The Lagomorpha

INTRODUCTION

The order Lagomorpha is divided into two families, the Ochotonidae (pikas) and Leporidae (hares and rabbits). The lagomorphs are characterized by having ever-growing incisors with enamel on both the posterior and anterior surfaces. They differ from the rodents in that there are two pairs of upper incisors, with the second pair located directly behind the first. It is a small order of only nine genera but with an extremely wide distribution. The Leporidae were found over the entire world except for Australia and southern South America, where they have been introduced by man. The pikas have a more limited distribution, being confined to montane areas in eastern Asia and western North America. It is generally conceded by paleontologists that the lagomorphs have been phylogenetically distinct from the rodents for a considerable period of time, but the two orders share certain ancient affinities, which led Simpson (1945) to place both rodents and lagomorphs in the same cohort-the Glires.

The order is characterized reproductively by induced ovulation (Asdell, 1964) and a trend toward the production of precocial young. Although the young of Ochotona are born sparsely haired with the eyes closed, as are the young of the European rabbit (Oryctolagus), the young of most species of North American rabbits (Sylvilagus) are born well furred but with the eyes closed. The young of hares A(Lepus) are born with the eyes open and are fully furred.

Female pikas typically bear their young in nests within the burrows built in the rock slides they inhabit. Young European rabbits are born in nests generally situated in a rather deep burrow and constructed of fur plucked from the mother's chest. On the other hand, young of the genus Sylvilagus are born in nests that are merely shallow depressions in the ground, although they are generally lined with fur plucked from the mother's chest as well as with a loose covering of vegetation gathered by the female after parturition. Lying in a shallow depression which may be partly covered with grasses, the young of hares are protected even less than the young of Sylvilagus.

Characteristically, female hares and rabbits suckle their young at long intervals, usually once a day (Southern, 1948; Denenberg et al., 1969; Sorenson et al., 1972). The female is thus not in continuous attendance upon the young, although if the young are disturbed and emit a sharp squeal, the female may return. Moreover, antipredator behavior may be exhibited if the nest has been disturbed by a snake, weasel, or other predator (Marsden and Holler, 1964). There is no recorded retrieving on the part of the females of the genera Sylvilagns, Oryctolagns, and Lepus (Sorenson et al., 1972; Denenberg et al., 1969). The absence of a retrieval response may be attributed in part to the fact that in Lepus the young are precocial enough to flee on their own, whereas in Sylvilagus the whole strategy of antipredator behavior is based on concealment, which is reminiscent of the pattern of hiding young in many species of ungulates. The absence of the retrieval response in Oryctolagus is a little more difficult to account for. Retrieving has not been tested for in Ochotona.

THE OCHOTONIDAE

The pikas in both the New World and Old World are found in alpine habitats and, in particular, choose rock slides or tallus slopes. They differ from other genera of the Lagomorpha in that they gather a variety of grasses and forbs during the summer months and lay them on rocks in piles to dry in the sun. This dried herbaceous material is then cached in rock crevices for use as fodder during the winter. The natural history of pikas has been well documented by Severaid (1956) in North America and by Kawamichi (1968, 1970, 1971) and Haga (1960) for the Asiatic species. Pikas appear to be diurnal and, although colonial, they are spaced with individuals occupying their own home ranges. In the Japanese pika (Ochotona hyperborea) a pair can occupy the same home range through a breeding season, but the North American pika (Ochotona princeps) usually shows separate centers of activity for the male and female throughout the annual cycle (Kilham, 1958). Males enter a female's home range only to court and mate. In all pikas males and females are extremely intolerant of members of their own sex.

Communication by means of chemical signals undoubtedly takes place in colonies of pikas. The animals typically defecate at one place in their home range and this could serve as a source of chemical information for neighbors or strangers intruding on the home range; however, we lack experimental data. Pikas have a conspicuous gland on the cheek (Harvey and Rosenberg, 1960), apocrine in structure, which shows shifts in activity through the reproductive cycle. The animals have been noted to rub the cheeks at various points within their territories, and sniffing of the glandular areas is frequent during male-female interaction prior to mating.

In contradistinction to the Leporidae, the pikas are rather vocal. So conspicuous are the vocalizations that most studies of communication in the Ochotonidae have concentrated on auditory communication. Somers (1973) defines two loud calls used in distance communication by members of a given family group or neighbors in a colony. The short call is used when the territory is invaded by a conspecific or when an aerial or terrestrial predator is sighted. Repetitive and quite harmonic in its structure, the call appears to alert colony members. It is reminiscent of similar warning calls given by diurnal montane rodents, such as marmots (Marmota) and the Andean viscacha (Lagidium). In addition to the short call with its warning function, pikas typically produce a "song," which is a series of short notes varying in duration as the song sequence progresses. Each song sequence can last for twenty to thirty-five seconds. In O. princeps it appears to be given predominantly by males, although the Asiatic species appear to show a similar song form that is not so pronounced in its dimorphism (Kawamichi, 1968, 1970). Somers suggests that the song may have both a territorial and a reproductive significance. It is similar to calls given by males of arboreal and semiarboreal rodents, including Erethizon and Dinomys (Eisenberg, 1974). Dialect variations between separate populations of pikas have been described for the short calls (Somers, 1973).

THE LEPORIDAE

The rabbits and hares do not produce the striking song and antipredator vocalizations found in the Ochotonidae. Most calls of rabbits and hares are used for short-range communication. Antipredator behavior in hares and rabbits often involves visual display, including the conspicuous white patches on the underside of the tail, which have evolved as a form of colony warning and individual distraction display during antipredator behavior. As a result of the lessconspicuous vocal repertoire in the leporids, most researchers have confined themselves to studies of nonvocal communication and, in particular, olfactory communication (Coujard, 1947; Mykytowycz, 1965, 1966a, 1966b, 1966c, 1967).

