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Sex in the Half-Shell: A Review of the Functions and Evolution of Courtship
Behavior in Freshwater Turtles
Author(s): Yu-xiang Liu , Christina M. Davy , Hai-Tao Shi , and Robert W. Murphy
Source: Chelonian Conservation and Biology, 12(1):84-100. 2013.
Published By: Chelonian Research Foundation
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Sex in the Half-Shell: A Review of the Functions and Evolution of Courtship Behavior in
,CHRISTINA M. DAV Y
,AND ROBERT W. MURPHY
College of Life Science, Hainan Normal University, Haikou, 571158, People’s Republic of China;
Present address: Department of Biology, University of North Carolina, Chapel Hill, North Carolina 27599 USA [email@example.com];
Department of Ecology and Evolutionary Biology, University of Toronto, Toronto, Ontario, Canada [firstname.lastname@example.org];
Chengdu Institute of Biology, Chinese Academy of Sciences, No. 9 Section 4, Renmin Nan Road, 610041 Chengdu, Sichuan Province,
People’s Republic of China;
Corresponding Author [email@example.com];
Department of Natural History, Royal Ontario Museum, 100 Queen’s Park, Toronto, Ontario Canada M5S 2C6 [firstname.lastname@example.org]
ABSTRACT. – Freshwater turtle courtship is an exciting and potentially phylogenetically important
field of study. Scattered data exist from the past century of research, yet no recent summary is
available. Courtship in freshwater turtles includes a number of common behaviors, which usually
involve visual, tactile, olfactory, and auditory signals. These signals function in both species and
sex recognition and in the seduction of potential mates. Specific behavioral sequences are required
to facilitate successful copulation, and these behaviors presumably play a role in mate choice. We
performed a series of meta-analyses to investigate the evolution of courtship behavior in
freshwater turtles. Biting, an aggressive form of courtship behavior, is plesiomorphic, conserved
only in the Chelydridae, Kinosternidae, subfamily Emydinae and South American species in the
Pleurodira. Head movement and foreclaw display are apparently apomorphic and evolved
independently in the Geoemydinae, Deirochelyinae, and Australian species of the Pleurodira.
Display type (pre- or postmounting display) and sexual size dimorphism also show phylogenetic
patterns. Therefore, the evolution of courtship behavior in freshwater turtles might accompany
the evolution of sexual dimorphism, which is directly subject to natural selection.
KEY WORDS. – Meta-analysis; sexual dimorphism; mating signal; natural selection
The courtship behavior of freshwater turtles (CBFT)
has been a topic of research interest for over a century.
Anecdotal reports and more detailed observational studies
have identified visual, tactile, chemical, and auditory
stimuli. Early reviews by Carpenter and Ferguson (1977)
and Harless (1979) noted a paucity of data. Over 30 yrs
later, an impressive body of literature on CBFT has
accumulated, but this literature is scattered, and no recent
summary is available. Thus, although observations of
courtship behavior exist for many species, our under-
standing of how CBFT operates remains limited because
the functions of most signals used in courtship remain
elusive. This is partly attributable to logistical difficulties
involved in studying behavior in freshwater turtles and to
the difficulty of determining the interpretation of signals
by the receiver.
Some more rigorous studies have produced quantifi-
able models of courtship behavior (e.g., Baker and
Gillingham 1983; Liu et al. 2008), and these lend
themselves to hypothesis testing. However, analyses and
applications of ethograms based on stereotype patterns
remain rare, and this precludes combining ethograms for
comparative studies. Harless (1979) has identified neces-
sary steps to move forward—hypothesis testing, identifi-
cation of stimuli that elicit signaling, and identification
of signal function—and much of this remains to be
Herein, we provide a brief history of the study of
CBFT. We review behaviors and signals currently
implicated in turtle courtship studies and discuss the
methods and statistical analyses commonly used in these
studies. This review unifies descriptions of behavioral
patterns with phylogenetic data to facilitate an under-
standing of the function and evolution of each signal.
