Chemical signals exchanged between members of the same species are known as pheromones Greek pherein, to carry, and hormon, to excite.. When researchers added extracts of male lipids to
Trang 1C H A P T E R 1 2
Intraspecific Behavior and Ecology
Very few animals are not, at one time or another, “social.”
While the social nature of schools of fish, flocks of migrating
geese, and herds of African big game animals is obvious, one
might hesitate to use the word “social” to describe the
intri-cate interaction between the members of a breeding pair or
between parents and offspring Likewise, the fighting between
rival males in the spring might at first glance seem to deserve
the epithet “antisocial” rather than “social.” The complex
interactions of individuals with kin groups such as Florida
scrub jays (Aphelocoma coerulescens) is much different from the
way individuals of non-kin groups, such as a flock of gulls,
interact Yet all of these interactions have a great deal in
com-mon; all contribute to the success of the species and all depend
on communication—albeit through many different
meth-ods—between individuals In short, social behavior—the joint
activities that make an animal community function—depends
on various types of interactions among individuals, each
play-ing its part in communication with others
The terms for groups of vertebrates are listed in
Appen-dix II Many have their origins quite far back in history;
some descend from the hunting royalty of England, France,
and Germany
Social animals do much more than merely stay together They
do things together; the activities of all members are jointly
timed and oriented, and they do this, too, by influencing
each other A family of ducklings, for example, goes through
a common diurnal rhythm Part of the day they feed,
keep-ing close together wherever they go On other occasions, they
bathe together and swim to the shore together, where they
may spend half an hour or so preening, standing next to each
other Then they fall asleep, side by side
Even while sleeping, ducks and many other birds continue
to interact Half-brain sleep—one cerebral hemisphere alert
and the other asleep—has been documented in a wide range
of birds and is thought to have evolved as a form of predator detection Rattenborg et al (1999) filmed rows of napping
mallard ducks (Anas platyrhynchos) The end birds tended to
keep open the eye on the side away from the other birds Researchers found outer birds resorting to single-hemisphere sleep rather than total relaxation during 32 percent of nap-ping time versus 12 percent for birds in internal spots, an increase of more than 150 percent Furthermore, birds at the edge position oriented the open eye away from the group’s center 86 percent of the time, whereas birds in the central position showed no preference for gaze direction This study
is believed to be the first evidence for an animal behaviorally controlling sleep and wakefulness simultaneously in different regions of the brain
On many occasions, there is a division of labor among members of a group Members of a flock of Canada geese take turns leading the V-shaped formation when migrating
Old, experienced chimpanzees (Pan) lead the group and keep
a sharp lookout at all times Perhaps the most extreme social hierarchy known among mammals occurs in naked mole rats There is also division of labor in more solitary animals, particularly between male and female This applies both to different roles in mating and to different parental activities Numerous examples of such division of labor in all verte-brate groups have been discussed in Chapters 5 through 9 Social interactions may be beneficial in many ways It has been estimated that 25 percent of all fishes school through-out their lives, and abthrough-out half of all fishes spend at least part
of their lives in schools (Moyle and Cech, 1996) Schooling can reduce the risk of predation, increase reproductive suc-cess, and in some cases, increase the efficiency of finding food for fishes and many marine animals For example, groups of dolphins and porpoises aid wounded members of their own species, raising them to the surface so they can breathe They also circle a female giving birth in order to pro-tect the mother and newborn against sharks
Mobbing behavior, in which one to a few individuals approach and often chase and/or attack a potential predator, is common in birds The primary purpose of mobbing is to force the predator to move on (Curio, 1978; Curio et al., 1978a, b)
Trang 2Clearly, no sexually reproducing species could exist
with-out intricate cooperation between male and female for the
purpose of mating This period of interaction may last only
long enough for fertilization to occur, or it may result in a
lifetime bond Many marine fishes simply discharge their
gametes into the surrounding water Most do this in response
to an environmental stimulus that induces the synchronized
release of gametes by both sexes This simple mode of
repro-duction ensures fertilization, genetic recombination in
off-spring, and hence, variation in the population
Species in which young receive parental care need close
cooperation between parents and young Mated pairs are
usu-ally more successful at raising offspring than a single animal
working alone Each member of a pair can share in food
gath-ering, defending the territory, and protecting its mate and young
from predators Protection is even more effective when a group
