Chapter 4 Behavioral Clues for Detection of Illness in Wild Animals: Models in Camelids and Elephants
As often noted, wild animals may be in an advanced state of disease before clinical signs are evident. Wild animals are not immune to pain or discomfort, but they do attempt to mask overt signs that would reveal their physical condition. Wild animal veterinarians should make every effort to diagnose disease at its earliest stages. Therapy may be useless unless it is initiated early in the course of a disease.
This chapter focuses on camelids and elephants in discussing normal and altered behavior in relation to the health and well-being of the animal.4,5 The influence of behavior on the health of animals is not a new concept, but it has become an important facet of veterinary medical education only during the last two decades. Several disciplines use behavior as a basis for study, including psychology, ethology, sociobiology, and animal behavior. Numerous contemporary authors discuss basic animal behavior and clinically abnormal behavior.1,10–13,16,25
Altered behavior is a key to detecting incipient illness. Each species or animal group has a repertoire of actions that astute observers are capable of evaluating and classifying. For purposes of this discussion, behavior is defined as all aspects of an animal’s total activity, especially those that may be externally observed. Behavior may be controlled by genetics, in which case the action is innate, but may also be learned or modified by individual experience.
Zoo and wildlife veterinarians may deal with hundreds of species of animals, each with their own behavioral characteristics. How then can they know all the subtleties of behavior that would allow them to detect early clues of altered behavior? In short, they cannot, but there are basic behavioral patterns that are shared by most mammals. Birds have their own patterns, as do reptiles and amphibians. Veterinary students become well versed in physical examination and laboratory detection of illness, but many receive little training or experience in simply observing normal behavior in a natural setting for domestic animals, let alone wild species. So how does one acquire the skills that will enable a person to detect the early stages of illness? One may read about behavior, but it takes time just looking at the species in a collection to learn enough to determine even minor variations from “normal” behavior. Another method is to listen to experienced keepers and trainers, but personal observation remains a key element.
Acquiring observational skills is important for the following reasons:
A veterinarian must first understand normal behavior to be able to detect abnormal behavior. Behaviors to be included are methods of offense and defense; communication (vocalization, body language, facial expression), social behavior, interaction with other animals, hierarchic status, locomotion, food intake, defecation/urination, scent marking, recumbency, getting up and down, reproductive behavior (courting, copulation), and stress.8,14,16,23,27
Offense and Defense
Offense and defense weapons used by camelids include kicking, charging, chest butting, biting, and spewing stomach contents (spitting) onto other camelids or people (Figures 4-1 and 4-2). Veterinarians and animal handlers must be aware of any abnormal behavior that may develop in hand-raised camelid neonates. Camelid neonates (cria in South American camelids [SACs], Spanish term for “baby animal,” and calf in Old World camelids [OWCs]) that are bottle-fed and kept without social intercourse with other camelids may become imprinted on people. The resulting abnormal behavioral characteristics are more critical in male camelids but may also occur in females. When the hand-raised male reaches sexual maturity, he may begin to treat humans as he would another male camelid. He will charge and chest-butt a person, who will likely be knocked down and then bitten. When male camelids fight other male camelids, they may bite each other on the legs, neck, or more seriously the scrotum, castrating the victim.
This situation occurs more often in privately owned camelids, but if a cria is placed in a zoo petting area with only human companionship, problems may develop at maturity. I was attacked by a hand-reared male dromedary camel, which charged open-mouthed. Fortunately, a lead rope warded off the attack until escape was possible.
Spitting behavior is, unfortunately, one of the few facts that the general public knows about SACs. They are capable of projecting the foul-smelling stomach contents a distance of 1 to 2 m (6½ ft). SACs spew forward, but OWCs may also “spit” out of the side of their mouths. In reality, llamas and alpacas are generally placid around people, and spitting at people is rare. If milder threat displays are disregarded, however, spitting is the ultimate response in social intercourse between SACs. The material spewed out of the mouth may be saliva or feed material, if in the mouth at the time. It is interesting to watch an annoyed cria spew out a vapor of saliva. The reflex response exists, but the first compartment of the stomach is not yet functioning, so there is no content other than saliva.
The behavioral sequence of spitting begins with the ears laid back against the neck, accompanied by a gulping or gurgling sound from the throat region. A bolus of food is then regurgitated from the first compartment of the stomach.
It has been my experience that alpacas are more prone to spitting than are llamas, but individual llamas may also develop a dislike for a particular person. Veterinarians often bear the brunt of such disfavor.
SACs usually “cow kick,” reaching forward and outward. OWCs may reach forward and strike with the foreleg and may kick in any direction with the hind leg. Camelids have long legs and may scratch an ear with a rear foot. Alpacas tend to be more prone to kicking than llamas.
Male camelids have formidable canine teeth and are capable of inflicting serious or fatal injury (Figure 4-3). OWCs have been known to grasp a child by the head and shake it, often breaking the neck and crushing the skull.
As in human society, an effective means of communication is vital for the survival of any population of wild or domestic animals. SACs communicate with each other, humans, and other animals by vocalization and body language and by scent (see Scent Behavior).
