Researchers interested in chemical ecology have primarily focused their attention on insects. This has been due to several factors, of which moral concerns, quantity, and life span are but a few. Lately, researches are turning their attention to mammals and the role of pheromones and allomones known as social odors (Gorman and Trowbridge, 1989; Brown, 1979) in their lives. Mammalian use of social odors for defending territory (Gese and Ruff, 1997), signaling one’s sexual availability (Komers et al., 1999), and individual identification (Rasmussen and Schulte, 1998) are just a few of the areas that have gained the attention of researchers. Other researchers are looking into the effect of social odors from one species on another species (Paquet, 1991). Confirmation of intent of odor has predominately been restricted to field bioassays. Scent marking, the physical act of depositing a social odor, may serve to intimidate non-clan aardwolves as well as synchronize female estrus (Sliwa and Richardson, 1998). Several studies are finding expected chemical compounds (Gorman and Trowbridge, 1989) in pheromones while other studies are finding unexpected compounds (Rasmussen et al., 1996) used in semiochemicals. Mammalian chemical ecology is still within its formative years. However, the future smells quite bright.

Keywords: Mammal, pheromone, communication, behavior, scent marking, scent odor

Researchers of chemical ecology tend to study insects. This has been due to several factors, of which moral concerns, quantity, and life span are but a few. Insect models are more accessible to researchers as they are relatively less complex have a short lifespan, tend to be ‘hard wired’ behaviorally (are more instinctual), and are prolific. Due to the absence of the "fuzzy factor" which elicits feelings of warmth and protection, insects typically illicit an aversion reaction in humans, that culminate in being squished. The "fuzzy factor" can be attributed to large eyes, an infantile head, a short nose, a soft rounded look, and a possible innate instinct in humans to hold and protect small cute animals (Temple Grandin, personal communication). Insects can be studied in controlled laboratory conditions without raising an ethical and moral concern. Whereas, most mammals elicit the "fuzzy factor" in humans and as thus are often considered unacceptable as research animals.

The study of mammalian chemical ecology has been primarily field behavioral observations with some chemical analysis and identification. The study of mammalian scent marking has resulted in several hypotheses about the role of scent marks, as well as some understanding about when and where they occur. Mammalian semiochemicals (chemicals used for communication) are not the same as pheromones in that they are often a mixture of chemical compounds, and the response they invoke is not scripted. Scripting refers to pre-programmed behavioral responses to detection of specific scents and/or pheromones. The use and interpretation of scent marks by mammals is dependent on past experience, context, and age of animal (Beauchamp et al., 1976). A few of the chemical compounds that form various carnivore scent marks have been isolated (Goodwin et al., 1999; Rasmussen et al., 1997a; Gorman and Trowbridge, 1989).

Scent marking can be accomplished via the urine, feces or scent glands (Gorman and Trowbridge, 1989). The study of urine and feces derived social odors is somewhat hampered by distinguishing between excretion to empty the bladder and excretion to deposit a chemical message. Small ‘token’ quantities of excrement are usually considered to be communicative (Macdonald, 1985; Kleiman, 1966) but not always. It is important to note that the majority of authors and researchers, referred to in this paper, classified scent marking as any urination or defecation event.

Scent glands. Unlike the point source location for urine and feces, scent glands are to be found in numerous locations on the body, from the area around the eye, to the feet/hands/paws, to the chest to the genital region. Some glands are species specific while others can be found across species. For example, in the family bovidae, the metatarsal gland is found on the impala, while the inguinal gland is found in several species of antelope (Estes, 1991a). In African species there are at least 15 different scent glands in antelopes, eight in carnivores, four in prosimians (bush babies and pottos), and an unknown number of scent glands in monkeys and apes (Estes, 1991b). Scent glands are present in most African antelope, however they are diffuse or even absent in some species (Estes, 1991a) such as the waterbuck, which has multiple skin glands that release a musky odor (Spinage, 1982).

Pasting. Scent marking using a whitish, paste-like substance excreted from the inguinal (near the groin) glands are common in a few species such as the hyena (Estes, 1991c) and aardwolves (Sliwa, 1996; Richardson, 1990) and is referred to as pasting. Brown hyenas are unique in their pasting as they secret two separate substances (Gorman and Trowbridge, 1989), a white 97% lipid (Mills et al., 1980) substance, and a black watery volatile substance. The substances come from different inguinal glands and have completely different chemical and possible behavioral properties (Gorman and Trowbridge, 1989). The white substance comes from the sebaceous gland, is deposited on a grass stalk first, and remains ‘effective’ (scented) for several weeks. The black substance is from the apocrine gland, is deposited after the white paste, and is very volatile and evaporates within a few hours. Mills et al. (1980) proclaims that the white substance is used for claiming territory in the physical absence of the brown hyena. The black substance may indicate intra-clan communication on location, time, and movement patterns of clan members (Mills et al., 1980).

There are several hypotheses regarding the role of and the communicative aspects of scent marks. Many of the hypotheses are based on the study of a particular species, and as such may not be applicable to other species. Regardless of the theory and how it was derived there is no consensus on the purpose of scent marking and the message it conveys.

