Download Display Behavior in Tortoises In spite of the knowledge gained over

AMER. ZOOL., 17:241-250 (1977).
Display Behavior in Tortoises
WALTER AUFFENBERG
The Florida State Museum, University of Florida, Gainesville, Florida 32611
SYNOPSIS When compared to lizards or snakes, signals related to warning and threat are
not very important in land tortoises. Within social and sexual contexts, tactile and chemical
signals seem more important than visual, and certainly than auditor)' ones. Color patterns
are rarely, if ever, sexually discriminatory. Seasonal color differences are rare. In general,
positional signals are rather limited, chiefly because of the shell. However, shell positional
changes are an important part of the visual and tactile signal repertory of all land tortoises.
Head movements are also important in several groups. Audible signals are poorly
developed. They are largely concerned with courtship and their role is not understood.
Chemical signals are pronounced, especially in displays related to sex identification, largely
based on scents associated with the cloaca. Tactile displays are important particularly
during courtship. They include biting and especially shell ramming by the male. The tail is
used as a tactile organ during courtship of some species.
INTRODUCTION
In spite of the knowledge gained over
the last several decades concerning reptile
behavior, it is clear that while we may know
several thousand species in the preserved
state, we are only vaguely familiar with less
than a hundred in the behavioral sense.
There is no question but that this lack
represents a challenge and an opportunity
many biologists are finding highly
stimulating.
In general, the behavior of turtles is
poorly known. At present most data are
available for land tortoises, but even here
our state of knowledge is very primitive.
As a result, comparisons are difficult and
only broad categorizations are possible.
The following, unfortunately, represents
the bulk of our knowledge of land tortoise
display behavior.
SIGNAL REPERTORY
Auditory signals
Despite early reports of turtle vocalization, little attention was directed to this
behavior until recently. This is largely due
to the once widespread belief that chelonians were deaf to airborn sound (Pope,
1955). Thus most workers regarded these
sounds as being accidental or incidental to
other activities. However, it is now clear
that many turtle species are actually quite
sensitive to airborn sounds, particularly
those below 1000 Hz (Wever and Vernon,
1956). Within this frequency range their
sensitivity is actually better than that of
many lizards and compares favorably with
that of the pigeon and guinea pig (Peterson, 1966). While sound production occurs
in a wide variety of turtles, it is particularly
common in the testudinids.
Many tortoise species are known to vocalize, particularly in a courtship context
(Table 1). Various species-specific sounds
may be produced by the males of some
species when following or approaching the
female, when mounted, or sometimes
when foraging (Campbell, 1967). Campbell
and Evans (1967) believed the latter might
serve the same function as the contact calls
of other vertebrates (Collias, 1960).
Campbell (1967) demonstrated that when
the sounds are played back the tortoises
sometimes exhibit a visual, but not an
auditory response. Some species are
known to produce sounds during male
combat (Table 1). At least two species
produce one vocalization during courtship
while following or approaching the female
and another during mounting (Geochelone
elephantopus, DeSola, 1930; Geochelone car-
bonaria, Snedigarand Rokosky, 1950; and
241
242
WALTER AUFKENBERG
TABLE 1. Vocalization reported in tortoise species.
Species
Geochelone carbonana
Geochelone elegans
Context
Mounted and
courtship
Foraging
Mounted
Geochelone elephanlopus Mounted and
Author(s)
Remarks
(as denliculata)
"grunts," "short croaks"
"roars and bellows"
courtship
Geochelone gigantea
Geochelone pardalis
Mounted
Mounted
Geochelone radiata
Mounted
Geochelone travanconca Foraging and
Gopherus agassizi
resting
Mounted
Gopherus berlandien
Gopherus polyphemus
Resting
Mounted
Mounted
Psammobates oculifera
Tesludo hermanni
Testudo graeca
Mounted
Mounted
Mounted
"moans and bellows"
"grunts and groans," "husky cry"
"rhythmic grunts"
Sometimes in choruses in rain;
"croaking"
"grunting"
"moan"
"grunts"
"grunts"
Gopherus agassizi, Campbell and Evans,
1967).
No complete analysis of sound production is available for any species, but preliminary work by Campbell and Evans
(1967, 1972) shows that the calls range
from 500-2500 Hz. While the overlap is
not great, studies show that maximum
auditory sensitivity for turtles is at about
400-500 Hz (see Adrian, Craik, and Sturdy,
1938 and Campbell and Evans, 1972 for
review).