The behavior of the European rabbit (Oryctolagus cuniculus) is perhaps the best studied of all lagomorphs (Southern, 1948; Myers and Mykytowycz, 1958; Myers and Poole, 1958; Mykytowycz, 1958, 1959, 1960, 1961). In brief, the European rabbit lives in organized social units called warrens. Activity centers around a series of burrows used for several generations. A warren generally contains several breeding adult females who can and do form a dominance order that restricts the breeding behavior of younger females by restricting their access to high-quality nesting sites. Females construct burrows for rearing the young and do so unaided by males.

Males form a distinct dominance hierarchy with a dominant adult male ranging over the entire warren and having access to several breeding females. A dominant male has active anal glands that impart an odor to the hard fecal pellets deposited in specific dung piles. Such fecal pellets are to be distinguished from those feces formed during an initial passage through the gut which are reingested and then passed in the hard form. The size of a male's anal glands correlates with his dominance status (Mykytowycz, 1966a). It has been suggested that the dung piles serve as indicators of adult male occupancy to any strange males wandering into the area.

The inguinal glands of adult male rabbits may play a role in sexual attraction (Mykytowycz, 1966b). Mykytowycz (1966c) has also noted that Harder's gland is dimorphic in the European rabbit, being larger in the male, and, furthermore, that this gland is dependent on androgen levels. Thus, in castrated males the Harder's gland diminishes in size.

Dominant adult male rabbits also possess an active submandibular gland. Secretions from this gland are deposited by "chinning" behavior, where the male rubs the chin on conspicuous objects in the environment or on does (Heath, 1972). Chinning is frequently exhibited by dominant males within a rabbit warren. It would appear that marking behavior in the wild rabbit insures that strange males are excluded from the warren and females are covered with the dominant male's scent, thus maintaining group integrity (Myers and Mykytowycz, 1958; Heath, 1972).

The European hare (Lepus europaeus) does not show the strong dimorphism or seasonal change in the size of anal glands that the European rabbit shows. However, conspicuous dimorphism and seasonal activity in Harder's glands and inguinal glands have been noted (Mykytowycz, 1966a, 1966b, 1966c). Hares typically do not form warrens, and their activities appear to be much more individualistic. Adults are generally well spaced, although temporary associations can be formed when does come into heat (see Lechleitner, 1958; O'Farrell, 1965).

Studies on North American rabbits have been carried out by Marsden and Holler (1964). The two species Sylvilagus floridanus and S. aquaticus were studied in confined populations. The swamp rabbit (S. aquaticus) displayed territoriality, while the cottontail (S. floridanus) did not. Both species demonstrated structured dominance hierarchies among conspecific males. S. aquaticus males actively marked their territories with the submandibular gland.

During courtship in rabbits and hares, a complex series of events occur whereby males attempt to approach females coming into estrus and a female generally responds by boxing or lunging at the male. The male may then turn and dash past her or leap over her, often urinating on her. Enurination behavior by males during approaches has been described for Oryctolagus (Southern, 1948; Heath, 1972), Sylvilagus (Marsden and Holler, 1964), and Lepus (Forcum, 1966; Lechleitner, 1958). Enurination while leaping or combined with flashing of the white underside of the tail (Southern, 1948) clearly involves visual as well as chemical communication. It has been described also for numerous caviomorph rodents (Kleiman, 1971, 1974).

Although auditory communication is not so pronounced in leporids as with pikas, rabbits and hares produce sounds in a variety of contexts. A sharp thump with the hind foot produced when the animal is startled can serve as a warning signal to colony members in Oryctolagus and Sylvilagus. A throaty growling sound may be produced by males and females when disturbed in their burrows. Females of the genus Sylvilagus produce a similar sound when they are disturbed on the nest. A graded series of squeaking sounds are produced by rabbits during courtship and copulation. Males will produce a squeak sound when approaching a female and females may produce a similar sound when approached by a male. A modified squeak, labeled the chirp by Marsden and Holler (1964), may be produced by a female while a male is driving her preparatory to mounting. A high loud squeal is given during copulation by male rabbits of the genus Oryctolagus (Myers and Poole, 1961). Marsden and Holler report a similar sound for Sylvilagus which they believe is produced by the female. A twosyllable call may be given by a startled cottontail rabbit who has made a run and then turns to observe the source of the disturbance. It can serve to alert colony members. All lagomorphs apparently produce a distress cry, which is a high-pitched screaming note generally given by an animal that has been captured by a predator.

The Rodentia

INTRODUCTION

The rodents form a distinct order of mammals having an ancient lineage. In fact sciurids are clearly recognized from the fossil records of the Oligocene. The group is characterized by having a single pair of rootless, ever-growing incisors in both the upper and lower jaws. The incisors have enamel only on the anterior surface. Since the posterior surface of the incisors wears more rapidly than the anterior, a chisellike cutting tool results, which provides rodents with their key adaptation, the ability to gnaw into hard surfaces and make effective use of a variety of plant parts for foodstuffs. There are fortythree living families of rodents, grouped into fifteen superfamilies, including over 1,680 species; it is the most diverse order of living mammals.

We will first briefly review rodent communication mechanisms and then discuss some key evolutionary trends resulting in convergence in communication patterns of different species. The subordinal classification of rodents into Sciuromorpha, Myomorpha, and Hystricomorpha is somewhat artificial and such taxonomic grouping has been criticized, but no alternative subordinal classification has been universally accepted (Wood, 1965; Simpson, 1959). We will therefore refer mainly to superfamilies when discussing adaptive trends within this diverse order.