faces a potential predator For example, gulls in a breeding
colony attack predators in force This concerted defense, quickly
mounted as the birds alert each other by alarm calls, is much
more successful than individual attacks This response is elicited
not just because the gulls nest close together, but also because
they nest synchronously and will benefit almost equally
Like-wise, many mammals, such as musk-ox and elephants, band
together to protect their young from potential predators
Social hierarchies occur in many groups of animals In
some, the female is dominant—a matriarchal hierarchy; in
others, the male is dominant—a patriarchal hierarchy The
dominant individual is usually an older member of the group
and controls activities until challenged and deposed by a
younger rival Classic studies of peck-orders in chickens have
clearly demonstrated the nature of the dominant–subordinate
behavior Similar studies have been carried out on a variety
of other vertebrates Within a clan of spotted hyenas (Crocuta
crocuta), for example, the highest-ranking female and her
descendants are dominant over all other animals (Nowak, 1991) Although all resident males court females, only the highest-ranking male was observed mating in a study by Frank (1986b) Dominant individuals in non-kin groups, such as flocks of sparrows, have been shown to gain access
to better food sources and suffer lower risks of predation than
do subordinate individuals Thus, the value of social behav-ior accrues to a greater extent among dominant individuals than it does among subordinate individuals
Some species of birds, such as white-fronted bee-eaters
(Merops bullockoides) of Africa, are cooperative breeders
(Emlen and Wrege, 1992) They live in colonies averaging
200 individuals making up several clans Young females remain in their parental group (clan) for 1 or 2 years until they begin to breed, at which time they leave their parents and join the clan of their mates Males, however, do not leave their clans Each clan establishes its own feeding territory, but all individuals of each clan roost and nest at the colony site Not all intraspecific interactions are peaceful Competition
in many birds, for example, begins in the nest as individuals compete for food and space Intraspecific competition, whether for a mate, food, or territory, however, rarely results
in injury to the participants Most species have ritualized aggressive behaviors that are used in these situations Many fishes engage in tail-beating, mouth-pulling, or mouth-pushing
activities Red-backed salamanders (Plethodon cinereus) raise
their trunks off the substratum and look toward their opponent (Fig 12.1a) A biting lunge directed toward the opponent’s tail or nasolabial groove area may follow Frogs attempt to topple intruders that come into their territory (Fig 12.1b) Rattlesnakes wrap their bodies around each other and butt each other with their heads Some lizards whip each other
BIO-NOTE 12.1
Mole Rat Societies
Naked mole rats (Heterocephalus glaber), which exhibit
eusociality or “true sociality,” usually live in colonies of 75
to 80 animals, although colonies of more than 250 animals
have been recorded Most colonies contain only a single
reproductive female (see Fig 11.3) Chores are performed
by both males and females, but not by all individuals
equally For example, the primary role of the breeding
female is to produce young, nourish the pups, and keep
them clean Nonbreeders help to clean and carry pups and
also to maintain and defend the colony’s tunnel system
Labor is divided according to size Large nonbreeders
defend their colony against mole rats from other colonies
and also against predators
Dominance hierarchies exist within colonies: The
queen and breeding males dominate the nonbreeders; larger
workers dominate smaller ones, regardless of sex
Chemical, tactile, and acoustic forms of
communica-tion are used At least 17 distinct categories of vocalizacommunica-tions
have been recorded, with the vocal repertoire being the
most extensive known among rodents
Naked mole rats, which are ectothermic, are the only known mammals whose body temperature fluctuates with the ambient temperature The temperature within their tunnels remains near 30°C most of the year If the animals get colder, they regulate their temperature by huddling with colony mates (social endothermy, like bees)
Inbreeding is a constant problem in such highly orga-nized societies Recently, a dispersal phenotype was discov-ered that may occasionally promote outbreeding These dispersers are morphologically, physiologically, and behav-iorally different from other colony members These rare morphs are fatter than average, have higher than normal levels of luteinizing hormone, have a strong urge to dis-perse, and will mate only with noncolony members
Although rare, they are essential in producing the gene flow that maintains the heterogenicity required for reproductive compatibility between isolated populations
Sherman et al., 1992 O’Riain et al., 1996
Trang 3A B
(a)
FIGURE 12.1
Male Masai giraffes (Giraffa camelopardalis) sparring for social
domi-nance Such bouts are primarily symbolic and rarely result in injury. FIGURE 12.2
(a) Red-backed salamander (Plethodon cinereus) escalating the intensity
(A–F) of its threat display toward an intruder (b) Male bullfrogs (Rana
catesbeiana) aggressively defend territories used as egg deposition sites;
fights are typically wrestling matches in which the larger male prevails.
