescues to parks, employ some sort of environmental interpretation education program to inspire young and old alike. It is the duty of scientists to make their r esearch known and accessible to everyone in order to sustain the captive environment endangered species rely on for survival.
73 Appendix Lion Ethogram Resting RHEF resting head erect far from conspecific (far = >10 ft) RHEN resting head erect near co nspecific (near = <10 ft) RHDF resting head down far from conspecific (far = >10 ft) RHDN resting head down near conspecific (near = <10 ft) Sit all four feet on ground, front legs straight, back legs folded Yawn mouth opens wide then closes, no noise ----------------------------------------------------------------------------------------------------------Activity Stand all four feet on ground, legs straight Crouch similar to sit but with front legs folded as well, head forward and erect, ears an d eyes alert Stretch stretches out muscles, usually after resting Roll rolls from one side of body to the other, usually during resting Walk moving one foot in front of the other while standing Run very quick walk Jump crouch then leap through air C hase run after conspecific or other being Stalk in crouch slowly Pounce short jump onto conspecific or other being/object Swat paw rapidly extends and retracts toward conspecific or object Bite mouth closes on object Startle quick short movement/jump away from conspecific, object or noise Hiss exhalation of air, teeth bared, ears back Growl rumbling in throat, teeth bared, ears back Grunt short low pitched sound, ears forward Roaring repeating grunting sound, beginning very l oud & strong and fading away Drink lapping up water and swallowing Urinate relieving bladder Defecate relieving colon Groom licking fur Sneeze quick exhalation of air through nostril, quick shake of head Scratch moving paw with claws extended across self or object Sniff inhalation of air directed at object or conspecific Spray short spurt of urine, may or may not
74 be preceded y pawing of ground by back feet Rub rub head on conspecific or object Flehmening response sniff, then lift head open mouth t ongue out, breath in -----------------------------------------------------------------------------------------------------------Stereotypical behaviour s Pace repetitive walking ---------------------------------------------------------------------------------------------------------Breeding behaviour s: Mating bout includes, according to sex, at least Mounting or Being mounted along with other breeding behaviours sequentially Rolling see roll above, female will roll after mating Rubbing head see r ub above Rubbing perineal area rubs perineal area on conspecific or object Lick/Groom mate conspecific licks or grooms mate before or after mating (during mating bout) Lordosis similar to crouch but with rear lifted and tail held to one side exposing perineal area (female) Mounting male moves on top of female in lordosis Being mounted when female in lordosis is mounted by male female walks in front of male and goes into lordosis Low growl growl but softer sounding usually witho ut teeth bared or ears back Auto grooming female grooming of perineal area Scent marking/urinating see spray/urinating above, male performs behaviour after mating
75 Leopard Ethogram Resting RHEF resting head erect far from conspecific (far = >10 ft ) RHEN resting head erect near conspecific (near = <10 ft) RHDF resting head down far from conspecific (far = >10 ft) RHDN resting head down near conspecific (near = <10 ft) Sit all four feet on ground, front legs straight, back legs folded Yawn mouth opens wide then closes, no noise ----------------------------------------------------------------------------------------------------------Activity Stand all four feet on ground, legs straight Crouch similar to sit but with front legs folded as wel l, head forward and erect, ears and eyes alert Stretch stretches out muscles, usually after resting Roll rolls from one side of body to the other, usually during resting Walk moving one foot in front of the other while standing Run very quick walk Jum p crouch then leap through air Chase run after conspecific or other being Stalk in crouch slowly Pounce short jump onto conspecific or other being/object Swat paw rapidly extends and retracts toward conspecific or object Bite mou th closes on object Startle quick, short movement/jump away from conspecific, object or noise Hiss exhalation of air, teeth bared, ears back Growl rumbling in throat, teeth bared, ears back Meow short higher pitched sound, ears forward Sawing repeate d coughing sound, ears forward Drink lapping up water and swallowing Urinate relieving bladder Defecate relieving colon Groom licking fur Sneeze quick exhalation of air through nostril, quick shake of head Scratch moving paw with claws extended acro ss self or object Sniff inhalation of air directed at object or conspecific Spray short spurt of urine, may or may not be preceded y pawing of ground by back feet Rub rub head on conspecific or object Flehmening response sniff, then lift head open
76 mout h tongue out, breath in ----------------------------------------------------------------------------------------------------------Stereotypical behaviour s Pace repetitive walking ---------------------------------------------------------------------------------------------------------Breeding behaviour s: Mating bout includes, according to sex, at least Mounting or Being mounted along with other breeding behaviours sequentially. (Note that no breeding behaviour was observed as female was pregnant during study.)
77 Lion Behaviour Codes and Categories Resting B1= RHEF B2= RHEN B3= RHDF B4= RHDN B5= Sit B6= Yawn ----------------------------------------------------------------------------------------------------------Activity B7= Stand B8= Crou ch B9= Stretch B10= Roll B11= Walk B12= Run B13= Jump B14= Chase B15= Stalk B16= Pounce B17= Swat B18= Bite B19= Startle B20= Hiss B21= Growl B22= Grunt B23= Roaring B24= Drink B25= Urinate B26= Defecate B27= Groom B28= Sneeze B29= Scratch B30= Sniff B31 = Spray B32= Rub B33= Flehmening response -----------------------------------------------------------------------------------------------------------Stereotypical behaviour s B34= Pace ---------------------------------------------------------------------------------------------------------Breeding behaviour s: B35= Mating bout -----------------------------------------------------------------------------------------------------------
78 Leopard Behaviour Codes and Categories Resting B1= RHEF B2= RHEN B3= RHDF B4= RHDN B5= Sit B6= Yawn ----------------------------------------------------------------------------------------------------------Activity B7= Stand B8= Crouch B9= Stretch B10= Roll B11= Walk B12= Run B13= Jump B14= Chase B15= Stalk B16= Pounce B17= Swat B18= Bite B19= Startle B20= Hiss B21= Growl B22= Meow B23= Sawing B24= Drink B25= Urinate B26= Defecate B27= Groom B28= Sneeze B29= Scratch B30= Sniff B31= Spray B32= Rub B33= Flehmening response ----------------------------------------------------------------------------------------------------------Stereotypical behaviour s B34= Pace ----------------------------------------------------------------------------------------------------------Breeding behaviour s: B35= Mating bout ----------------------------------------------------------------------------------------------------------
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