While some headway has been made in
establishing the species groups in which
sounds are produced, and there is now at
least some information on energy level and
sensitivity, the purpose of these sounds
remains unclear. The sound of tortoises is
made by the breathing apparatus, except
for G. travancorica in which it seems to be
produced by the mandible rubbing against
the maxillary.
Hissing represents another sound category. This common signal in tortoises is
believed to be of value in discouraging
predation (Mertens, 1946). It is usually
produced when the limbs are quickly pulled into the shell.
Snedigar and Rokosky, 1950;
Grant and DeSola, 1934
Campbell, 1967
Jayakar and Spurway, 1966;
Deranyagala, 1939
DeSola, 1930; Heller, 1903;
VanDenburgh, 1914, Watson,
1962
This paper
Archer, 1948; Leaky, 1944;
Watson, 1962
This paper
Auffenberg in Campbell and
Evans, 1972
VanDenburgh, 1922; Grant,
1936; Nichols, 1953
Campbell and Evans, 1967;
Householder, 1950
Hallinan, 1923; Carr,
1952
FitzSimons, 1935
Obstand Meusel, 1965
Mertens, 1946, Watson,
1962; Nikolski, 1915
Chemical signals
Not only are chemical signals widespread in reptiles, but they are at least
equally as diverse in function as visual, and
more diverse than auditory types. When
compared to other systems, chemical signals possess several advantages. They can
transmit through darkness and around
obstacles. Furthermore, they are the only
signal type that may be useful in a future
context. While chemical signals have a
greater potential transmission range than
other signal types used by reptiles, in tortoises these signals have a range of from
several centimeters to several meters.
Scents and musks are commonly produced by turtles (see Mertens, 1946), and
tortoises are no exception. While no pronounced musk glands are found on the
shell, as in kinosternids and chelydrids, the
hinge-back tortoise (Kinixys belliana)
exudes a "strong smelling" viscid material
from the cloaca when handled (Lang, in
Schmidt, 1919). Similar defensive tactics
include voiding part of the digestive or
excretory contents. Thus Geochelone radiata
regurgitates the stomach contents when
TORTOISE BEHAVIOR
243
under potential predator attack. Most subdentary gland secretions. He was able
species empty the bladder when handled to show that males respond to adults of
or otherwise stressed. In addition, the both sexes when the glands of both are
large intestine is evacuated by most tor- active, and only to males when the glands
toises when under either physiological or are inactive. Females react to males when
psychological stress. While none of these the glands of both are active, but do not
has.intraspecific communicative functions, discriminate when the glands are inactive.
pheromones are used by tortoises for this
During the courtship of at least G.
purpose. The best known is produced by polyphemus (Auffenberg, 1966; Weaver,
the subdentary glands found in the genus 1970) other behavior patterns, such as
Gopherus (Fig. 1).
head bobbing, are often interrupted by
The glands occur in both sexes of all either tortoise wiping the subdentary
four extant Gopherus species. During gland over an enlarged scale on the medial
breeding they become enlarged, especially edge of one or both forelimbs. The limbs
in males. Rose, Drotman, and Weaver are then extended anteriorly, when the
(1969) have shown that the protein com- other individual may sniff at them (Fig. 2).
position of the gland exudate is sexually
Pheromones are also associated with the
and specifically differentiated, and that cloaca and perhaps the head. Olfactory
esterase composition is species-specific. investigation of the cloacal scent of females
That the glands serve as both olfactory and is often a prerequisite to courtship by the
visual recognition signals during courtship male (Auffenberg, 19646, 1965, 1966 for
and combat has been made reasonably Geochelone travancorica, G. carbonaria and G.
clear by Weaver (1970), who has also dem- denticulata, and Gopherus polyphemus respeconstrated that in at least G. berlandieri the tively; Weaver, 1970 for Gopherus berlansecretion is probably partly controlled by dieri). Males also sniff the hindlegs; parboth day length and testosterone level. He ticularly the parts that come into contact
concluded that males of G. berlandieri can- with the cloaca, such as the heel. They also
not distinguish females entirely by either pay considerable attention to the shell at its
cloacal scent, external morphology, or flair over the hindlegs and often seem to
movement alone, which suggests that sex- sniff the snout, or perhaps even the air
ual discrimination by males may rest exhaled out of the nostrils. MacFarland
largely with chemical differences of the (1972) reported that males of G. elephantopus "sniff the air for female scent"; presumably that associated with the cloaca.