Source: (a) After Jaeger and Schwartz, 1991, Journal of Herpetology in
Stebbins and Cohen, A Natural History of Amphibians, 1995, Princeton
University Press.
with their tails Turkeys drive off their rivals by means of
threatening calls and/or by jumping at them Giraffes, deer,
elk, and bighorn sheep butt each other with their heads (Figs
12.2 and 12.3) Brown bears may charge, growl, and push one
another with their forelegs Oryx antelope possess
sharp-pointed horns with which they stab potential predators such
as lions, but when faced with a conspecific adversary, they
merely butt heads and do not attempt to stab each other
In spotted hyenas (Crocuta crocuta), sibling rivalry is
car-ried to a deadly extreme Females generally give birth to twins
in underground dens Sibling fighting begins at the earliest
possible moment, sometimes while the second pup is still in
the amniotic sac This instant antagonism lets the pups
estab-lish a ranking order that determines which one gets the most
of a limited food supply: their mother’s milk The dominant
animal generally grows larger and has a better chance of
suc-ceeding in the dangerous adult world The loser often dies
Female twins fight the hardest and longest—probably
FIGURE 12.3
Butting bouts among desert bighorn sheep (Ovis canadensis) appear to
be contests of skill and stamina with little real antagonism involved It has nothing to do with the pre-mating collection and maintenance of a
“harem,” nor does it seem to result in the elimination of one ram from participation in mating activity with a certain ewe It appears to have
no objective whatever except the satisfaction of some deep-seated urge aroused by the mating instinct and demanding and receiving an outlet for its own sake When males are 12 feet apart, with every muscle bulging for a final effort, and with amazing timing and accuracy, they lunge forward like football tackles The remarkable synchronization of movement pictured here is the rule, not the exception Every effort seems to be made to ensure a perfect head-on and balanced contact Note that both heads are tilted to the same side Occasionally, one slips or miscalculates and a severe neck-twisting or nose-smashing results The combined speed at impact has been estimated at 50 to 70 miles per hour and to be the equivalent of a 2,400-pound blow More than 40 blows between two rams have been counted in one afternoon.
(b)
Trang 4Male African elephant (Loxodonta africana) showing the temporal
gland and its secretion The glands exude a dark, strong-smelling, oily substance that stains much of the lower part of the face.
FIGURE 12.4
because large size is favored if a female is to give birth to
healthy pups of her own Battles between male–female twins
usually are not as intense (Frank et al., 1991)
Animals show submission in various ways Some fishes
collapse their fins and change coloration Bullfrogs (Rana
catesbeiana) that maintain a low position in the water are not
challenged or attacked Iguanas flatten themselves to appear
as small as possible Many canids flatten their bodies and
bring their ears to lie flat against their heads The tails often
will be tucked between their legs
BIO-NOTE 12.2
Intraspecific Parasitism
Although parasitism usually is considered an interspecies
interaction, intraspecific brood parasitism occurs in a
large number of bird species in which females lay eggs in
the nests of conspecifics, who then provide parental care
Females without nests, as well as those with viable nests,
engage in brood parasitism In several species, parasitic
eggs have been found to be less successful than
nonpara-sitic eggs Many paranonpara-sitic females are young birds of poor
competitive ability Some lay eggs in the nests of other
females before laying eggs in their own nests
The addition of parasitic eggs to those already in a
nest may result in more young than the host parents can
rear successfully This may lead to reduced incubation
efficiency and overcrowding Antiparasite behaviors
include nest guarding, aggression, ejection of eggs, and
nest desertion
Petrie and Moller, 1991
COMMUNICATION
For effective organization to exist within a population that
maintains a social structure such as a family group, school,
flock, or herd, some form of unambiguous communication
must exist among the members of that population This
exchange of information influences the behavior of both the
sender and the recipient In general, those forms that live in
social groups have the more highly developed sets of
com-munication signals However, even in solitary or unsocial
ani-mals, elaborate signals may be required to establish and
maintain the species’ dispersed spatial patterns (Bradbury
and Vehrencamp, 1998)
Sensory reception and communication among
verte-brates are accomplished in a variety of ways They may use
pheromones, sound, vision, tactile stimulation, electrical
sig-nals, signal patches, or a particular behavior such as the
slap-ping of the tail (beaver) on the surface of the water or
foot-drumming (kangaroo rats)
Olfaction
Olfactory communication is widespread among vertebrates and may be the primary mode of communication for many species Chemical signals exchanged between members of the same
species are known as pheromones (Greek pherein, to carry, and
hormon, to excite) They control a wide variety of behaviors and
physiological states and may be detected from considerable dis-tances during both day and night Normal, or nonpheromonal,
chemoreception influences behavior Both pheromonal and
non-pheromonal chemoreception are important means of commu-nication Olfactory communication is effective beneath the surface of the ground and in dense vegetation, both areas where visual and auditory signals would be difficult to detect Pheromones may contain steroid or steroidlike organic compounds, which may be part of a mixture of compounds
Castoreum from the castor sacs of beaver (Castor canadensis),
for example, consists of 6 alcohols, 14 phenols, 1 aldehyde,
15 amines, 6 ketones, 9 aromatic acids, and 5 esters (Müller-Schwarze and Houlihan, 1991) A total of 37 compounds have been identified from the temporal gland secretion of the
Asian elephant (Elephas maximus) (Rasmussen et al., 1990).