Although SACs are not highly vocal, they do have a repertoire of sounds. Alpacas are generally more vocal than llamas. The most common sound has been described as humming (bleating). The pitch and tone of the humming are significant in SAC communication. Franklin7 describes the “contact hum” as an auditory contact between herd members and especially between a mother and her cria. “Status humming” is a deeper tone that communicates contentedness, tension, discomfort, pain, or relief. The “interrogative hum” is higher pitched and has an inflection at the end. Other variations in intonation are described as a “separation hum” or a “distress hum.”
Llamas emit a snort characterized by a short burst of air through the mouth with loose lips. The snort indicates mild aggression. A clicking sound may be made with the tongue, which also indicates mild aggression. A grumbling threat is emitted when a feeding animal is approached too closely by another, or when an aggressor is about to regurgitate onto an offender.
Screaming indicates extreme fright. Some llamas and alpacas scream continuously when restrained for diagnostic or therapeutic procedures. Screeching is a loud squealing sound, usually made by males chasing one another during a territorial dispute or a fight.
The SAC alarm call is emitted when a male or female perceives danger to be near. The approach of strange dogs or other predators may trigger an alarm call. The alarm call is a high-pitched series of sounds variously described as “whistling” or “neighing” and by some as the “braying of a hoarse donkey.” When the alarm call is sounded, other SACs within hearing become alerted and turn toward the source of the sound.
Male llamas, alpacas, and guanacos emit a rhythmic expiratory grunting sound called orgling while chasing a female or copulating. Vicuñas may or may not orgle. The word “orgling” is not in a dictionary but is in common usage by people involved with camelids. An owner coined the term, which is a phonetic approximation of the sound made.
Body language, including ear and tail position, is a sure indicator of the mental state of a SAC. Various degrees of aggression are communicated between herd mates by ear, head, and tail positions, usually displayed in concert (Figure 4-4). The ears of a contented, nonaroused SAC are in a vertical position and turned forward. In the alert animal the ears are cocked forward; relaxed SACs may allow the ears to lie horizontal to the rear (Figure 4-5). This is a normal position and should not be considered aggression because other signs of aggression are absent. In some individuals the ears may appear to spread sideways from the top of the head. This ear position may be used when listening to activity behind them or just for relaxation. Asymmetric ear positions may also be seen. Ear and tail position may be in a continual state of flux, especially when animals are fed and if feeding stations lack adequate space for all herd members.
Fig 4-4 Camelid ear and tail positions: A, normal alert; B, slight aggressive; C, aggressive; D, extreme aggression (threat); E, normal relaxed; F, alert tail stance; G, alarm tail stance; H, aggressive tail stance, also submissive tail stance.
Mild to moderate aggression is signaled by the head held horizontal, with the ears positioned above the horizontal. As aggression increases, the ears are below the horizontal and may be flattened against the neck. Intense aggression is exhibited by the nose being pointed in the air and the ears flattened against the neck.
Camel ears are much shorter but may still be observed in the same positions as for SACs, signaling similar emotional states.
Tail position also communicates social information. In the nonaroused SAC, the tail lies flat against the body. Mild aggression or alertness is indicated by the tail being slightly elevated, but below horizontal. As the degree of agitation escalates, the tail may be carried horizontal, curled above horizontal, or vertical. Basically, the higher the tail, the higher is the level of aggression. The tail may also be seen to wave from side to side, especially in males that are slightly agitated. These aggressive behaviors are employed by social animals to minimize outright fighting.
Submissiveness in the llama, guanaco, and alpaca is indicated by curving the tail forward over the back, with the head and neck held low, the ears in a normal to above-horizontal position, and the front limbs slightly bent (Figure 4-6). This behavior is frequently seen in SACs that become imprinted on humans. The submissive crouch of a vicuña is with the tail curved forward, but with the head curved back over the body.
Llamas generally move at normal gaits with the head held vertically or slightly forward. Alpaca normal neck position is approximately 70 degrees above horizontal. When either of these species rushes or charges at dogs, coyotes, other SACs, or humans, it does so with the neck held almost horizontal. This position may be used for balance, because it is also the head and neck position used when running downhill.
All four species of SACs are social animals (Figure 4-7). Alpacas are generally more flock or herd oriented than llamas. Alpacas are also shyer, more easily frightened, and less curious than llamas. Wild SACs (guanacos and vicuñas) live in social groups.
Fig 4-7 Four South American camelids: top left, vicuña; top right, guanaco; bottom left, alpaca; bottom right, llama. (See Color Plate 4-7.)
Vicuñas have separate family feeding and sleeping territories defended by a single adult male, with a few breeding females and their young offspring. The territories are delineated by strategically located dung piles and perhaps other scent-marking stations. Pathways between feeding and sleeping territories may be shared with other family groups. Juvenile and subadult males live in bachelor herds.
Guanacos may be sedentary or migratory. They also have feeding territories, live in family groups during the breeding season, but disperse or seasonally migrate into larger social groups during the nonbreeding season.