The basis for much of our knowledge of mammalian physiology, psychology, and psychophysics has resulted from intensive studies on a few selected species of muroid rodents. Behavioral investigations on Rattns norvegicus have been carried out for seventy years and much of the work was summarized by Munn (1950). Similar to investigations on the laboratory rat are those on the laboratory mouse (MILS MUSCULUS). In recent years the Syrian golden hamster (Mesocricetus auratus) and the Central Asian jird (Meriones unguiculatus) have become popular rodents for behavioral studies. The only two genera of wild muroid rodents for which intensive studies have given us a reasonable picture of the communication systems are Microtus and Peromyscus. Recent research on Peromyscus has been summarized in the volume edited by King (1968).

Comparisons of rodent behavior repertoires were summarized by Eibl-Eibesfeldt (1958), Eisenberg (1967), and Grant and Mackintosh (1963). The behavior of hystricomorph rodents has been reviewed by Kleiman (1974), and the vocal repertoires of South American hystricomorphs (= caviomorphs) are the subject of a review by Eisenberg (1974).

SIGNALS AND COMMUNICATION-A BRIEF REVIEW

The sensory capacities of Rattus norvegicus and the role of the brain in sensory integration were painstakingly studied by Lashley (1950). Although his studies did not intentionally analyze communication by rats in their normal social environment, Lashley's theories were pervasive. Lashley concluded that many complex activities of rats did not depend either on a specific area of the rat's sensory cortex or on a specific form of sensory input. Strongly influenced by Lashley's conclusion, Beach studied the sexual response of the male rat and the retrieval response of the lactating female. After a series of ablation experiments, Beach and Jaynes (1956) concluded "It appears that the female's retrieving behavior, like the sexual behavior of the male rat or like the maze-learning performance of both sexes, normally involves multi-sensory controls." There is no doubt that several sensory inputs may be involved in the integration of behavior between two interacting rodents, but it is equally evident that certain behavior patterns may be released by very specific signals during interactions. The discovery of infant ultrasonic sounds as releasers of retrieval behavior in rodents (Zippelius and Schleidt, 1956) and a renewed interest in olfaction as a communication channel have dominated recent research on rodent communication.

Utilizing the golden hamster (Mesocricetus auratus) as an experimental species, Murphy and Schneider (1970) demonstrated that male copulatory behavior will not be exhibited unless the male can perceive the odor of the estrous female. The vaginal secretions of the estrous female have now been implicated as the source of the chemical signal (Murphy, 1973). Thus, the presence of a stimulus from a single source is necessary for the release of sexual behavior in the male hamster. Obviously care must be exercised in the application of general theories to both new social contexts in well-studied species and analysis of interaction forms in species that are newly studied. Some forms of social interaction in rodents may indeed depend on a multiplicity of stimulus inputs, whereas other signal systems may in fact conform to the classifical concepts of releaser and innate release mechanisms (Lorenz, 1950).

Although considerable attention has been devoted to the analysis of those behavior patterns thought to have communicatory significance, the analysis of the reception and processing of stimulus inputs has proceeded more slowly, although the patterning of social interactions is very dependent on the perception of conspecific signals.

This differential emphasis is noticeable in the field of hormone-behavior research. Although there are numerous reports indicating that physiological state affects behavior output (e.g., see Levine, 1972), the converse area of study has been almost ignored. The most direct proof that hormonal state affects stimulus reception has been provided by Komisaruk et al. (1973) for the tactile sensory system. They have shown that the sensory field of the pudendal nerve (the perineum) is significantly increased in female rats given estrogen treatment. Thus, there are changes at the level of the peripheral receptors due to gonadal hormones. Since the lordosis posture is stimulated by both the mounting and the pelvic thrusting of the male, it would appear that increased sensitivity of the perineum might facilitate the female's response during copulatory attempts by the male and thus improve the chances of successful intromission.

Within the olfactory system there is increasing evidence that odor detection depends, to some degree, on physiological state. For example, Sakellaris (1972) has shown a decreased threshold to the odor of pyridine in adrenalectomized rats when compared with normal rats. Corticosterone administration raised the threshold to normal levels. Recently Pietras and Moulton (1974) have reported increased performance in odor detection (using mainly cyclopentanone) in rat females during natural estrus when compared with other stages of the estrous cycle or pseudopregnancy. There is every reason to believe that the sensitivity to conspecific odors would also be affected.

Using enclosed conspecifics as the odor source, Carr and Caul (1962) could not detect any differences in the abilities of normal and gonadectomized male and female rats to discriminate the odors of sexually active or inactive members of the opposite sex. However, recent studies have indicated that hormonal state as well as experience affect odor preferences. For example, Carr et al. (1966) have shown that sexually active intact male rats prefer the odors of receptive females to those of nonreceptive females, while both sexually inactive and castrated male rats show no preference, as measured by the time spent investigating the different odors.

These studies clearly suggest that hormones are affecting the sensory systems, but where such changes occur, i.e., at the peripheral receptors or at other levels in the central nervous system, should be examined more closely.

Visual Input

Numerous studies of rodent behavior have resulted in the description of characteristic postures, movements, and configurations, many of which are common to a wide range of rodent species (Grant and Mackintosh, 1963; Eibl-Eibesfeldt, 1958; Eisenberg, 1962, 1963a, 1967; Kleiman, 1974). (See Fig. 1.) The description of postures and movements has allowed certain forms of comparison within or between species when the postures and movements are quantified under controlled test situations and expressed as frequencies or ratios. Some movements or postures are associated with the genesis of auditory, olfactory, or tactile input; other postures could serve solely as visual signals. (See Fig. 2.) Yet proof of stereotyped movements or postures serving as visual signals is lacking. Many of the commonly studied rodent species are nocturnal or crepuscular. It is supposed that the role of visual communication in these species (e.g., Rattus, Mus, Peromyscus, Mesocricetus) is minimal, yet diurnal rodents have a rich repertoire of postures and movements, some of which may be true visual displays (Steiner, 1970; Horwich, 1972; Kleiman, 1971, 1972, 1974).