This gland, located in the mid-cheek region, is a modified apocrine sweat gland and has been implicated in chemical
communication of African (Loxodonta africana) as well as
Asian elephants Secretions occur only during the
physiologi-cal state of musth, the strange emotional state that periodiphysiologi-cally afflicts all male and some female elephants Musth (a state of
increased serum testosterone) occurs after elephants reach maturity and is accompanied by great activity of the tempo-ral glands The temples become puffy, and the glands exude
a dark, strong-smelling, oily substance that stains much of the
lower part of the face (Fig 12.4) Elephants in musth either
become highly excitable or dull and morose
Trang 5This male cheetah (Acinonyx) is spraying a pheromone onto a tree in
order to mark his territory Scent marking is a well-recognized and important aspect of mammalian communication.
FIGURE 12.5
Biological activity of several compounds of a mixture
may interact in synergistic, redundant, or addictive fashion
In some cases, individual components of a mixture are
inac-tive, but when combined or dissolved in a fluid such as urine,
they become effective olfactory signals
Pheromones may represent a primitive communication
technique They may serve to attract members of the same
species, including a mate; they may elicit courtship
behav-ior; they may stimulate ovulation; they may serve as a
warn-ing when used to mark the boundaries of a territory; they may
be used for defensive purposes; or, in some cases, they may
indicate danger
Among fishes, pheromones are important in species, like
catfishes, that lack keen eyesight By means of pheromones,
migrating salmon may be able to discriminate members of
their own population from individuals of other populations,
thus permitting increased precision in their homing
Some salamanders can distinguish between odors
pro-duced by conspecifics and heterospecifics and distinguish
between odors of familiar and nonfamiliar conspecifics
(Mathis, 1990) Pheromones, which may also convey
infor-mation about gender, are used by many salamanders to
mark their territories The nasolabial grooves of
pletho-dontid salamanders serve as specialized channels to
trans-mit chemicals, such as pheromones, to the vomeronasal
organs (see Fig 6.27)
During the breeding season, the glands of some turtles
enlarge and are thought to secrete pheromones Many lizards
and snakes use pheromones for species and sex recognition
as well as the recognition of eggs Some, such as male
broad-headed skinks (Eumeces laticeps), have been shown to follow
female conspecific odor trails (Cooper and Vitt, 1986)
Chemical trailing of conspecifics occurs widely in snakes
Skin lipids extracted from female red-sided garter snakes
(Thamnophis sirtalis parietalis) are attractive to sexually active
courting males (see Fig 8.29) The lipids contained a female
sex attractiveness pheromone consisting of a series of
non-volatile long-chain methyl ketones (Mason et al., 1989)
When researchers added extracts of male lipids to female
extracts, male courtship stopped, suggesting that males emit
specific chemical cues that identify them as males One
chemical in the male lipid—squalene—caused a significant
drop in courting and is an important part of the male sex
recognition pheromone Preliminary studies of related groups
of snakes suggest that some of the same methyl ketones are
found in females of several species
Pheromones are well developed in mammals, especially
those with the keenest senses of smell Scent marking is a
well-recognized and important aspect of mammalian
com-munication and has been observed in a variety of mammals
(Fig 12.5) Glandular secretions and urine are used as the
principal means of chemical communication Estrous female
mole rats (Spalax ehrenbergi) are known to be attracted to
sub-stances in adult male urine Menzies et al (1992) reported the
extraction of sexual pheromones from lipids and other fractions
of the urine Male meadow voles (Microtus pennsylvanicus) emit
odors that are attractive to females at the beginning, but not
at the end, of the breeding season (Ferkin et al., 1992) Some mammals can differentiate between individuals on the basis
of odor Female house mice (Mus musculus), for example, use
smell to recognize related females (Manning et al., 1992) The similarity in smell results from related females sharing genes of the major histocompatability complex (MHC), which is involved in fighting disease In addition, if recently mated female mice are exposed to the urine or pheromones
of strange males before implantation, pregnancy block occurs and pregnancy fails (Brennan et al., 1990)
In black-tailed deer (Odocoileus hemionus), secretions from
four glands are considered important in social communication (Müller-Schwarze, 1971) (Fig 12.6) The scent of the tarsal
3a
4 5
3a 2a
2b
1
3c
3c
6 6
4 2 1 FIGURE 12.6
Pathways of social odors in black-tailed deer (Odocoileus hemionus).