Scents are also important in a social
context. While several pheromones may be
involved, the most important seem to be
associated with fecal pellet sign posting.
Though more evidence is clearly needed,
it is suggested in Patterson's work (1971a),
as well as in my tortoise compounds at
Florida, that fecal pellets of both Gopherus
agassizi and G. polyphemus cause dispersal in
conspecifics, particularly when the fresh
fecals are from a dominant male. Fecal
pellets, normally expelled after waking
and during the early phases of basking, are
commonly distributed near the sleeping
pallet (see Auffenberg and Weaver, 1969).
The fecal pellet frequently elicits much
attention on the part of other individuals,
FIG. 1. Adult male Gopherus berlandieri, showing particularly new recruits into the social
subdentary glands (arrow) enlarged during the
structure.
breeding season.
244
WALTER AUFFENBERG
facing one another in a head-to-head encounter.
The relative unimportance of vision is
shown by the fact that seasonal breeding
colors are reported only in males of one
species (Geochelone travancorica,
Auffen-
berg, 1964a), and these changes are very
slight. Swindells and Brown (1963) reported a similar color change in heatstressed adults of the closely related G.
elongata.
Positional changes are the most important of the visual signals in tortoises.
Ritualized head movements are most
common and have been reported in several species. The movements are speciesspecific and apparently based on olfactory
motor patterns (Auffenberg, 1965;
Weaver, 1970). Much more work is needed
on the action patterns of head movements
to determine individual and species variation. Ritualized head movements may
occur whenever two tortoises meet but are
most common and most vigorous in
male-male
combat and courtship contexts.
FIG. 2. External surface of left antebrachium of
Gopherus polyphemus, showing enlarged medial scale There is, however, no observable difference in the movements performed in the
(arrow) used to rake subdentary glands.
different contexts.
Courting males usually move their heads
more
vigorously than females. Movements
Visual signals
usually occur at a distance of one meter or
While it is clear that in lizards visual less. While Weaver (1970) is not certain
signals are most important in species iden- that head movements are species-specific
tification, as well as the status of individu- in the genus Gopherus, they are clearly so in
als within the dominance systems, there is at least one sympatric species pair
no evidence that vision is equally impor- (Geochelone carbonaria and G. denticulata,
tant in tortoises. However, I have shown Auffenberg, 1965).
elsewhere (1965) that visual signals are
Tortoise head movements include reimportant in species recognition in at least peated vertical bobbing in some groups
some tortoise groups, and that they are (such as Gopherus), or horizontal wagging
common components of courtship and in others (subgenus Chelonoides, genus
combat. Visual signals are probably not as Geochelone), and sometimes with compoimportant in tortoises because of the posi- nents of both (Geochelone travancorica).
tional and visual limitations imposed by Both Weaver (1970) and I (1965) are of
the shell and their proportionately short the opinion that these ritualized head
limbs. Thus tortoises are probably unable movements are sterotyped, exaggerated
to transmit the delicate shading or rapidly movements based on rather simple olfacfluctuating moods of both courtship and tory motor patterns that Eglis (1962) has
combat as readily as some other reptiles. shown are characteristic for each major
More than in any other reptile, visually- tortoise group.
communicating tortoises must be oriented
Head position may serve as a visual
to one another in such a way that the status indicator among some species.
signals can be seen, usually when they are Thus, dominant males of Gopherus berlan-
245
TORTOISE BEHAVIOR
dieri and G. polyphemus incline their heads
at a higher angle than subordinate males.
In courtship the neck of an aroused courting male is fully outstretched and inclined
in a high arch. A male thus aroused automatically exhibits a display of dominance
and inhibits interruptions by other, less
motivated males (Weaver, 1970). MacFarland (1972) stated that combat among
when the female stops, the male stops,
often moving its head. The significance of
the ritual-like cadence of this behavior on
the part of both individuals remains unknown. Female Gopherus polyphemus may
take a more active role in courtship and
approach the male (Auffenberg, 1966). In
Homopus areolatus the trailing male progresses along the ground by pushing him
adult male Geochelone elephantopus usually self with his rear feet and holding the front
ends in victory for the individual whose feet limp (Eglis, 1963).
head towers highest.