Fig. 1. Contact postures during encounters with Peromyscus maniculatus. The arrows indicate important features and the dotted lines demarcate the white ventrum from the brown upperparts. A. Elongate posture during exploration or prior to contact—note the erect ears and tense, extended tail. B. Naso-nasal contact—note the juxtaposition of the mouths and depression of ears. C. Naso-anal contact. D. Acceptance of contact by the animal on the right—note the closed eyes and flattened ears. E. Submission by the animal on the left—compare with D. (From Eisenberg, 1962.)

Even in nocturnal rodents such as Rattus and Peromyscus visual acuity may be quite well developed (Munn, 1950; Lashley, 1932, 1938; Vestal, 1973). Grant, Mackintosh, and Lerwill (1970) offer evidence that the black chest patch in Mesocricetus displayed during the assumption of an upright posture may intimidate a conspecific. In follow-up experiments, Johnston (1973) has not been able to determine why or how the chest patch might function during agonistic encounters; he has questioned the interpretation of Grant et al., since postures involving the display of the patch during fights are normally shown by subordinate males. The white venter of many nocturnal rodents could also serve as a signal during the assumption of upright postures in a thwarting context. No doubt many of the markings or coat color patterns of various rodent species are also the result of predator selection and thus function either as cryptic patterns or during antipredator display and as such may be examples of interspecific communication (see Benson, 1933; Kaufman, 1974).

Fig. 2. Threat in Peromyscus maniculatus. Animal on the left shows expanded pinna and open mouth as he emits a threat squeak. The animal on the right is in an elongate posture with the ears slightly folded. (From Eisenberg, 1968.)

Surely in nocturnal and fossorial rodents or in rodents with reduced eyes, olfaction and audition must be the primary input channels for distance communication. Tactile and olfactory input become extremely important during encounters at close range, and the interaction patterns may well be considered as the establishment and maintenance of joints" in the manner outlined in the chapter by Eisenberg and Golani in this volume. The establishment of joints between partners can result in extremely stereotyped configurations and postures with a minimum of visual input.

Auditory Input and Perception

The study of the genesis of sounds produced by rodents is still in its early stages, but an excellent analysis for Cavia was recently completed (Arvola, 1974). Comparisons of audiograms for selected rodent species is much more advanced. It is clear that many rodent species show more than one sensitivity peak when cochlear microphonics are measured (Ralls, 1967; Brown, 1973), suggesting that certain frequencies are more important for survival than others. Whether optimum sensitivities are related to predator detection, prey detection, or the perception of conspecific signals remains to be investigated.

One consistent pattern that has emerged is that many muroid rodents (Peromyscus, Apodemus, Rattus, Mus) can perceive sounds well above the range of human hearing (> 18 Khz-<70 Khz; see Zippelius and Schleidt, 1956; Ralls, 1967; Price, 1970; Brown, 1973). On the other hand, many rodent species seem to have sensitivity ranges not too different from the human range (e.g., Cavia: Strother, 1967).

In addition, those rodent species with an enlarged mastoid bulla typically show a peak of maximum auditory sensitivity for rather low-frequency sounds (Webster, 1962), and the larger the relative bullar inflation, the greater the sensitivity to selected lower frequencies (Lay, 1972). Some species having slight bullar inflation retain a sensitivity peak for frequencies greater than 20 Khz (Brown, 1973), but those species exhibiting extreme bullar inflation appear to have maximum sensitivities for frequencies less than 20 Khz. This sensitivity shift is not correlated with a particular rodent taxon since it includes the caviomorph genus Chinchilla (Rothenberg and Davis, 1967); the muroid subfamily Gerbillinae (Lay, 1972), and the heteromyid genus Dipodomys (Strother, 1967; Webster, 1961, 1962).

For those species of rodents that show auditory sensitivity above 25 or 50 Khz, a number of important signal forms have been identified which are inaudible to humans and may be either inaudible to their mammalian predators or difficult to localize. The production of ultrasonic signals in muroid rodents was recently reviewed in Sewell (1970) and Sales (1972a, 1972b). Production of ultrasonic cries by young rodents displaced from the nest and/or handled has received the most attention to date (Mus, Rattus: Noirot, 1966, 1968; Mus, Rattus, Mesocricetus, Clethrionomys and Apodemus: Okon, 1970a, 1972; Peromyscus: Smith, 1972). Yet adult sounds in the ultrasonic range are receiving increasing attention (Barfield and Geyer, 1972; Sales, 1972a, 1972b; Whitney et al., 1973).

A wide variety of rodent sounds are produced with frequencies below 20 Khz. These include sounds produced mechanically by foot stamping, tooth chattering, or quill rattling. Unvoiced exhalations include hissing, while true vocalizations exhibit astonishing variety and forms of modulation. The form and function of vocalizations have been analyzed for Cavia (Arvola, 1974; Coulon, 1973); selected caviomorph rodents (Eisenberg, 1974); the lemming genera Dicrostonyx and Lemmus (Brooks and Banks, 1973; Arvola et al., 1962); Sciurus carolinensis (Horwich, 1972); Cynomys (Waring, 1970); Citellus ornatus (Balph and Balph, 1966); and Dipodomys, Perognathus, and Liomys (Eisenberg, 1963a).