Scents of the tarsal organ (1), metatarsal gland (2a), tail (4), and urine (5) are transmitted through air When the deer is reclining, the metatarsal gland touches the ground (2b) The deer rubs its hind leg over its forehead (3a) Marked twigs are sniffed and licked (3c) Inter-digital glands leave scent on the ground (6).
Trang 6gland identifies the age and sex of an individual at close
range The scent from the metatarsal gland acts like an alarm
pheromone over moderate distances The scent of the
fore-head glands is left on branches when a deer rubs its fore-head and
serves to mark the home range Scent from the interdigital
glands, which also is used in marking the home range, is left
on the ground
Flehmen is a reaction of some mammals to direct
physical contact with a scent mark and its incorporated
pheromones (Pough et al., 1996) After sniffing the scent
mark, the animal licks it and takes it into its mouth The
upper lip curls, the jaws open, and the head is raised and
turned from side to side or is nodded up and down The
ani-mal inhales deeply to move the scent into the vomeronasal
organ Flehmen occurs during the breeding season and is
characteristic of many ungulates, especially members of the
deer family (Cervidae) It is also known to occur in some
cats (Felidae)
Glandular secretions may be deposited on the substrate
or on objects in the environment; they may be applied to
the animal’s own body or to the bodies of other members
of the social group; or they may be released into the air
Feces and/or urine often contain pheromonal secretions
Koalas (Phascolarctos cinereus) and other marsupials use
sternal glands, paracloacal glands, and urine for marking
Trees are marked by koalas as they climb, by rubbing their
sternum on the tree Mitchell (1991a) noted: “Although
koalas produce scent and inspect their environment for
scent, there was no direct evidence that they used scent to
define space, recognize individuals or recognize
physio-logical states.” Whole-body and pouch gland odors are
important chemical signals between young Virginia
opos-sums (Didelphis virginiana) and their mothers just prior to
weaning (Holmes, 1992)
Some pheromones signal the presence of danger Some
wounded fishes release a substance from special cells in the
epidermis, which induces other members of the school to
flee for shelter Similar effects have been recorded in
amphibian tadpoles (Eibl-Eibesfeldt, 1949; Kulzer, 1954)
and in mice (Heintz, 1954) Chemical signals also have been
shown to facilitate schooling of young fish (Kuhme, 1964)
Some pheromones are very similar in structure to sex
steroid hormones that are used to attract the opposite sex
Humans secrete pheromones, but most humans continually
remove the real musks by bathing and then apply scented
ani-mal musks (perfumes) as a substitute The symbolic message
is still communicated, and the opposite sex still responds
The morphology and chemistry of scent glands and
the role of pheromones in mammalian social
communica-tion have been discussed in Brown and Macdonald (1985)
and Gorman and Trowbridge (1989) The influence of
selective factors such as substrate, persistence, intensity,
and localizability on the signal structure in mammalian
chemical communication systems has been reviewed by
Alberts (1992)
Sound
The production and reception of sound is most highly devel-oped in anurans, birds, bats, primates, and cetaceans Many fishes, including grunters and croakers, produce sounds by contracting muscles attached to their swim bladders Other fishes produce sounds by grinding their teeth or rubbing the base of a fin spine against the socket
Sound production is limited in salamanders and caecil-ians, but auditory commmunication is highly developed in male anurans, particularly during the breeding season Many males possess vocal sacs that serve as resonating chambers The purpose of most anuran calls is to advertise for mating
or to maintain territories or interindividual distances Male
gray tree frogs (Hyla versicolor) with long calls—known to be
favored by females—sire higher quality young than those with short calls (Welch et al., 1998) For two years, researchers compared how the offspring fared as tadpoles and after they metamorphosed into frogs, measuring their growth rates under regimes of scarce and plentiful food Offspring of males with long calls always performed significantly better than or not significantly differently from offspring of males with short
calls Because female H versicolor do not gain direct benefits
from their choice of mate, the indirect genetic benefits sug-gest good-genes selection as a probable explanation for the evolution and maintenance of the female preference in this species Among reptiles, vocal cords are present only in a few lizards, such as geckos (Hildebrand, 1995)