Although data remain limited, where possible we test
explicit hypotheses to clarify the evolution of CBFT.
Finally, we recommend directions for future study in the
hope of stimulating further research.
HIGHLIGHTS IN THE STUDY OF
The literature on CBFT can be roughly divided into 3
categories: 1) anecdotal observations; 2) qualitative study;
and 3) quantitative study. Early works contain anecdotal
observations only. The first observation of CBFT of which
we are aware is Maynard’s (1869) description of the
display of elongated foreclaws in male Centronyx bairdii.
Soon thereafter, Darwin (1871) reported the mounting
behavior of Chrysemys picta. Natural history texts and
literature in the early 20th century contain occasional
opportunistic descriptions of courtship behavior in fresh-
water turtles such as observations of biting and mounting
(e.g., Gadow 1901; Camp 1916).
Chelonian Conservation and Biology, 2013, 12(1): 84–100
g2013 Chelonian Research Foundation
Nowadays, CBFT is a subject unto itself, and
anecdotal reports of courtship behavior in different
species appear regularly. Observations of in situ turtle
courtship (e.g., Pisani 2004, Ashton 2007) are necessarily
opportunistic because wild turtles are difficult to observe
for long periods of time. Therefore, such observations
often contain only one or a few segments of the whole
behavioral sequence. However, these observations pro-
vide an important basis for comparison because behaviors
in captivity, may differ from those exhibited in the wild.
As more turtle species are maintained in captivity
observations of ex situ courtship have accumulated,
especially for species whose behavior is difficult to
observe in the wild (e.g., Drajeske 1983, Molina 1996).
As a result, most studies dedicated to CBFT have
occurred in captivity.
Studies conducted in captivity allow the collection of
a greater volume of detailed data in less time and with
fewer logistical difficulties (e.g., Lardie 1975; Norris
1996). Most studies of CBFT whether in situ or ex situ
consist of qualitative rather than quantitative efforts (e.g.,
Plummer 1977; Horne 1993; Norris 1996; Jenkins and
Babbitt 2003). Taylor (1933) has provided the first study
dedicated exclusively to freshwater turtle courtship,
focused on Trachemys scripta elegans. Next, several
researchers have set out to divide turtle courtship into
discrete phases. Mahmoud (1967) has characterized 3
phases in the courtship behavior of 4 kinosternid species: 1)
tactile, mounting, and intromission; 2) biting; and 3)
rubbing. Similarly, Christensen (1975) has divided the
courtship of Rhinoclemmys pulcherrima incisa into 3
components: 1) male activity; 2) female activity; and 3)
copulation. Such studies provide useful starting points for
further research, and they often describe previously
unknown behaviors. Unfortunately, exclusively qualitative
studies preclude statistical hypothesis testing.
New technology facilitated the addition of quantita-
tive analyses of turtle courtship. Photographic (e.g.,
Lardie 1975; Murphy and Lamoreaux 1978; Duda and
Gupta 1981), videographic (e.g., Jackson and Davis
1972), and cinematographic analyses (Baker and Gilling-
ham 1983; Thomas and Altig 2006; Liu et al. 2008)
allowed for more detailed observations to be made.
Recording allows for the repeated viewing of behaviors
and the observation of behaviors in cryptic or shy species
who will not exhibit some behaviors while under direct
observation. Repeated ex situ observations combined with
imaging techniques have facilitated the development of
robust courtship ethograms and quantitative analyses.
The extent of quantitative assessment has varied.
Some early quantitative studies report the duration and
frequency of a few easily recognized behaviors only
(Jackson and Davis 1972; Murphy and Lamoreaux 1978).