Rodent species from diverse taxa produce sounds that are physically similar. These sounds are often associated with contexts similar enough to suggest behavioral homologies. For example, tooth chattering is widespread in the Rodentia and generally accompanies aggressive arousal and threat behavior. Low-intensity, repetitive calls may occur during courtship (Eisenberg, 1974). Calls may be produced by the male following ejaculation. In Rattus these calls are ultrasonic (Barfield and Geyer, 1972), while in Octodon, Octodontomys, and Myoprocta, they have audible components (see Kleiman, 1974; Eisenberg, 1974).

Fig. 3. Gradation of some syllable types in Cavia porcellus. The basic cluck (Type II syllable) can be uttered with a specific temporal patterning to yield the tut-tut or purr. Longer clucks (Type I syllable) may transform to short squeaks or loud wheets. Series C was produced by scratching a male on the neck and then on the groin. Series B was produced by a two-week-old juvenile exploring an open area but separated from the mother and siblings. Series A is an inflected squeak series produced by "grooming" the young around the neck. The ordinates are in 1 kHz increments; the abscissae are in 0-3 sec increments. (From Eisenberg, 1974.)

Many rodent species produce a graded series of calls which involve, on the one hand, emphasis on single frequencies to, on the other hand, emphasis on a wide range of frequencies that may approximate noise. Such a series of calls may reflect subtle changes in motivation from low-intensity arousal to extreme arousal with a high tendency to avoid a conspecific (for a discussion of Cavia, see Arvola, 1974; for Dicrostonyx, see Brooks and Banks, 1973). (See Fig. 3.) Graded series of vocalization forms that parallel motivational shifts in thwarting contexts have been described by Dunford (1970) for Tamias striatus and Coulon (1973) for Cavia.

The young of rodents born altricially generally have a stereotyped call given when they are displaced from the nest. In muroid rodents the call is generally in part or wholly ultrasonic (Sewell, 1970). On the other hand, precocially born rodents may produce short, audible contact notes that allow them to remain near or locate the mother when they are moving together (Eisenberg, 1974).

Sounds produced as part of a species' antipredator strategy often vary greatly in form and pitch (Marmota: Barash, 1973; Waring, 1966; Spermophilus: Melchior, 1971; Dasyprocta: Eisenberg, 1974; Lagidium: Eisenberg, 1974). These pitch differences may reflect different selective pressures, which have acted to produce calls audible at different distances in habitats differing in their efficiency of sound propagation (Eisenberg, 1974).

Finally, some rodent species appear to produce calls that are related to the establishment and maintenance of spacing and/or the attraction of sexual partners. These calls include the territorial calls of the North American red squirrels (Tamiasciurus: Smith, 1968) and the prairie dogs (Cynomys: Waring, 1970), and the "song" of Dinomys (Eisenberg, 1974).

Chemical Signals

In the early studies of rodent interaction patterns too little attention was paid to the role of olfaction in the coordination of social behavior. In an exhaustive analysis of filmed encounters of Mus musculus, Banks (1962) was unable to define any unique set of postures or movements which could reliably indicate that a bite with subsequent fighting would be delivered. Yet it is now known that an attack by one male mouse upon another is profoundly influenced by odor (Mackintosh and Grant, 1966). Olfactory communication in mammals has been the subject of several recent reviews (Ralls, 1971; Eisenberg and Kleiman, 1972;Johnson, 1973), and only a brief summary for rodents will be included in this section.

Chemical signals in rodents are derived from many sources. Vaginal secretions of Mesocricetus release sexual behavior in the male (Murphy, 1973). Specific glandular areas may be found in most rodent species, e.g., flank glands in Mesocricetus and Cricetus (Lipkow, 1954; Eibl-Eibesfeldt, 1953; Dieterlen, 1959), ventral glands in Meriones and Peromyscus (Thiessen et al., 1968; Doty and Kart, 1972), and supracaudal glands in Cavia (Martan, 1962). Urine, also a source of information, has been extensively studied in Mus, Peromyscus, and Rattus (see Mackintosh and Grant, 1966; Doty, 1973; Carr etal., 1965;Lydell and Doty, 1972).

Movements associated with the deposition of chemical traces may be more or less elaborate, depending upon the odor source. Flank marking and ventral gland marking are usually visually conspicuous acts while urine deposition on the substrate or even on a conspecific (which occurs while crawling over in Rattus) may go unnoticed by a human observer. Urine marking on a conspecific in most caviomorphs, however, is associated with elaborate postures (Kleiman, 1974). (See Fig. 4.) An unusual source of odor with associated marking movements has been described by Collins and Eisenberg (1972) in Dinomys. Eye gland secretions drain from the external nares onto the rhinarium, which is then rubbed on various points in the living space.

For many rodents both gland size and marking frequency are sexually dimorphic, the male exhibiting a larger gland and higher levels of marking (e.g., Mesocricetus: Vandenbergh, 1973; Meriones: Thiessen et al., 1968; Cavia: Martan, 1962).

Chemical signals function in a variety of ways. Godfrey (1958) demonstrated that male bank voles (Clethrionomys) could distinguish between the odor of their own subspecies and that of a closely related subspecies. The ability to select the appropriate species for mating may be critical in areas of sympatry. Moore (1965) demonstrated that Peromyscus maniculatus males discriminated between odors of maniculatus females and other species. Sympatric populations of P.eremicus and P. californicus also showed an ability to discriminate on the basis of odor (Smith, 1965). Recently Doty (1972) has shown that male urine alone can serve as an attractant to estrous females of P. maniculatus and that these females can discriminate between the odors of male P. maniculatus and P. leucopus, which occur in sympatry over a wide range of habitats. (For a full discussion, see Doty, 1972, 1973.) Thus sexual isolation in sympatric populations may be mediated by olfactory cues.

