Chemical communication

Elephants have a highly sophisticated system of chemical communication. A wide variety of chemical compounds are broadcast from modified skin and mucous membrane structures, including glands. These chemicals may be secretions, excretions, or filtrates. To sense these signals, the elephant is endowed with a sensitive olfactory apparatus for gaseous compounds and a vomeronasal organ for detecting liquid compounds. Centuries-old elephant lore from India (Nilakantha's Matangalila) recognized the role of chemical signals in the following observations: "And from the smell of their sweat, dung, urine, and must-fluid other elephants instantly are excited." "Upon smelling their own dung and urine, let them always produce a tickling of the palate" (Edgerton 1931, p. 53).

The leading researcher on this subject is Bets Rasmussen, who has collaborated with several veterinarians, physiologists, chemists, and ecologists, notably Irvin Buss, Michael Schmidt, David Hess, Bruce Schulte, Anthony Hall-Martin, and V. Krishnamurthy, over three decades to bring us a detailed picture of the anatomy, histology, physiology, chemistry, and behavior associated with chemical communication in elephants, especially the Asian species. Much of the work on chemical communication relates to signaling between the sexes for mating. Thus, the physiological and behavioral attributes of chemical signaling as they relate to reproduction are dealt with in chapter 3. In this section, I provide the background to the anatomical structures associated with chemical production and detection, the chemistry and function of the compounds, and only a brief account of the associated physiology and behavior.

The compounds that act as signals in elephant communication are produced and released from several parts of the body. Research is just beginning on secretions from the elephant's skin itself. Asian elephants have been observed exuding liquid around the toes on hot days. Recently, it has been established that Asian elephants possess well-developed sweat glands in the interdigital region, presumably for secreting liquids that contain chemical messages. A specialized skin gland, the temporal gland, is of course a very visible producer of chemical secretions. Located on each side of the head in the temporal depression, this modified apocrine sweat gland opens to the cheek surface through a thick-walled duct. The gland itself, lying just below the skin, consists of numerous lobules joined by connective tissue. A network of smaller ducts interconnects the lobules and leads into the main duct, which expels secretions in both male and female elephants. The temporal glands also release gaseous compounds that may act as signals. Messages may also be broadcast through saliva produced by glands in the oral cavity and by the mucous-lined trunk through expelled breath. The urogenital tract is also an important source of chemical signals released in urine or through cervical mucus (in females) and accessory sex glands.

The trunk of the elephant has a more complex structure than earlier believed (fig. 4.12). Its role in chemosensory function is only partially understood. The specialized vibrissae or hair on the dorsal trunk tip, although mainly tactile in function, may also play a chemosensory role (fig. 4.8). The long nostril passages have an olfactory membranous lining that clothes the well-developed ethmoturbinates and nasoturbinates. The epithelial cells associated with these turbinates are the smell receptors. The elephant's nose is believed to be five times as sensitive as that of a bloodhound, a remarkable olfaction capacity. Running through the trunk are the facial nerves and the maxillary branch of the trigeminal nerve. The elephant possesses one of the most developed trigeminal systems, with nerve endings that are important in detecting noxious compounds.

Two other chemosensory organs in the elephant have to be mentioned. The first is the vomeronasal organ (or Jacobson's organ) found in many amphibians, reptiles, and nonprimate mammals. In the elephant, the vomeronasal organ is a paired tubular structure (about 4 cm in diameter) located on the roof of the mouth (fig. 4.13). It is surrounded by connective tissue and cartilage and partially embedded in the vomer bone. This organ seems to be the key detector of chemical signals in less-volatile liquid substances such as urine. Small samples of the substance are transferred via the trunk tip to the roof of the mouth by the so-called flehmen response. From there, the neuroreceptors of the vom-eronasal organ transmit the information to higher brain centers for identification. The vomeronasal organ is especially important in processing signals relating to reproduction, such as detection of the estrous chemical signal in female urine by bulls. At the same time, it also seems to play a role, through the

Figure 4.13

The pair of vomeronasal organs located on the roof of an elephant's mouth. (Photo courtesy of L.E.L. Rasmussen.)

flehmen response, in other contexts, such as male-to-male and male-to-female musth signals and female-to-female signals of social significance.