Males of many species of birds have highly characteris-tic territorial songs announcing that the resident is a sexu-ally mature male attempting to attract a suitable mate and defend an area against other males of the same species Birds possess a unique modification of the lower trachea, the syrinx Contraction of muscles attached to membranes within the syrinx produces the characteristic songs and calls of each species, which usually are heard most often during the breed-ing season Individuality is common Extensive studies on a variety of species show that songs differ among individuals
in pitch, speed, and details of phrasing In addition to their
voices, some birds, such as ruffed grouse (Bonasa umbellus),
also communicate by vigorously moving their wings back and forth, creating a drumming sound
Young birds are predisposed to learn a specific kind of vocal information Their learning pathways are highly selective and very sensitive to the “right” information (Adler, 1996b) For example, young male white-crowned
sparrows (Zonotrichia leucophrys) and white-throated spar-rows (Z albicollis) possess a neural template that allows
them to repeat the songs from males of their species If the young bird does not receive this information during a crit-ical song-learning period, it will not develop a typcrit-ical full song 5 to 6 months later (Fig 12.7) This song learning period extends from the 10th to 50th day of its life (Some other species do not show this critical learning period.) In addition, juvenile males must be able to hear themselves sing; otherwise, they will develop aberrant songs While
Trang 7Song sparrow song rejected Abnormal song Abnormal full song
(c) Only different species song presented
Hatching Critical song
learning period
10 days
of full song
(a) Isolation
(b) Different songs presented together during critical period
reproduced at maturity
Adult male white-crowned
sparrow song accepted
Song sparrow song rejected
by innate template
(a) Exposed to no song at all, male white-crowned sparrows (Zonotrichia leucophrys) produce subsong, but develop only a rudimentary version of their species’ normal song (b) Exposed to tapes of both their own species’ song and that of the related song sparrow, they produce more complex subsong and a fully developed song characteristic of their own species (c) Exposed only to the other species’ song, they fail to learn.
FIGURE 12.7
the songs of male white-crowned sparrows within a
pop-ulation are strikingly consistent from year to year, males of
other distinct populations have easily recognizable dialects
(Marler and Tamura, 1962) (Fig 12.8a–c)
Sound production and reception is very efficient in
mam-mals Vocal cords for producing sound are well developed,
and the middle ear contains three bones (malleus, incus, and
stapes) for receiving sound The pinnae of many mammals
(e.g., deer) are mobile, and each can be controlled
indepen-dently of the other to enhance hearing Mammals may emit
many sounds They may squeak, bark, bugle, howl, bellow,
roar, neigh, moo, oink, cry, laugh, and speak They may
engage in tooth chattering, tail rattling, and drumming on
the ground with their hind feet
Foot-drumming in kangaroo rats (Dipodomys) is
indi-vidually distinct (Randall, 1989) Individual rates are higher
in males than in females Rates are also higher in young adults than in juveniles and older adults; thus, foot-drumming rates may be used to communicate age, sex, or vitality Foot-drumming may also be important in territorial defense
East African vervet monkeys (Cercopithecus pygerythrus)
give different alarm calls in response to three major preda-tors: leopards, eagles, and snakes (Seyfarth and Cheney, 1992) (Fig 12.9) Each call elicits a distinct escape response from nearby vervets Alarm calls about leopards cause vervets
to run into trees Eagle alarms cause them to look upward or run into the bushes, whereas snake alarms cause them to stand on their hind legs and look into the grass
Prairie dogs (Cynomys spp.) have a “vocabulary” of 10
different calls ranging from a commonly used warning bark
to a chuckle, a “fear” scream, and a fighting snarl (Waring, 1970; Smith et al., 1977) Each call results in a specific action
Trang 8Different alarm calls are given by vervet monkeys (Cercopithecus pygerythrus) in response to the sighting of at least three major predators: leopards (top), martial eagles (middle), and snakes, such as the African rock python (bottom) The monkeys change their escape route to match
the specific alarm call.
Source: From Seyfarth and Cheney, “Meaning and Mind in Monkeys” Scien-tific American, 267(6):122–128, 1992.