The sex of an individual can be discriminated on the basis of odor alone in Mus, Meriones , and Rattus (Bowers and Alexander, 1967; Dagg and Windsor, 1971; LeMagnen, 1952). Furthermore, the relative age of an individual may be assessed on the basis of odor since immature animals do not yet exhibit the hormone-dependent changes in glandular size and marking.

Fig. 4. Enurination (Harnspritzen) postures in some hystricomorph rodents, a. Myoprocta male, bipedal, b. Octodon male, tripedal. c. Cavia male, tripedal. d. Dolichotis male, bipedal, e. Cuniculus male, bipedal. (From Kleiman, 1974.)

Reproductive behavior is profoundly influenced by chemical signals. Some chemicals act almost as "releasers" in that normal sexual behavior will not proceed if they are absent or if the olfactory nerve function is impaired (Doty and Anisko, 1973; Heimer and Larsson, 1967). Other chemical substances act as "primers" since their effects are delayed. Chemical signals or pheromones that act as primers may in Mus inhibit pregnancy (Parkes and Bruce, 1962); induce estrus (Whitten, 1966); or advance puberty (Vandenbergh, 1967). The nature of these priming and releasing effects has only begun to be investigated, and considerable variation with respect to the nature and degree of these effects will no doubt be shown when the phenomena are compared over a range of species drawn from several families.

Several recent studies have shown that odors can indicate the mood of the animal, e.g., fear in Mus (Muller-Velten, 1966).

Tactile Input

Close-range behavior involves touching, grasping, opposing or locking incisors, allogrooming, and a host of other interaction forms. Olfaction is strongly involved in many forms of interaction involving tactile stimulation, and extremely stereotyped configurations can result during initial encounters between two conspecifics (see Eibl-Eibesfeldt, 1958, for a summary of his work; Eisenberg, 1962, 1968, for Peromyscus; Eisenberg, 1963a, 1963b, for the Heteromyidae; Kleiman, 1971, 1972, for Myoprocta; Steiner, 1970, 1971, for Spermophilus colombianus; Stanley, 1971, for Notomys; Horwich, 1972, for Sciurus; Koenig, 1960, for Glis glis; Ewer, 1971, for Rattus rattus; Wilsson, 1968, for Castor; Dieterlen, 1959, for Mesocricetus).

The extent to which tactile input can promote the assumption of specific postures has been experimentally analyzed only within the context of mating behavior. Because many species of rodents show a specific mating posture (lordosis) assumed by the female, the analysis of the stimuli necessary to induce lordosis has been the subject of some study. Females of Rattus and Cavia assume lordosis in response to the mounting of the male. The study of the stimuli necessary to induce lordosis in Mesocricetus indicates that olfactory and perhaps visual stimuli from the male increase the ease with which lordosis is elicited by tactile stimuli, but ultimately tactile stimuli are both sufficient and necessary to elicit lordosis in the female of Mesocricetus auratus (Murphy, 1974).

The ubiquity of allogrooming in the sexual and maternal behavior of rodents attests to its important role in promoting exchange of tactile stimuli. It is entirely possible that both gustatory and olfactory stimuli are perceived by the groomer; however, this complex of possible stimulus exchanges has not been analyzed to date.

EVOLUTIONARY TRENDS IN RODENT COMMUNICATION SYSTEMS

Auditory Communication and Predator Detection in Nocturnal Desert Rodents

An anatomical peculiarity shared by many arid-adapted, nocturnal rodents is the presence of an inflated middle ear cavity (Howell, 1932). Externally this anatomical peculiarity is reflected in the expansion of the mastoid bulla. Extreme inflation of the mastoid bulla is occasionally accompanied by an enlargement of the external ear (Ognev, 1959), but often in those species having the largest bullae, the pinna is small (e.g., Dipodomys and Microdipodops) . Some species of nocturnal desert rodents show little bullar expansion but extremely hypertrophied pinnae (e.g., Alactaga and Euchoreutes) . For these species it is assumed that the large pinna increases sensitivity to low-amplitude sounds by focusing sound energy at the meatus. The propagation of sound in desert air involves considerable energy loss, especially at frequencies > 10 Khz (Knudsen, 1931, 1935). The resulting signal attenuation may have necessitated the evolution of anatomical adaptations to increase sensitivity to low-amplitude sounds. Pinna enlargement is one way, bullar inflation another.

The expanded middle ear cavity has been correlated with structural modifications in the cochlea; and the most extreme cochlear modifications are found in those species exhibiting the greatest bullar inflation (Pye, 1965; Lay, 1972). Generally speaking, those species from the most arid habitat with the least vegetational cover show the greatest bullar expansion (Petter, 1961). Indeed, a whole range of bullar expansions can be demonstrated within a single genus such as Meriones (Lay, 1972), and environmental correlates with respect to aridity and ground cover can be made.

One outstanding acoustical feature of the rodents possessing an expanded bulla is the enhanced sensitivity for low-frequency sounds (less than 2 Khz). Wisner et al. (1954) and Legouix et al. (1954) hypothesized that the sensitivity of hearing was maximized toward values near the resonant frequencies of the ossicles. Lay (1972) demonstrated for a series of gerbilline rodents that a shift in auditory sensitivity for lower frequencies parallels increased bullar expansion. Webster (1960, 1962) demonstrated for Dipodomys that not only does the inflated tympanic bulla maintain sensitivity for low-frequency sounds, but, furthermore such sounds are often generated by the predators themselves, e.g., snake movement or the wing beats of owls. Webster went on to show that the ability to avoid the strike of a snake on the part of Dipodomys was dependent on intact mastoid bullae (Webster,1962).