The other possible chemoreceptor system is the palatal pits, which are small paired structures, numbering from 5 to 21, located at the junction of the trunk and the hard palate. The palatal pits seem involved in the commonly observed trunk-to-mouth contacts by individuals within a family. Although some of this contact may be tactile, it is certain that chemical signals are being transmitted through breath.

A bewildering array of chemical compounds may be present in the temporal gland secretion (TGS), exhaled breath, or excreted urine. It is not an easy task to find the specific identity of the compounds that act as biological signals in a given context. The first task is to identify the precise chemical nature of the compounds released, then identify likely candidates for bioactivity before carrying out field trials with elephants to recognize their possible signaling function. This is precisely what Bets Rasmussen and her associates have been doing for over three decades—a combination of sophisticated laboratory chemistry, field behavioral trials, and observation in captive and wild situations. They have so far focused on temporal gland secretions, breath, and urine in the context of sexual signals. Most of their work pertains to the Asian species unless stated to the contrary (table 4.4).

Secretion from the temporal glands of male Asian elephants when they come into musth, a rutlike sexual state, has been described since ancient times (see chapter 3). Female Asian elephants, too, on occasion secrete from their temporal glands. I have seen this happen only when a cow is in an advanced

Table 4.4

Conspecific chemical signals of Asian elephants: exudate-elicited behaviors and identified compounds.

Directionalitys

Exudate

(Putative Pheromone)

Chemosensory response* (Observed Behavior) [Postulated Intent]

Receiver

(Olfactory System)

Females male

Females female

Males female

Urine: preovulatory ({Zj-7-dodecenyl acetate)

Urine: follicular

UG mucus: prior LH-1

Urine: musth

Secretions: TGt (Whole)

(Cyclohexanone) (C5-C9 Ketones) (Frontalin)

Flehmens: high frequency (Precopulatory behaviors) [Concentration assessment] Checks and flehmens (Aggression) [Estrous detection] Checks

(Sender: tail flicking maximum)

[Detection: impending estrus]

Approaches, checks, places

(Reciprocal urination, vocalizations, tail erect)

[Assessment of musth status]

Flehmens

Checks, flehmens

Sniffs, repulsion

Attraction Indifference Moderate repulsion

Mature males (Sequentially MO, VNO)

Mature female, follicular stage (MO and VNO)

Mature female, follicular stage (MO and VNO)

Mature female, follicular stage (MO and VNO?)

Mature females:

(MO and VNO) Subordinate females:

(MO, VNO, palatal pits) Subordinate female: (MO)

Mature female, follicular stage (MO) Mature female in luteal stage (MO) Pregnant female (MO)

Male^ male Urine: musth

Breath: musth

Secretion: TG (Whole)

(Frontalin)

Maternal urine

Mothers offspring

Attraction

Flehmen

Deterrent

Sniffs

Retreat

[Spacing]

Repulsion

Attracted, indifferent, repelled Indifferent

Flehmen, check, retreat Flehmen

Most males (MO) Young males (VNO) Teenage males (MO) Males

Subordinate, nonmusth males

Teenage males Adult males Adult males Teenage males Offspring

Source: Modified from Rasmussen (1998), courtesy L.E.L. Rasmussen.

LH-1, first serum luteinizing hormone elevation; MO, main olfactory system; TG, temporal gland; UG, urogenital; VNO, vomeronasal organ system.

*Significantly elevated over controls.

tin male Asian elephants only during musth.

stage of pregnancy or just after calving (fig. 4.14). It is therefore not unreasonable to attribute a communication function to this secretion. Given that the protection of a newborn and allomothering are important within elephant family groups, an adult cow could be communicating this need to other family members.