A specific courtship visual display is Tactile signals
suggested in only one tortoise species,
Communication in tortoises is maximally
Homopus areolatus. Eglis (1963) reported
that in the courtship of this species the developed in those intimate sequences of
male rushes from one side to another of aggregation, combat, and courtship that
the female, placing his shell at a 90° angle bring tortoises into bodily contact. While
with hers. Whether or not this is an impor- one might presume the presence of the
tant communication signal in this genus is shell in tortoises would severely limit the
usefulness of bodily contact, this is not the
unknown.
There is no question but that the sight of case. Tactile signals are reasonably effia moving tortoise is a strong visual signal, cient.
particularly during the breeding season.
Biting is one of the most obvious of the
Several authors (Leakey, 1944; et al.) have tactile signals of tortoises and is used in
reported male tortoises following the both combat and courtship contexts (Table
female for hours, or even days prior to 2). My earlier comment (1965), that biting
breeding. Weaver (1970) calls this trailing may not occur in combat of Geochelone
behavior and shows that it marks the be- elephantopus as reported by Van Denburgh
ginning of courtship. In Gopherus berlan- (1914), is incorrect in view of MacFarland's
dieri the male often follows one to three (1972) descriptions. In combat of all
meters behind the female. Most important, species, parts of the adversary may be
TABLE 2. Biting reported in the behavior of tortoise species.
Species
Context
Part bitten
Chersine angulata
Courtship
Geochelone denliculala Courtship
Geochelone elephantopus Combat
Legs
Legs
Head
Courtship
Legs
Geochelone radiata
Gopherus agassizi
Courtship
Courtship
Shell (rare)
Edge of shell
Gopherus berlandieri
Courtship
Gopherus polyphemus
Combat
Courtship
Homopus areolala
Tesludo hermanni
Courtship
Courtship
Head, legs, and mainly
edge of shell
Head, legs
Head, front limbs and mainly
epiplastral projection
Head
Head, legs
Testudo graeca
Courtship
Head, legs
Author(s)
Rose, 1950
Beltz, 1954
VanDenburgh, 1914;
MacFarland, 1972
DeSola, 1930; MacFarland, 1972;
Heller, 1903
This paper
Camp, 1916, 1921; Grant, 1946;
Woodbury and Hardy, 1948;
VanDenburgh, 1922
Weaver, 1970; Householder,
1950
Weaver, 1970
Auffenberg, 1966
Eglis, 1963
Obstand Meusel, 1965; this
paper
Doumerque, 1899; Nikolski,
1915; this paper
246
WALTER ALFFENBERG
bitten, but the head and legs are the usual
targets. In the courtship of some species,
of some species the ramming is rhythmic
and prolonged; in others it is irregular in
such as Gopherus berlandieri and Gopherus both cadence and length. It is usually the
polyphemus, most of the biting by the male is posterior or lateral slope of the shell that is
concentrated on particular parts of the struck. Ditmars (1910) reported a peculiar
shell (Table 3). Females never seem to bite. lateral bumping in the courtship of
Another important tactile signal is shell Geochelone elephantopus, but he did not deramming during both combat and court- scribe clearly just how it was done. Neither
ship. What has not been mentioned previ- MacFarland (1972) nor DeSola (1930)
ously is that there are two types of shell mention it. However, something similar
ramming. The common form utilizes the occurs in a defensive context in Gopherus
epiplastral projection. It may grade into a particularly when the defender is in its
pushing or hooking type of behavior. The burrow, plugging the hole with its shell. In
other form of ramming utilizes primarily this case the edge of the shell is quickly
the thickened anal scute area of the adult thrust laterally against the antagonist.
males. To distinguish them, the two types Though it is rare, I have seen a single
should be called epiplastral and xiphiplas- lateral head butt used by females of both
• tral ramming. Epiplastral ramming is easily Geochelone denticulata and Gopherus
and frequently recognized and applies to polyphemus against the heads of aroused,
all "ramming" mentioned in the literature courting, conspecific males.