Intimidation. Intimidation is the hypothesis that in absence of the resident animal, the scent mark conveys to a potential intruder that the area is claimed by another animal, and the potential of being attacked if encountered by the resident animal (Richardson, 1993). This theory holds that the resident animal must attack intruders in order for the scent marks to carry any weight. This theory has a particular troublesome failing. Based on current understanding of training and learning by animals, there is a critical time relationship between cause and effect. The period between the signal (I.e. scent mark) and the reinforcement (I.e. attack by resident) needs to be fairly close in time in order for the animal to realize the connection (Pryor, 1985). This time period is critical to learning the association between the signal and the corresponding reinforcement. The time period between discovering a scent mark, entering the territory, and being attacked by the resident animal may be quite long; it is most often much longer than the time established by trainers required for associative learning. Another problem with this intimidation theory is the ability of an animal to generalize that the scent mark from one animal that resulted in an attack means that all scent marks are signals for an attack. Although many animals are able to generalize one situation to another similar situation (Skinner, 1953), it is uncertain whether an animal can generalize the scent of one animal, to being attacked by an animal regardless of ownership of the scent. According to animal behaviorist Temple Grandin (personal communication), animals are capable of a degree of generalization, however, they are also situation specific. For example, the author has witnessed zoo animals demonstrating a dislike for the zoo veterinarian. These animals would negatively respond to the presence, sound, or odor of the veterinarian, as well as the approach of the clinic vehicle. However, these animals did not generalize to the extent that a response would be evoked by the presence of an unknown veterinarian, or the approach of vehicles similar to the clinic vehicle. This leads to an even bigger dilemma. If an animal can associate a scent mark with the probability of being attacked, then how do they distinguish between friendly animals (I.e. group or clan members) and non-friendly individuals? The hypothesis that scent marks act as indicator to a potential intruder that another animal has claimed the area is possible. However, the idea of a scent mark indicating the potential of being attacked if encountered by the resident animal appears counter to current information on animal behavior and learning.

Orientation. The orientation theory (Walther, 1978; Lyall-Watson, 1964), suggests that scent marks are primarily for the resident to use as a compass or map for navigation within a territory. In short, scent marks help prevent an animal from becoming ‘lost’.

Border maintenance. The border maintenance hypothesis (Johansson and Liberg, 1996; Gosling, 1986) is somewhat of a hybrid between the intimidation and orientation hypotheses. This theory holds that the scent marks define territory, thus communicating to other animals that another animal has claimed the area. In effect, it states to others that they are about to leave their map.

Territory. Several mammalian species have been studied regarding usage of chemicals to define, mark, and claim territory. Hypotheses regarding scent marking and territory are abundant, with the general consensus being that scent marking often occurs at the edge of territories, however, the message is unknown. It was found that the presence of multiple oribi (dwarf antelope) males guarding a territory caused a single male in an adjacent territory to mark (via preorbital glands) his borders more often than single males with single males as neighbors (Brashares and Arcese, 1999). Brashares and Arcese (1999) did not find that size or number of territories or females neighboring the territory were related to the frequency of marking. It was found that scent marking increased on the borders patrolled by a multiple males, compared to borders patrolled by a single male oribi. In coyotes, (Gese and Ruff, 1997) it was found that dominant (alpha and beta) adults scent marked (via urine) on the edge of their territory with greater frequency than in the interior. Double marking and ground scratching was the most prevalent at the borders or the territory. Overall, the alpha mated pair did the majority of scent marking and increased the frequency during the mating season. Size of the pack did not appear to have an affect on the scent marking frequency. This study further found that transient coyotes scent marked less than resident coyotes, and while scent marking did so with the same posture as the resident pups and beta coyotes.

In the aardwolf it was reported that scent marks that were taken from one territory by the researcher and placed in another aardwolf’s territory, that the ‘invaded’ aardwolf would mark (via pasting) on top (overmark) of the invading scent, especially if the scent was near the boarder (Sliwa and Richardson, 1998). The first scent mark found by the ‘invaded’ aardwolf would be investigated much longer than subsequent scent marks from the same foreign aardwolf, 15 s and 9 s respectively. This was in contrast to the first scent mark found belonging to aardwolves from the same territory. Both the first scent mark and subsequent scent marks were investigated for equal amounts of time. When male aardwolves were presented with scent marks from a female within the territory and a female from outside the territory, the males would go directly to the unknown females scent mark, sniff for approximately 17 s, then investigate the familiar female’s scent mark for approximately 4 s and overmark the scent.

Captive subadult male hyenas were found to increase frequency of scent marking as they approached adulthood, with the dominant males marking more often than the subordinates (Woodmansee et al., 1991). Groups of hyenas patrolling the border of their territories will combine scent marking with various aggressive behaviors (Mills, 1987). This combination of scent marking and aggression suggest a defensive and/or territorial chemical signal targeted at non-group members. Ethiopian wolves scent mark with greater frequency during visual encounters with neighboring wolves, and double mark along the border of their territory during routine border patrols (Sillero-Zubiri and Macdonald, 1998). Sillero-Zubiri and Macdonald (1998) suggest that this behavior signals pack "composition and status" to their neighbors. The other papers did not as strongly suggest what the scent marks were communicating to the neighbors. Gese and Ruff (1997) felt that scent marking probably signaled maturity, while Sliwa and Richardson (1998) felt that scent marking was an intimidation tactic. Brashares and Arcese (1999) thought that scent marking assisted in maintaining the border, but do not state what the marks are actually communicating to other oribi.