Among African elephants, or at least those in savanna and woodland habitats, both males and females secrete rather freely from their temporal glands, often in response to disturbance, such as being chased. The scientific literature on the African species was initially rather confused on this subject. Elephant observers during the 1960s and 1970s loosely termed this as musth in both the sexes. They further postulated that temporal gland activity or musth had entirely different functions in the Asian elephant and the African elephant, a sexual role in males of the former and a more general communication function in both sexes of the latter species. An article on Amboseli's elephants by Joyce Poole and Cynthia Moss in 1981 cleared this confusion. They firmly estab-

Figure 4.14

Female elephants secreting from their temporal glands. While female African elephants (top) seem to secrete temporin quite freely, Asian females (bottom) do so only when in advanced stage of pregnancy or soon after calving.

Figure 4.14

Female elephants secreting from their temporal glands. While female African elephants (top) seem to secrete temporin quite freely, Asian females (bottom) do so only when in advanced stage of pregnancy or soon after calving.

lished that African bull elephants also come into musth, with the accompanying physical and behavioral traits with strong sexual overtones, as do their Asian counterparts. Secretion from the temporal glands of African bulls in musth is different from the secretion of immature and adult females and males at other times, which should be termed temporin. The temporin possibly plays a role in communication among individuals in a social group, as suggested above.

The early studies of temporin in African elephants by Irvin Buss and his associates focused on analysis of proteins and lipids (chiefly the steroid cholesterol), but later turned to the phenols, cresols, and the sesquiterpenes. Three sesquiterpenes (farnesol and two derivatives) were initially isolated from the temporal gland secretions of mature African elephants culled at Kruger National Park, South Africa. Prior to sample collection, these elephants had been stimulated into secretion by chasing them from a helicopter, thereby inducing stress. Recently, Thomas Goodwin identified two more farnesol-related compounds, one a bumblebee pheromone never seen before in a mammal, and the other known only from a Greek variety of the tobacco plant.

Although not much is known about temporal gland secretions in female Asian elephants, over the years Bets Rasmussen has been assembling chemical profiles of volatiles from temporal glands of individuals in various physiological states. Two sick females dying from foot infection had high levels of iso-prenes and ketones in addition to phenols. Some of the pregnant females had high levels of aldehydes. A female that secreted when she ran excitedly had an interesting compound that is a precursor of a farnesol. Secretions from the temporal gland, either visible liquids (temporin) or gaseous volatiles, may thus provide information to other members of the family group about health, physiological status, and stress.

Temporal gland secretions from musth bulls also contain a variety of lip-ids, proteins, steroids, and other organic volatile compounds, many of which are also seen in exudates of other mammals. The lipids in TGS include cholesterol, while protein concentrations may vary from about 25 mg/ml (in one Asian bull sample analyzed by P. S. Easa) to about twice this figure in African bulls. TGS in musth bulls also shows very high concentrations of testosterone, the male sex hormone, compared to its levels in blood serum during the same phase. None of these compounds, however, has demonstrated bioactivity as chemical signals, although they could in principle serve as long-duration signals given their greater persistence. For this, we should turn toward the volatile compounds, a mixture of several alcohols, ketones, dienes, and aldehydes found in TGS. All these are also seen in musth breath and urine, with the addition of several hydrocarbons in breath and furans in both (table 4.4).

Not all of these volatiles, however, may convey a specific message or evoke a response from other elephants. A signal about the musth status of a bull may be contained in some of these volatiles, either singly or in combination. It is not clear which of these volatiles are responsible for causing other nonmusth males to avoid a musth male, a behavior observed frequently in the wild. A

complex natural mixture of 10 compounds, including 8 ketones, an alcohol, and frontalin, elicited a distinct retreat response from subordinate and young female elephants during trials. These compounds of low molecular weight and high volatility (thus short-duration signals) are not seen in exudates of females or nonmusth males.

As a bull goes through various phases of musth, the chemical composition of the signals may also change. The TGS of young Asian bulls in musth have sweet-smelling ("honeylike") compounds, such as esters and 3-hexen-1-ol, that are not detected in the TGS of older bulls. Among the older animals, the chemical 2-butanone seems to signal the premusth period before TGS is visible. Compounds such as the frontalins and 2-nonanone, which are foul smelling, appear in the TGS of older bulls, especially during late musth.