FIGURE 12.9
by nearby individuals Howler monkeys (Alouatta sp.) of
Panama have a vocabulary of 15 to 20 calls (Sekulic, 1982)
Their calls have been heard by people 3 km away through the
jungle and 5 km away across lakes (Nowak, 1991) Koalas
bellow, squeak, groan, and moan (Mitchell, 1991a) Twelve
different social and communicative calls are given by
white-tailed deer, including snorts, bawls, grunts, mews, bleats, and
whines (Atkeson et al., 1988)
Sherman (1977) found that female Belding’s ground
squir-rels (Spermophilus beldingi) (Fig 12.10a) gave alarm calls when
a predator was in the vicinity more often than expected by
chance, whereas the converse was true for males (Fig 12.10b)
Females are generally sedentary (with respect to emigration) and mature and breed near their natal sites, whereas males always emigrate from their birthplace and do not aggregate with siblings after emigration As such, females were warn-ing close kin (often offsprwarn-ing) by givwarn-ing such alarm calls, whereas no such benefit accrued to males for warning
oth-(a)
(b)
(c)
a
b
c
d
e
f
g
h
i j k l m n o p
FIGURE 12.8
(a) Songs of eight male white-crowned sparrows (Zonotrichia
leu-cophrys) recorded at Sunset Beach, Santa Cruz County, California in
April 1959 The horizontal time scale is marked at 1-second intervals.
The vertical frequency scale ranges from 2 to 7 kHz (b) Songs of eight
white-crowned sparrows recorded at Sunset Beach in May 1960.
Note the consistency of the song when compared with the songs of the
same population of males in 1959 (c) A–H, songs of eight
white-crowned sparrows recorded at Inspiration Point, Contra Costa County,
California, in May 1960 I–P, songs of eight birds recorded in
Berke-ley, Alameda County, in April 1959 and May 1960 Note the
consis-tent difference in dialects in these birds from Contra Costa and
Alameda counties from those in Santa Cruz County
Trang 9ers about the presence of a potential predator Further
sup-port for the kinship hypothesis includes evidence that
“invad-ing” (nonnative) females gave alarm calls less frequently than
native females
The young of some bats and rodents, such as house mice
(Mus musculus), emit both audible and ultrasonic sounds.
These calls elicit search behavior in the female for her young;
they also reduce maternal aggression (Ehret, 1983) Many
pinnipeds produce a variety of underwater and airborne
sounds that appear to be related to breeding activities and
social interaction (Riedman, 1990)
Cetaceans produce a variety of pulsed calls and sounds
The eerie and plaintive songs of the humpback whale are
repeated according to identifiable patterns These sounds
usually range between 40 Hz and 5 kHz in frequency and can
be detected over 30 km away (Winn and Winn, 1978) They
may last from 6 to 35 minutes before being repeated One
whale was recorded singing nonstop for at least 22 hours
(Winn and Winn, 1978) Singing may take place during
migration, as well as during courting The singers are normally solitary males found in shallow coastal areas of 20 to 40 m in depth (Evans, 1987) One function of the humpback’s song
is thought to serve “as a spacing mechanism for courting males advertising their sexual availability to females” (Tyack, 1981) Identification is an important function of the sounds made by many baleen and toothed whales The sounds may give the location of the whale, its sex, status, emotional or activity state, and possibly even its individual identity (Evans, 1987) The vocal repertoire of many toothed whale cetaceans consists of ultrasonic clicks Most cetacean strandings, par-ticularly those involving pilot whales, occur on gently slop-ing beaches Some biologists believe that the gradual slope
of the beaches may not reflect the whales’ ultrasonic signals effectively If the whales do not hear an echo, they may receive
a false impression of deep open water ahead and continue swimming toward shore until it is too late
Bats (order Chiroptera) are the only mammals known to use echolocation as a principal means of locating prey
80
70
60
50
40
20
10
0
Adult
females
Adult males
Expected
1-year females 1-year males Juvenile females
First Squirrel Giving an Alarm Call
to a Predatory Mammal
Juvenile males
80 70 60 50 40 20 10 0
Callers, Regardless of Precedence,
to a Predatory Mammal
Observed
“G” statistic: 88.5
p : 0.001
Expected Observed
“G” statistic: 73.5
p : 0.001
Adult females Adult males 1-year females 1-year males Juvenile females Juvenile males
(b)
(a)
FIGURE 12.10
(a) A female Belding’s ground squirrel (Spermophilus beldingi) emitting a predator alarm call (b) Expected and
observed frequencies of alarm calling in Belding’s ground squirrel The overall significance of both comparisons is due
to females calling more than expected and males calling less Data based on 102 observations.