Flow diagrams and sequential photography have been
used to qualitatively describe the intrinsic relationships
among different courtship behaviors and the order in
which they occur (e.g., Jackson and Davis 1972; Lardie
1975; Duda and Gupta 1981; Baker and Gillingham 1983;
Bels 1983; Kramer and Fritz 1989; Bels and Crama 1994;
Norris 1996; Liu et al. 2008). Some studies have used
statistical applications to test for correlations in their order
of occurrence. For example, intra-individual dyadic
transition matrices have been used to isolate important
motor pattern dependencies. Chi-square tests can deter-
mine whether or not behavioral sequences are random
patterns (Baker and Gillingham 1983; Bels and Crama
1994; Liu et al. 2008). Baker and Gillingham (1983) and
Bels and Crama (1994) have used Z-scores (Poole 1978),
and Liu et al. (2008) have used kappa analyses (White-
hurst et al. 1986), to find significant correlations between
the dyadic pairs and to determine whether certain
behaviors are followed predictably by others. A review
of statistical analyses of behavior is beyond the scope of
this article, but they are an important tool for studying
courtship (e.g., Runyon and Haber 1976) and should be
incorporated into future research on CBFT.
Hypotheses of the evolution of courtship behavior
have sometimes been used for species identification and
the construction of phylogenies. For example, Seidel and
Fritz (1997) have suggested that foreclaw display provides
evidence of monophyly for the genus Pseudemys. Although
controversial, Berry and Shine (1980) have hypothesized
that male courtship and mating strategies are a function of
sexual dimorphism in body size.
COURTSHIP SIGNALS IN FRESHWATER
TURTLES AND THEIR FUNCTIONS
In the process of communication, a signal is the
vehicle by which information passes from the sender to
the receiver (Bradbury and Vehrencamp 1998). Therefore,
for an honest signal to function it must transmit the
intended information to the intended receiver. For
example, initiation of successful mating behavior depends
first on recognition of conspecifics and then of the
opposite sex (Weaver 1970; Murphy and Lamoreaux
1978; Hidalgo 1982; Bels and Crama 1994; Bradbury and
Vehrencamp 1998). Deciphering the true function of a
signal requires an understanding of both the information
coded within it and the effect of that information on the
recipient. In this regard, data for CBFT are nearly
nonexistent. Nevertheless, when possible, we summarize
the current understanding of potential courtship signals in
freshwater turtles and discuss their functions to identify
future directions for research.
Signals implicated in turtle courtship involve visual,
tactile, chemical, or auditory pathways. Some signals may
be difficult to observe objectively. For example, olfaction
probably plays a key role in finding a mate and in the
initiation of courtship in kinosternids (e.g., Lewis et al.
2007). Turtles probably receive and respond to subtle
courtship signals (olfactory and subtle visual signals)
before they begin to exhibit easily detectable behaviors,
which might carry tactile or visual signals.
LIU ET AL. — Courtship Behavior in Freshwater Turtles 85
Table 1 lists potential courtship signals reported for
freshwater turtles and their potential pathways (visual,
tactile, chemical, or auditory). In some cases, a signal may
involve more than one pathway and/or have more than
one function. For example, head bobbing is probably a
visual signal but may also dissipate pheromones, thus,
functioning as a chemical signal as well (Baker and
Gillingham 1983). Below, we review common courtship
signals in freshwater turtles. Where sufficient data exist,
we also investigate their evolutionary histories by
mapping them on an existing phylogeny of freshwater
turtles (Seddon et al. 1997; Barley et al. 2010) and test
phylogenetic constraints on behaviors using the data listed
in Table 2.
Several studies have indicated that body shape is an
important visual signal in the initial stages of turtle
courtship (e.g., Davis and Jackson 1973; Hidalgo 1982;
Baker and Gillingham 1983). Body shape is one of the
first things a male turtle can assess when it encounters
another turtle. Hidalgo (1982) has reported that male R. p.
incisa show a positive response to moving objects that
resemble turtles. Baker and Gillingham (1983) have
observed a male Emydoidea blandingii mounting a rock
about the size of a conspecific turtle on 3 occasions. There
are numerous examples of turtles misidentifying potential
mates. Eglis (1962) has described a male Mauremys
rivulata courting a female Trachemys scripta. Davis and
Jackson (1973) have reported a Trachemys scripta taylori
attempting courtship with other turtles regardless of
species or sex but not with randomly shaped objects.