Domestication of llamas and alpacas has modified intense territorial behavior, but most of the communication forms have been retained. Separation of an individual from a SAC herd should raise a “red flag,” warranting close inspection and examination.
Interaction with Other Animals and People
Llamas and alpacas are curious about the presence of any strange animal in their environment. Their curiosity may lead to trouble if an animal investigates the presence of a venomous snake, and nose bites are common.
Dogs are tolerated if they are familiar farm dogs. Large dogs, such as maremmas, Great Pyrenees, and Anatoli sheepdogs, are used to guard llamas and alpacas from marauding coyotes and other dogs. Such guard dogs live with the animals and may even be seen to herd a SAC away from danger. Strange dogs always elicit an alarm stance or even an alarm call to bring the herd to attention. If the dog enters the enclosure, a single animal may attack it, or the entire herd may face the dog and rush it in concert.
Dogs are occasionally used to herd alpacas, but camelids generally do not tolerate this well. A dog that approaches from the rear is likely to be soundly thumped by a flying foot unless it is experienced in avoiding the rapid-fire kick of either llama or alpaca. If the dog approaches from the front, it likely will be charged. SAC aversion to dogs carries over from the attitude toward other would-be predators that could threaten juvenile camelids. North American predators include packs of dogs (Canis familiaris), coyotes (Canis latrans), and mountain lions (Felis concolor).
A group of SACs, whether all males, all females, or of mixed gender, quickly establishes a hierarchy (“pecking order”). Hierarchic status may be determined by seniority in the herd, age, or gender and relatedness. Once established, the rules are obeyed, or action is taken by the dominant over a subordinate individual. The action may be only a threat or may be carried to a conclusion by spewing stomach contents at the offender. However, adult males may engage in vigorous combat.
Defecation and Urination
South American camelids normally urinate and defecate at communal dung piles (Figure 4-8). The ritual begins when first arising in the morning at daybreak. This may be the only time that urine samples and fresh fecal samples may be collected. The dung pile is a social gathering site. Camels defecate indiscriminately. Camel fecal pellets are so dry that they may be used for fuel immediately on discharge.
Male and female camelids partially squat and project urine rearward, clear of the hind limbs. Changes in frequency, position, and duration of urination and defecation are important indicators of incipient illness.
Grooming and Water Behaviors
Rolling or dust bathing is one form of grooming in SACs (Figure 4-9). This behavior is so innate that pack llamas with full packs have been seen to lie down and attempt to roll. It may be similar to scratching one’s back. In addition to dusting, grooming involves other behaviors, such as scratching with a hind foot on the bottom of the abdomen, front limb, or head and neck; rubbing against fence posts, fencing, barns, or trees; and chewing at accessible points on the body or limbs. These behaviors do not necessarily signify a skin condition; it is often a simple itch.
Alpacas like to play in water. If water is provided in tubs, buckets, or tanks, they will joyously splash. Both llamas and alpacas seek out water during hot weather (Figure 4-10). If a pond or large water tank is available, they may stand in the water up to their abdomen. Both species are capable of swimming but do so only when forced; however, they will stand or lie down in shallow ponds or streams to cool themselves. Heavy fiber normally covers the legs of alpacas down to the fetlocks. In hot weather they may stand in water so long that the leg fiber becomes macerated and sheds, leaving a blocked-haircut appearance on the upper leg.
Locomotion is a form of behavior, and evaluation of locomotion patterns is important in assessing conditions of the musculoskeletal and nervous systems. Camelids have four natural gaits: the walk, pace, trot, and gallop. The long-legged llama is more prone to use the pace as a medium-speed gait, whereas the shorter-limbed alpaca tends to gallop more easily.
Juvenile SACs often engage in play behavior; tussling with one another and, especially at twilight, engaging in a fifth gait, a stiff-legged bouncing called stotting or pronking. Occasionally, young adults will also join in the activity, particularly females trying to attract the attention of males.7
If an animal is removed from a herd, or if a new grouping is formed, the stress level in the herd may be elevated until hierarchic status is reestablished. In most cases it is easy to spot the dominant individual in a herd, but subtle nuances are detected by carefully observing the animals eating at a manger. This is a good time to note the repertoire of ear and tail positions.
South American camelids spend many hours each day grazing or browsing and ruminating. Although llamas and alpacas are not ruminants in a taxonomic sense, they do ruminate (regurgitate a bolus of stomach contents, rechew the cud, and reswallow it). The progenitors of both camelids (suborder Tylopoda, “padded foot”) and ruminants (suborder Ruminantia) separated and followed different evolutionary pathways 40 to 50 million years ago, when both groups had simple stomachs. Parallel evolution brought them both to a foregut fermentation strategy to utilize highly fibrous forages.
The pattern of chewing is different from that in horses, cattle, sheep, goats, dogs, or cats, being a figure-eight configuration. The cheek teeth normally have sharp enamel points to assist in the shearing and grinding process. The cycle of ingestion of feed, regurgitation of a bolus by reverse esophageal peristalsis, rechewing, and reswallowing is a series of behaviors that merit notice by managers and veterinarians alike. Variations in the rhythm, rate, and characteristics provide valuable insight to digestive function.