Petter (1961) felt that the inflated mastoid bullae of desert rodents could enhance their sensitivity for the low-frequency sounds produced during various aspects of intraspecific communication. In particular he noted the ubiquity of foot stamping or drumming as a mode of signaling in desert rodents. He further noted that the largest tympanic bullae occurred in those species most strongly adapted to extremely arid habitats and thus living at very low densities where the carrying capacity is understandably low.

Sparse cover, low carrying capacity, and enforced foraging for seeds in open areas all intercorrelate. Webster would argue that predator selection is primarily responsible for the inflated mastoid bullae and the resulting shift in auditory sensitivity. Lay (1972) agrees in general with Webster's hypothesis. Both workers cite reports indicating that paradoxically many vocal sounds of gerbillines and Dipodomys are high pitched.

While it is agreed that predator selection may be decisive in the evolution of the expanded middle ear cavities of nocturnal, arid-adapted rodents, selection may have also acted on the sound-producing mechanisms of these species to produce call forms that must function over a considerable distance and that furthermore emphasize frequencies to which this auditory apparatus is maximally sensitive. Close-range sounds during fighting, sexual behavior, or distress might not be under such selective constraints, but the cry of a displaced young could be so modified. Thus, any similarities in syllable structure or pitch of the young animal's calls could be the result of evolutionary convergence.

In a detailed study of the family Heteromyidae (Eisenberg, 1963b) it was noted that young kangaroo rats when displaced from the nest do not emit ultrasonic pulses but instead emit a repetitive buzzy sound that emphasizes low frequencies. The threat growl of adult Dipodomys nitratoides also emphasizes frequencies <2 Khz. Recently Owings and Irvine (1974) have replicated these observations with Dipodomys merriami. In a recent review (Eisenberg, 1975) the comparison of "abandoned cries" for a series of young nocturnal desert rodents suggested that the overall pitch may conform to the optimum sensitivity of the adult cochlea. Thus, a gerbilline such as Tatera indica exhibiting little bullar inflation has neonate young that give calls with energy at 4 to 6 Khz, while Meriones hurrianae with a larger tympanic bulla has an abandoned cry pitched from 2 to 3 Khz. At the other extreme the young of D. nitratoides and D. merriami call with energy less than 2.5 Khz.

In conclusion, then, it would appear that the restrictions of open, arid environments favor selection for enhanced sensitivity to low-frequency sounds on the part of nocturnal rodents. That predators have been the primary selective force is undoubtedly true; however, it would seem reasonable to assume that certain classes of auditory signals (e.g., cry of the displaced young) have undergone selection to exhibit a pitch conforming to the optimal sensitivity of the adult cochlea.

Sandbathing as a Form of Chemical Marking

The development of increased secretory activity in the sebaceous glands associated with the hair follicles of arid-adapted rodent species is a widespread phenomenon (Sokolov, 1962). In addition, many species have evolved specialized gland fields on the ventrum (Gerbillus and Meriones) or mid-dorsal region (Dipodomys) in addition to the classical glandular areas of the anogenital region (see Quay, 1953; Fiedler, 1974). The sebaceous glands associated with the hair follicles act as epidermal lubricants to reduce drying of the skin. The pelage will generally become quite oily if excess depositions of sebum are not removed through dust bathing. Obviously chemical substances in the sebum as well as depositions from other skin glands and even urine at sandbathing loci could serve in chemical communication (Eisenberg, 1963a and 1963b). Rodents from diverse families adapted to arid habitats show sandbathing behavior, including the Gerbillinae (Fiedler, 1974); the Heteromyidae (Eisenberg, 1963a), the Dipodidae (Eisenberg, 1967), and several genera of caviomorph species, including Chinchilla, Octodon, Octodontomys, and Pediolagus (Wilson and Kleiman, 1974). (See Fig. 5.)

Although the movement patterns in sandbathing may vary widely from one genus to another in a species-specific manner (Eisenberg, 1967), all species tend to sandbathe at specific loci and these same spots are utilized by conspecifics ranging within the same living space. The potential for communicating by chemical signals by means of such sandbathing spots is strongly implicated (Eisenberg, 1967). Such spots may be used by species living in family groups (e.g., Pediolagus) as a means by which group odor can be maintained through successive use by all colony members (Kleiman, 1974). Indeed, a class of play movements called "locomotor-rotational movements" are released by conspecific odors. Such odors may be exchanged either while sniffing a partner or while sniffing a sandbathing spot (Wilson and Kleiman, 1974); the arid-adapted forms (e.g., Pediolagus and Octodontomys) exhibit locomotorrotational movements more often in response to sniffing sandbathing loci.

Fig. 5. Dipodomys sandbathing. a. Flexion of the body followed by b. extension in performing the ventral-rubbing component, c. Side rubbing by extending with the side pressed into the substrate. (From Eisenberg, 1963a.)

Differences in the patterns of rubbing, extension, and flexion as well as differences in the specific body areas rubbed in sand are to be found when a series of species are compared (Eisenberg, 1967). Chemical marking and pelage dressing appear to have been combined into a single movement complex in many desertadapted species, although pure marking movements may be retained without a necessary pelage dressing function. Comparative studies strongly suggest that pelage dressing movements in the form of sandbathing have evolved independently within several lines of rodent evolutionary descent and that such patterns should be considered examples of convergent behavioral evolution.

Visual Signals and Diurnality

In the evolution of diurnality in the Rodentia, several types of movement patterns have evolved that imply visual communication. The tail movements of the diurnal, arboreal sciurids, often accompanied by vocalizations, could serve to accentuate the position of the sender as well as to communicate varying degrees of arousal to a potential receiver (Bakken, 1959; Horwich, 1972). In the aggressive acouchi, piloerection of the rump hair serves a similar function (Fig. 6).