Arndt (1986) has observed male Glyptemys muhlenbergii
mounting female Clemmys guttata and conspecific males.
Kramer and Fritz (1989) have described a captive
Pseudemys nelsoni with a preference for a female
Pseudemys concinna. Thus, body shape appears to
function as a visual signal in the initial stages of courtship
to distinguish turtles from other objects but is not used for
the recognition of either species or gender.
MARKINGS AND PIGMENTATION
Most species of turtles have species-specific mark-
ings. Although the forces that select for coloration in
turtles are not well understood, color pattern may function
in species recognition. Mansfield et al. (1998) have
reported an experiment using hoop traps, some baited
with a turtle-shaped object painted to simulate the
markings of C. guttata. In the spring mating season,
baited traps caught more C. guttata than either unbaited
traps or traps baited with food. Because the decoys were
not providing olfactory, auditory, or movement-related
signals, it seems that C. guttata likely identifies potential
conspecific mates based on their markings. Moll et al.
(1981) have reported that males of the closely related and
sympatric Batagur baska and Callagur borneoensis
conversely change the color of their head and shell
during the breeding season, and Kuchling (1999)
considers this shift to function for conspecific recognition
Beyond the initial recognition of potential mates,
markings and coloration may play a further role in
courtship in some species. Lardie (1975) has noted that
male Kinosternon flavescens expand their yellow throat
while biting and rubbing the head of the female. This may
either be incidental or provide a deliberate visual signal to
the female. Baker and Gillingham (1983) have suggested
that the swaying behavior of E. blandingii, in which the
male angles his head down in front of the female and
sways it from side to side, functions to display his
conspicuous yellow throat at a crucial point in the
courtship ritual. Rovero et al. (1999) describe a similar
chinning behavior in Emys orbicularis, in which males
also display their yellow throat to females. In both E.
blandingii and E. orbicularis, the action of displaying the
chin to the female immediately precedes either successful
mating or reticence on the part of the female. Liu et al.
(2008) suggest that head bobbing in Sacalia quadriocel-
lata functions to display the bright red stripes on the
ventral part of the neck. These speculations on the role of
bright markings as visual cues in courtship could be tested
Table 1. Pathways by which commonly observed turtle courtship signals are potentially assessed by the receiver. See text for
definitions of each signal.
Visual Tactile Chemical Auditory
Body shape X
Head movements (head bobbing and variations) X X X
Eye blinking X
Nudging/rubbing X X
Chinning X X X
Barbel contact X X
Biting X X X
Foreclaw displays X X X
Water propulsion (gulping and nasal squirting) X X
Shell clapping X X X
Chemical (olfactory) signals X
86 CHELONIAN CONSERVATION AND BIOLOGY,Volume 12, Number 1 – 2013
Table 2. Some main male courtship behaviors, display type, and mounting position in freshwater turtles. FD, foreclaw display; HM,