A compound found in trace amounts in musth TGS and urine was fortuitously discovered to act as a male-to-female signal. This ketone of higher molecular weight, cyclohexanone, elicited a high frequency of flehmen responses from subordinate female elephants, although the response from dominant females was less. In fact, the females responded with a greater frequency when presented with an extract of cyclohexanone compared to the original male urine. Another behavior noticed when a group was exposed to this compound was a tendency for adult cows to bunch protectively around the juveniles. Males do not respond to this compound.

The search for a compound that acts as a female-to-male signal of estrous status led to a remarkable discovery by Bets Rasmussen and her associates. Among captive elephants, it was well known that bulls pay increasing attention to cows as the cows approach their estrous periods. While a bull may regularly test the urogenital region or the urine of a cow, the frequency of flehmen responses increases about 10-fold when the cow is in estrus. The chemical released in preovulatory urine by female Asian elephants to signal their estrous state has been identified as (Z)-7-dodecen-1-yl acetate (Z7-12:Ac), a compound of low molecular weight and high volatility.

The location and the biochemical pathway of synthesis are not known, although it is speculated that the acetate is produced in the liver. The playback experiments also show that a full response from Asian male elephants is obtained only when this acetate is presented in the medium of control urine, thereby suggesting that other compounds may be important for the estrous signal (fig. 4.15). Free Z7-12:Ac in urine will gradually combine with water to form the alcohol Z-7-dodecenol. Proteins can bind to the acetate and prolong its pheromonal lifetime. Many other volatile compounds are also released in urine. While some of these elicit a mild response, it is not yet clear whether any of these act singly or as cofactors with Z7-12:Ac in signaling reproductive condition. An odorant binding protein (OBP), similar to a class of compounds known as lipocalins, has been recently isolated from mucus in the elephant's trunk. The OBP is believed to regulate the transfer of acetate from urine to the vomeronasal organ during the flehmen response.

Figure 4.15

Bioassays of the female estrous signal, 1.0 mM (Z)-7-dodecen-1-yl acetate, tested on Asian bull elephants in Myanmar timber camps and in U.S. zoos. The results are expressed as mean (±SE) flehmen responses per hour. Note that with the "control" elephants, a full response was obtained only when the acetate was presented in (preovulatory) urine. (From Rasmussen 1998. Reproduced with the permission of Ecoscience, Canada.)

Figure 4.15

Bioassays of the female estrous signal, 1.0 mM (Z)-7-dodecen-1-yl acetate, tested on Asian bull elephants in Myanmar timber camps and in U.S. zoos. The results are expressed as mean (±SE) flehmen responses per hour. Note that with the "control" elephants, a full response was obtained only when the acetate was presented in (preovulatory) urine. (From Rasmussen 1998. Reproduced with the permission of Ecoscience, Canada.)

The same compound (Z7-12:Ac;) is used by many female insects, especially the Lepidoptera (moths and butterflies), as pheromones to attract mates, an amazing example of convergent evolution. Interestingly, African male elephants hardly respond to Z7-12:Ac; female Loxodonta must thus be using a different compound to attract mates.

Several other aspects of chemical communication in elephants are poorly understood. Female elephants provide information to other females about their estrous state through urine, but the identity of the compounds is not known.

This signaling could be for social reasons within elephant family groups or for promoting synchrony of estrous periods among females. The role of chemical signals in interindividual recognition among elephants needs to be explored further. In this long-lived species, it can be expected that social interactions would be based on individuals recognizing each other in the long term. There is already some evidence that an elephant calf can recognize its mother from her urine. This chemical memory from early imprinting may be retained for years or decades. In fact, bulls even show reduced flehmen response to the estrous urine of their mother several years after separation from her. This could be one mechanism for avoiding inbreeding irrespective of the precise nature of male dispersal from the natal family. Further research on chemical communication in captive elephants and the corroboration of results when possible in a wild situation would undoubtedly uncover fascinating new details about elephant society.

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