so far. Characteristically it occurs when the
Epiplastral ramming is also common in
male raises himself on four legs, rocks combat among conspecific males, but more
backward and then suddenly forward, often it takes the form of pushing, in
sending the epiplastral projection crashing which, as soon as contact is made with the
into the shell of another individual (Fig. 3). adversary's shell, the hindlimbs are used to
The resulting noise can be heard for 100 m push against the ground. Pushing may
or so in larger species. Epiplastral ram- occur against any shell surface, but most
ming is not accompanied by any other often against the anterior edge of the
signal, but it often alternates with head adversary's shell. With the head of both
movements and sniffing. During courtship turtles withdrawn, the shells tend to interTABLE 3. Major tactile signals utilizing the shell in tortoises.
Species
Signal types represented
Chersine angulata
Geochelone carbonana
Geochelone denticulata
Geochelone elegans
Epiplastral
Epiplastral
Epiplastral
Epiplastral
ramming, pushing, and hooking
and xiphiplastral ramming, pushing
and xiphiplastral ramming
ramming and pushing
Geochelone pardalis
Xiphiplastral ramming
Epiplastral ramming, pushing, and hooking
Gopherus agassizi
Xiphiplastral ramming
Pushing and hooking
Xiphiplastral ramming, pushing, and hooking
Epiplastral and xiphiplastral ramming
Pushing
Epiplastral ramming, pushing, and hooking
Gopherus berlandieri
Gopherus flavomarginatus
Gopherus polyphemus
Testudo hermanni
Xiphiplastral ramming
Same as G. agassizi
Same as G. agassizi
Same as G. agassizi
Epiplastral ramming and pushing
Testudo graeca
Same as T. hermanni
Geochelone radiata
Geochelone travanconca
Context
Combat
Courtship
Courtship
Combat and
courtship
Courtship
Combat and
courtship
Courtship
Combat
Courtship
Courtship
Combat
Combat and
courtship
Courtship
Combat and
courtship
TORTOISE BEHAVIOR
247
FIG. 3. Agonistic ramming by male Geochelone travancorica during courtship.
lock, and the two tortoises push against mon it is usually directed more to the
one another until one is forced backward; flange above the hindlegs. Hooking is
thus becoming the loser in the contest.
often missing in courtship.
Most often the pushing in combat has a
During xiphiplastral ramming, pushing,
definite upward component. The epiplas- or hooking, a common defensive tactic
tral projection is placed under the edge of and/or rejection signal is shell drop, in
the shell of the adversary and lifted (Fig. which the edge of the carapace is lowered
4). When combined with a forward rush, it to the ground at the point where it is
may turn the adversary over. This is usu- touched by the male. The same signal is
ally the end of the match. I call such sometimes used by females when mounted
behavior hooking. Patterson (1971a) re- by males. Presentation, or shell lift, is a
ported that male Gopherus agassizi on their strong tactile acceptance signal in which
back may give a call, upon which the victor the posterior part of the shell is lifted,
turns it onto its plastron; I have not yet exposing the cloacal area to the caudal
observed this particular behavioral se- probing of the male. Another tactile rejecquence, though I have often seen tortoises tion signal is a lateral waggle, in which the
rolled over again—sometimes over and female rapidly thrusts her shell from side
over several times. When hooking is com- to side—apparently in an effort to dis-
FIG. 4. Agonistic hooking behavior by male Geochelone radiata during courtship and combat.
248
WALTER ALFKENBERG
lodge or discourage the mounted male.
nals. The total compares favorably to that
The second major type of shell tactile of total displays in fishes (10-26), birds
signal is xiphiplastral ramming. It has not (15-28), or even mammals (16-37). (Data
been reported before. Employed only by after Moynihan, 1970)
males and restricted to courtship (except
While signals used in a sexual context
for homosexual activity), it occurs during are obviously important, those related to
the times that males are mounted. The agonistic behavior are particularly imporfront feet of the mounted male are used as tant in establishing and maintaining
a pivot around which the body swings hierarchies, especially in colonial forms.