head-movement; Bite, biting; Nudge, nudging; Rub, rubbing, Gulp, gulping; Disp, display; Pos, position; +, behavior present; 2,
behavior absent; ?, no data; Pre, premounting display type; Post, postmounting display type; All, 4 limbs clasp female’s carapace
during copulation; and Two, 2 limbs clasp female’s carapace during copulation. See text for definitions and explanations
Species FD HM Bite Nudge Rub Gulp Disp Pos Source
Chelodina expansa 2+2222 Pre ? Legler 1978
Chelodina longicollis 2+2+22 Post All Murphy and Lamoreaux 1978
Elseya latisternum ++2+2+Pre All Murphy and Lamoreaux 1978
Emydura macquarii ++2+2+Pre All Murphy and Lamoreaux 1978
Emydura subglobosa ++2+2+Pre ? Norris 1996
South American species
Acanthochelys pallidipectoris 22 +2+2Post ? Horne 1993
Chelus fimbriatus ++2? ? ? Pre ? Drajeske 1983
Hydromedusa maximiliani ?????? Post ? Novelli and Souza 2007
Mesoclemmys vanderhaegei 2+2?+2Post ? Brito et al. 2009
Pelomedusa subrufa 2++? ? ? Post ? Harding 1981; Bels 1983
Phrynops geoffroanus 22 +? ? ? Post ? Molina 1996
Phrynops hilarii 22 +? ? ? Post ? Richard 1999
Platemys platycephala +22 +++ Post All Harding 1983; Medem 1983
Podocnemis erythrocephala 22 +++2Post ? Ferrara et al. 2009
Podocnemis vogli 22 +? ? ? ? ? Ramo 1982
Actinemys marmorata +22+22 Post ? Holland 1988; Ashton 2007;
Clemmys guttata 22 ++22 Post Two Ernst 1967, 1970; Chippindale 1989
Emydoidea blandingii 2+2+++ Post All Richmond 1970; Baker and
Emys orbicularis 22 +2+2Post Two Rovero et al. 1999
Glyptemys insculpta 2+++2+Pre All? Evans 1961; Ernst and Lovich 2009
Glyptemys muhlenbergii 22 +? ? ? ? All Campbell 1960
Chrysemys picta +2+? ? ? Pre ? Taylor 1933; Ernst and Lovich 2009;
Deirochelys reticularia*+22222 Pre ? Ewert et al. 2006, Seidel 2010
Graptemys barbouri +22222 Pre ? Wahlquist 1970
Graptemys ernsti 2+2222 Pre ? Ernst and Lovich 2009
Graptemys flavimaculata +22222 Pre ? Cagle 1955
Graptemys geographica 2+2222 Pre ? Ernst and Lovich 2009
Graptemys kohni 2+2222 Pre ? Ernst and Lovich 2009
Graptemys nigrinoda 2+2222 Pre ? Lahanas 1982
Graptemys ouachitensis ++2222 Pre ? Ernst and Lovich 2009
Graptemys pseudogeographica +2+222 Pre All Ernst 1974
Graptemys pulchra ++2222 Pre ? Shealy 1976
Graptemys versa +22222 ? ? Ernst and Lovich 2009
Malaclemys terrapin tequesta ++2+22 Pre All Seigel 1980
+22 +22 Post All Marchand 1944; Jackson and Davis
Pseudemys floridana +22222 Pre ? Cagle 1955
Pseudemys nelsoni +2++22 Pre ? Kramer 1984; Kramer and Fritz 1989
Pseudemys peninsularis +22222 Pre ? White and Curtsinger 1986
Trachemys gaigeae 2+222 +Pre ? Stuart and Miyashiro 1998
Trachemys scripta elegans +2222 +Pre Two Jackson and Davis 1972
Trachemys scripta taylori 22 +222 Pre ? Davis and Jackson 1973
Trachemys scripta troosti +22222 ? ? Conant 1938
Mauremys caspica 2+2? ? ? Pre ? Eglis 1962
Rhinoclemmys areolata 2+2+22 Pre Two Perez-Higareda and Smith 1988
Rhinoclemmys funerea ++2222 Pre ? Iverson 1975
2+++22 Pre Two Hidalgo 1982
Sacalia quadriocellata 2+2+2+Pre Two Liu et al. 2008
Chelydra serpentina 2++22 +Post All Hamilton 1940; Conant 1951
Macrochelys temminckii 22 ++22 Post Two Harrel et al. 1996
LIU ET AL. — Courtship Behavior in Freshwater Turtles 87
by experimental comparisons of courtship behavior and
success in mark-manipulated individuals.