Reproduction. Scent marking has also been associated with reproduction. In small cats in zoos it was found that reproductively active cats scent marked more often than cats that were not reproductively active (Carlstead et al., 1999). In fallow deer it is thought that females control when they ovulate based on the availability of a suitable male (Komers et al., 1999). The chemical message for reproductive readiness is transmitted via the urine. Komers et al. (1999) suggest that the females are in control of their ovulation. Male rats are aroused by chemical cues from females (Sachs, 1997). The above two studies suggest a different twist to the hypothesis that males induce ovulation in females. A study in moose suggested that bull (male) urine induces ovulation in the cows (females) (MIQUELLE, 1991). In female Asian elephants, the "come-hither" chemical has been identified from their urine (Rasmussen et al., 1997a; Rasmussen et al., 1997b; Rasmussen et al., 1996). The authors hypothesize that female African elephants also produce a "come-hither" chemical as well. It has been known that male elephants emit a substance from their temporal glands (near the eyes) and their urine during musth that signal to the female that they are sexually active (Rasmussen and Schulte, 1998).

Individual awareness. Few studies have been conducted on animal self-awareness, or individual identification. This politically sensitive topic has been alluded to in several studies, but a proclamation that animals are self-aware has been distinctly omitted. Often it has been assumed that self-awareness must be based on visual awareness. This view projects how humans identify themselves and others. However, many mammalian species use scent as their primary information sense. The idea that self-awareness occurs in mammals other than humans is beginning to find popularity in those who study behavior. The author feels that many studies imply self-awareness in animals. For example, animals tend to scent mark within their own territory, which often has well defined borders. Notable researchers such as Temple Grandin (personal communication) and Bernard Rollin (personal communication) also believe that animals are self-aware. The first step in studying this sensitive area is the study of whether animals can distinguish between individuals and self. One such study found that giant pandas are able to discriminate between urine of con-specifics (Swaisgood et al., 1999), with the males showing more interest in urine from females than from males. Studies on beagles (Dunbar, 1977) and cats (Veberne and de Boer, 1976) have demonstrated their ability to recognize the gender of their con-specific based on the scent of the urine. These studies suggest that mammals may be able to distinguish individuals and sex based on urine scent. They do not demonstrate that animals are self-aware or that they can pair a scent with a particular individual. However, a recent study suggests that aardwolves are both self-aware and can correctly pair a scent to the owner of the scent. Aardwolves presented with a scent mark of a neighboring aardwolf would investigate the scent, and then often headed directly to the border where the invading aardwolf resided (Sliwa and Richardson 1998), implying the animal recognized the neighbor’s scent and connected it to the other aardwolf’s territory. This same study noted that aardwolves that came across their own scent failed to react to it as they did to another’s scent. In fact, they spent very little time investigating the scent and none were ‘overmarked’.

Interspecies communication. The idea that the scent marking may serve a purpose between species is an exciting area of research that is wide open to investigation. If scent marks have an affect between species then the applicability to managers of mammals, whether domestic or wildlife is eminent. Studies have suggested that scent marking may facilitate similar species dispersal. For example, coyotes and wolves are closely related (Norwak, 1978), and they are known to inhabit overlapping habitats (in space and time) (Arjo and Pletscher, 1999; Paquet, 1991). It has been reported that wolves attempt to exclude coyotes from wolf territories (Bekoff and Wells, 1986), and on occasion have killed coyotes (Paquet, 1991). Coyotes have been reported to ‘overmark’ scent marks left by wolves, though the converse was not observed (Paquet, 1991). Does this suggest that wolves are dominant to coyotes, that coyotes are generally more territorial than wolves, or were these aberrant behaviors? The behaviors mentioned in the studies suggest that scent marking may be a method to keep the species dispersed (Paquet, 1991), and as such may prevent over utilization of resources by two similar species.

Unpublished observations by the author suggest that trails marked by dominant ungulate (hoofed mammals, i.e. deer, zebras) feces are avoided by subordinate species. It was noted that once the dominant species (zebra and eland) abandoned a trail then less dominant species (axis deer and black buck) would claim the trail via defecation and usage.

The study of mammalian social odors (pheromones) has resulted in several hypotheses about their role, when and where they occur, and their communicative aspects. Many of the hypotheses are based on the study of a particular species, and as such may not be applicable to other species. Regardless of the theory and how it was derived there is no consensus on the purpose of scent marking and the message it conveys. Mammalian chemical ecology is still in its formative years, as insect models are more accessible to researchers. Insects have a much less complex life history due to their much shorter lifespan; tend to be reactive rather than proactive, and vast numbers of subjects can be studied less expensively in controlled laboratory conditions.