downward when the rear feet are both The social hierarchy in tortoises is deterlifted off the ground simultaneously in a mined largely by superiority in aggressive
short, hop-like movement. At this instant encounters and ultimately regulates order
the anal thickening on the xiphiplastron is of access to food or forage areas, mates,
slammed against the rear lower part of the and resting sites. In tortoises it is a simple
female's shell, making a loud "thud" or system of essentially two levels, the higher
"crack" that can be heard for several tens one controlling, at least to some extent, the
of meters. At the same time the male may activities of the lower levels, though reverutter a loud "cluck" or similar sound. sals are common. Individuals are conThese are the "thrusting" movements nected by weak social bonds and a few
often mentioned in the literature. How- communicative signals. In general, the
ever, it is important to point out that at this number of conspecifics contacted by the
point intromission has not yet occurred. At average individuals per unit time is low
coition these movements are modified so (highest in the more or less colonial
that the loud noise and hopping are usu- forms). However, aggression is common in
ally absent. Movements are, in general, less adult males during the breeding season,
vigorous and cadenced. Tactile signals but may take place during the entire year
using the shell are listed and compared in in some species. While non-random spacTable 3.
ing is often obvious in colonial species, it is
During the xiphiplastral ramming of the not common. In fact, sleeping aggregafemale, the tail of the male of at least some tions are the rule in captive herds of several
species may be used to maintain a proper species.
mounting position (Auffenberg, 1965; PatDominance is established during initial
terson, 19716, 1972). Gopherus agassizi encounters, followed by future individual
males use the tail as an aid in attaining recognition in at least captive situations.
cloacal contact (Patterson, 19716). This Strength, established through pushing and
also occurs during xiphiplastral ramming hooking, is usually the ultimate determinin Geochelone radiata. In this species the tail ing factor, though size and experience are
tip is eventually inserted into the cloaca, also important. The losing contender
and the tail is then used as a guide by exhibits strong submissive signals (turning
which the penis locates, and is finally in- or walking away) that help it to leave the
serted into the cloaca.
field without being turned over. Other
submissive signals are head and limb withdrawal and shell drop.
DISCUSSION
Courtship of tortoises includes both
Compared to lizards, the signal reper- agonistic and sexual signals. In two earlier
tory of land tortoises may seem limited. contributions (1964a, 1965) I have tried to
However, the minimum total signals emphasize the usual steps of land tortoise
utilized in a single species, such as courtship ritual, particularly the early
Geochelone radiata, is as high as 15 (plus five phase in which the female is more or less
possible ones). Of those that are certain, immobilized. This is usually brought about
nine are tactile (plus two?), three are visual by vigorous and repeated biting and/or
(plus one?), two are olfactory, and vocaliza- epiplastral ramming by the male. Particution possibly represents two auditory sig- larly aggressive attacks usually result in the
TORTOISE BEHAVIOR
249
female withdrawing her head and legs, the probability that the signaler is still in
and are often renewed only when the the vicinity. Most important, there is little
female again begins to walk away. Im- visual advertisement of sex or reproducmobilization is usually followed by mount- tive status in tortoises.
ing and, during the early part of the reStatus signaling is also poorly developed
productive period, unsuccessful attempts in tortoises. However, individuals of at
at intromission.
least some species (usually the larger ones)
It is only days or weeks later, after seem capable of discriminating among
repeated mating attempts, that the females conspecific individuals. While visual sigseem to become receptive. The seemingly nals are clearly important in many social
endless, redundant tactile signals of con- contexts, chemical ones may provide the
tinuous epiplastral and xiphiplastral ram- most discriminating signals by which indiming, pushing, hooking, and biting are viduals are separated. Thus, cloacal scent
apparently very important in establishing and (in Gopherus) the subdentary glands
the pair bond. The repetition may also may serve an important discriminatory
serve to awaken a state of arousal in the function. These probably develop in confemale and may serve to alter her repro- junction with the individual's rank, so that
ductive physiology as well. Lehrman perhaps only large, dominant males and
(1965) and others have shown that male mature females are able to impart their
behavior in some birds during early court- own odor signatures. The capability is well
ship induces changes in ovarian develop- known in mammals (see Wilson, 1975 for
ment and female sexual behavior. Re- review). Reptile pheromones, including
peated mounting and copulation in rats those in tortoises, are largely unexplored
may increase the amount of sperm trans- and would handsomely repay careful inported to the uterus and also the per- vestigation.
centage of successful implantations by fertilized ova (Adler, 1969; Adler, Resko, and
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Anatomical structures and physiological
characteristics used as status signals in
courtship are examples of effortless sustained signals. The sex-specific cloacal
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