Melanism is common in several species in the family
Emydidae (Lovich et al. 1990b), and it correlates with
courtship strategy. In Trachemys scripta scripta, levels of
sex steroids correlate with both the extent of melanism
and intensity of courtship behavior (Garstka et al. 1991),
although individuals with different extents of melanism
employ the same tactic, and the correlation may be, in
part, attributable to a problematic system of scoring
behavior. Thomas (2002) has reported that small,
nonmelanistic males use foreclaw displays in courtship
and are unlikely to bite or chase females. In contrast,
larger, melanistic males use the converse tactic. This
ontogenetic shift in courtship behavior is a conditional
strategy under status-dependent selection (Gross 1996;
Thomas 2002). These results suggest a causal relationship
between melanism (a by-product of hormonal variation)
and courtship strategy. Similarly, ontogenetic reticulate
melanism occurs in adult Chrysemys picta bellii (Gronke
et al. 2006), although it does not occur consistently in
all individuals (MacCulloch 1981). One hypothesis for
reticulate melanism is that these markings serve as visual
cues aiding in recognition of inter-specific, intersex, and
reproductive condition (Schueler 1983).
Our ability to determine the importance of markings
and pigmentation as a stimulus through unaided observa-
tions is limited. Turtles have tetrachromatic vision,
allowing them to see color in the UV end of the color
spectrum (Ventura et al. 2001). This potentially allows
them to use or react to color-related displays not visible to
humans, including the presence of UV-reflective mark-
ings. Responses to color signals are difficult to deduce
through observation, and they require experimental
testing to confirm. Future work should investigate the
effects and interactions of markings, melanism, hormone
manipulation, and female response.
NUDGING AND RUBBING
Males of many species first approach a female from
the rear, nudging (nosing and gently touching) her cloaca.
Nudging is the first observable male–female interaction
in CBFT, and it occurs widely (Table 2). In several
kinosternid species, males approach females and nudge or
nose the female’s plastral bridge (Mahmoud 1967; Seigel
1980). This behavior also plays multiple roles in
courtship, yet 2 roles occur most frequently. First,
nudging is a tactile signal that stimulates the female and
precedes the female turning to facing the male (Murphy
and Lamoreaux 1978; Hidalgo 1982; Liu et al. 2008). In
species where the male displays other precopulatory
behaviors, nudging occurs after securing the female’s
attention. Second, nudging facilitates the collection of
olfactory signals for mate recognition and female
receptivity (Kuchling 1999).
In several species, males rub their head on the
female’s carapace and head after mounting (Table 2). In
rubbing his chin on the female, the male is presumably
giving a tactile signal, but rubbing behaviors may also
facilitate transfer of scent from the male’s chin glands to
the female, therein providing a chemical signal (Manton
Male turtles of some species use their front limbs
and foreclaws during courtship. These courtship displays
include gentle stroking of the female’s head, as in Elseya
latisternum and Emydura macquarii (Murphy and La-
moreaux 1978) and the more complex foreclaw displays
of some Deirochelyinae, which are also called titillation.
Gentle stroking of the female’s head by the male’s
foreclaws is reported in several Australian pleurodire
species. During this behavior, the male positions himself
Table 2. Continued.