In some diurnal caviomorphs, e.g., the acouchi (Myoprocta pratti), tail wagging combined with body trembling and alternate stepping movements of the forefeet are important components of courtship which may indicate the approach-withdrawal tendencies of the courting male (Kleiman, 1971, 1974). Such tail and body movements are reminiscent of similar movements by diurnal ungulates, e.g., the Uganda kob (Adenota kob: Buechnerand Schloeth, 1965) during courtship, and some diurnal macropods, e.g., the whiptail wallaby (Macropus parryi: Kaufmann, 1974), and have probably evolved from intention locomotor movements (Andrew, 1972). The stereotypy of such displays in diurnal caviomorphs, macropods, and ungulates is probably the result of evolutionary convergence resulting from a similarity in selective pressures within the three groups. Other convergences in morphology and behavior can be discerned when the forest-adapted cursorial caviomorphs (Dasyprocta, Myoprocta, and Cuniculus ) are compared with their ungulate counterparts in the Old World tropical forests (Dubost, 1968; Eisenberg and McKay, 1974).

Fig. 6. Piloerection in Myoprocta pratti. Erection of the rump hair is a ritualized aspect of aggressive behavior in the acouchi. Note that the apparent size of the animal is exaggerated. (From Kleiman, 1972.)

During the course of the evolution of steppeadapted cursorial caviomorphs, such as Dolichotis, a striking form of antipredator behavior has evolved, which bears a strong resemblance to similar patterns shown by the smaller antelope genera of East Africa. The pattern involves a peculiar gait, "stotting," which serves to display the white rump markings prominently. Such a signal pattern could serve to induce a predator to launch a futile attack because the display is always given when the sender is well outside the normal attack range of the predator. At the same time the signal appears to alert mates or young of the predator's presence in the living space (for a full discussion, see Smythe, 1971). Similar movements are also employed during the play of certain caviomorphs (Kleiman, 1974; Wilson and Kleiman, 1974).

Conspicuous movement patterns are involved in the challenge and territorial defense of the colonial prairie dog (Cynomys ludovicianus:King, 1955; Smith et al., 1973). The territorial call is given during the course of a complicated movement sequence when the caller "throws its body upwards and rises on its hind legs with nose pointed straight up and with forefeet thrust out from the body, and then returns to its normal quadrupedal position" (King, 1955). In this classical description, a vocalization and a stereotyped movement sequence are combined in a single display.

The preceding examples of movement patterns shown by diurnal rodents suggest that information is transferred via the eye of the presumptive receiver. Yet the experimental analysis of the exact role of such movement patterns in the transfer of information has lagged behind the original descriptions. Auditory signals often accompany stereotyped movements, which suggests that the presumptive signal can often not be reduced to a single physical component. For the nocturnal rodents visual signals probably play a much reduced role in the information transfer system.

The Antipredator Calls of Colonial Rodents

One of the more conspicuous examples of convergent behavioral evolution in the Rodentia is the development of specific vocalizations that are emitted by colonial rodents either when a potential predator is perceived or when the subjects are disturbed by a novel stimulus input. This behavioral phenomenon is typical of rodents that live in rather open habitats where the predator can be kept in view by the calling animal; however, similar warning calls or sounds have been evolved by species in forested habitats. During responses to a mobile predator, the calls of the latter are often not repetitive but rather are given before or during a directed flight from the predator (Eisenberg and McKay, 1974). These forms of antipredator strategy are not confined to rodents but have evolved convergently in ungulates, lagomorphs, primates, and some small carnivores. The specific form and pitch of the call apparently involve a complex of factors including the size of the species, the vocal apparatus, and those physical features of the habitat that affect sound propagation (Eisenberg, 1974).

The evolutionary adaptations leading to coloniality and ultimately to the formation of communal groups defending a group territory in diurnal rodents have been reviewed by Barash (1973, 1974) for the genus Marmota. The use of warning calls as an antipredator strategy has been described for Marmota olympus, M. caligata, and M. flaviventris (Barash, 1973; Waring, 1966; Armitage, 1962). Convergent trends have been noted for Cynomys (King, 1955; Waring, 1970) and Spermophilus (Balph and Balph, 1966). Within the colonial Caviomorpha, similar calls have been noted for Lagidium (Pearson, 1948), Spalacopus (Reig, 1970), Ctenomys (Pearson, 1959), and Lagostomus (Hudson, 1872).

Specific distinctiveness exists when calls are compared from one species to the next, but the ecological sources of such variations have not been explored. These kinds of adaptive aspects in the varying forms of "warning cries" in colonial rodents will surely prove to be rewarding areas of study for future students of rodent communication.

CONCLUSIONS

It is evident from the preceding discussion that the rodents display significant diversity in their communication systems. The basis for the diversity can be found in the variety of habitats and niches to which members of this order have become adapted. We did not attempt initially to outline the natural history of selected species since such an approach would have necessitated another chapter to deal with an order containing so many species. However, it must be emphasized that the analysis of communication can yield biologically significant results only if a study is conceived and executed with regard to a species' natural history. That this has not always been done in the past is evidenced by the fact that the first complete natural history study of the Norway rat appeared in 1962 (Calhoun, 1962), and Ewer (1971) has only recently published on Rattus rattus. Guinea pig research has flourished since the early part of this century, but the ecology and social behavior of Cavia and related genera were ignored until Rood published in 1972. There is, as yet, no detailed study of the natural history of Meriones unguiculatus, although the gerbil is being used increasingly in research on communication. Experimental analysis of a species' communication system must proceed in step with field research dealing with the adaptive nature of the behavioral repertoire. It is heartening to note that this unified approach is now under way.

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