Source: (b) Data from Sherman, in Science, 197:1246–1253, 1977.
Trang 10FIGURE 12.11
Elephants in the breeding herd at Circus World, Haines City, Florida.
The arrow indicates the region of the elephant’s forehead where
flutter-ing can be observed durflutter-ing the production of infrasonic calls.
Calls at frequencies below the level of human hearing—
infrasound—may provide a significant means of
communi-cation in some social species such as elephants (Loxodonta africana), hippopotamuses (Hippopotamus amphibius), and alligators (Alligator mississippiensis) (Payne et al., 1986;
Lang-bauer et al., 1991a, b; Montgomery, 1992) The long wave-lengths of low frequency sounds are not reflected or absorbed
by vegetation or blocked by obstacles the way higher frequency sounds are The frequency of most elephant calls ranges from
14 to 24 Hz, with durations of 10 to 15 seconds Fluttering (Fig 12.11) in a particular area of the elephant’s forehead can
be observed during infrasonic calling Infrasonic calls may be important in coordinating the behavior and activity of animals
in thick vegetation or in communicating among separated groups of elephants Fin whales were the first marine mammals known to produce infrasound; elephants were the first terres-trial mammals known to produce such sounds
Hippopotamuses can produce infrasonic vocalizations both above and below the surface of the water (Montgomery, 1992) Above-water sounds are transmitted through the animal’s nos-trils, whereas the underwater signal is delivered close-mouthed and is transmitted through the tissue of the head and neck
Vision
Visual communication occurs in all vertebrate groups, with the eye being a highly specialized special sensory organ in most species In most fishes, vision is an important sense for BIO-NOTE 12.3
The Bark of the Dog
The wolf (Canis lupus) is considered to be the ancestor of
the modern domestic dog By comparing mitochondrial
DNA from wolves and dogs in different parts of the world
today, researchers have found that about 100,000 years ago
there was a genetic fork in the road of canine evolution—
biologically separating wolf and dog Previous estimates,
based on archaeological findings of bones in Germany and
Israel, placed canine domestication back about 13,000 years
ago—older than cats, cows, and horses, but not by much
Cattle were domesticated only about 8,000 to 9,000 years
ago; horses, 6,000 to 7,000 years; cats, 5,000 to 6,000 years;
and chickens, 4,000 years Over time, dogs have become
progressively less wolflike, evolving smaller teeth, a more
delicate body, and puppylike juvenile characteristics—traits
more appealing to human beings
Barking is the hallmark of the domestic dog (Canis
familiaris) Coyotes and wolves, on the other hand, bark
only rarely In one study, only 2.5 percent of 3,256
vocaliza-tions by captive wolves were barks And when wild canids
do bark, their barks tend to be brief and isolated, as
opposed to the long, rhythmic barking of the domestic dog
Repetitive barking in wolf pups is significantly more
frequent than it is in adults As the wild animal matures
and develops normal adult behavior, it gradually loses its
puppylike characteristics
Regulatory genes control an organism’s overall pat-tern and growth and the rate at which its individual parts grow Any change in the timing of these regulatory genes
is referred to as heterochrony (Greek hetero-, “different,”
and chronos, “time”) Heterochronic evolutionary
mecha-nisms can speed up or slow down the rate at which an animal grows from a newborn into an adult It may slow the rate so much that the animal may not attain its “nor-mal” full adult form Some biologists believe the dog “is
an adolescent in a state of change”—reproductively capa-ble but not yet endowed with the full physical and psy-chological maturity of a “real” adult Heterochronic
change is believed to have frozen Canis familiaris in
mid-metamorphosis It remains a “metamorphic” adolescent for life Its bark is thought to be a juvenile characteristic serving no real function, but probably is motivated by indecision Some dogs, however, learn to use barking as a means of communication, adapting this initially function-less behavior to serve specific functions such as indicating when they want to be let in or out of the house, or when they want food or attention
Coppinger and Feinstein, 1991
Vila et al., 1997 Morell, 1997d
However, baleen whales (order Cetacea) and pinnipeds (order
Pinnipedia) may use echolocation to a limited degree in
intraspecific interactions Some terrestrial species, such as
shrews, voles, tenrecs, oilbirds, and the cave swiftlet, appear
to use echolocation in certain instances