Species FD HM Bite Nudge Rub Gulp Disp Pos Source
Kinosternon baurii palmarum 2++++2Post Two Lardie 1975; Wilson et al. 2006
22 +++2Post All Lardie 1975
Kinosternon scorpioides 22 +2+2? ? Sexton 1960
Kinosternon sonoriense 22 +++2Post ? Hulse 1982
22 +++2Post All Mahmoud 1967
Staurotypus salvinii ???+? ? ? ? Schmidt 1970; Sachsse and Schmidt
Sternotherus carinatus 22 +++2Post All Mahmoud 1967
Sternotherus minor 2+++22 Pre All Bels and Crama 1994
Sternotherus odoratus 22 +++2Post All Lagler 1941; Mahmoud 1967
Apalone mutica 222 +22 Post All Plummer 1977
Apalone spinifera 22 ++22 Post ? Ernst and Lovich 2009
Lissemys punctata 2+2+22 Pre Two Duda and Gupta 1981
Pelodiscus sinensis 22 +??2Post ? Thieme 1979
Foreclaw display of Deirochelys reticularia involves the whole arm and is considered to be a primitive version of the foreclaw display used by other
emydid turtles (Seidel 2010).
88 CHELONIAN CONSERVATION AND BIOLOGY,Volume 12, Number 1 – 2013
in front and slightly to the side of the female and faces
her. He uses the forearm closest to the female to stroke
her head slowly; the number and frequency of strokes
varies by species (Murphy and Lamoreaux 1978; Norris
1996). A variation of this behavior is recorded in Chelus
fimbriatus where the male positions himself beside and
slightly ahead of the female, turns his head to face her and
uses the leg nearest the female to ‘‘tickle’’ her barbells
‘‘with a vibrating motion’’ (Drajeske 1983).
A different use of the male’s forelimbs is noted in
many early descriptions of emydid courtship (Table 2,
titillation). In the context of courtship, the emydid
foreclaw display is also called titillation. Titillation
consists of ‘‘a complex, stereotyped series of movements
in which the adducted forelimbs of the male are brought
parallel to the head of the female and the claws of the
forelimbs are drummed and vibrated against the eyes and
interocular region of the female’’ (Jackson and Davis
1972). Carpenter and Ferguson (1977) have explicitly
identified this as a courtship behavior, and its role in
courtship is frequent and well documented. Titillation
may or may not involve sexually dimorphic, elongated
Seidel and Fritz (1997) have classified titillation in
courting emydid turtles into 2 categories. First, the
titillation posture of Graptemys and Trachemys involves
the male facing the female directly, extending his
forelimbs, and vibrating his foreclaws near or against
her eyes and head. Second, the male Pseudemys swims
above a female’s carapace, reaches his head and forelimbs
down toward her face, and then vibrates his foreclaws.
The distinct posture of Pseudemys has been used to
support the monophyly of the genus (Seidel and Fritz
Titillation does not only function as courtship display
in emydid turtles. In some emydids, males, females, and
juveniles use foreclaw displays outside of courtship
(Kramer and Burghardt 1998, Thomas and Altig 2006).
Foreclaw display in juveniles may function as social play.
Kramer and Burghardt (1998) have reported juvenile P.
nelsoni displaying to each other and have suggested that
young turtles learn a behavior that will be used later
for courtship. The behavior also occurs in juvenile P.
concinna and P. nelsoni, which display both to each other
and to food items (Cagle 1955; Petranka and Phillippi
1978; Kramer and Burghardt 1998). Juvenile Deirochelys
reticularia exhibit a rudimentary display using the entire
arm (Krefft 1955). Thomas and Altig (2006) demonstrat-
ed that foreclaw displays of female T. scripta are not
exclusively courtship related. Foreclaw displays are likely
a compound signal with context-dependent functions
(including courtship-related male foreclaw displays or
titillation), which deserve further attention.
It has been suggested that foreclaw display such as
stroking and titillation in courtship function similarly to
biting (Murphy and Lamoreaux 1978; Hidalgo 1982;
Baker and Gillingham 1983), but the findings of Thomas
(2002) appear to contradict this scenario. In T. scripta,
young males who are much smaller than the females use
titillation. This suggests that, unless it has significantly
different functions in different species, foreclaw displays
may be more of a fitness signal than an inhibitory or
coercive tactic. Foreclaw displays in courtship involve
strong visual and tactic signals, and they may serve to
immobilize females and facilitate mounting.
From an evolutionary perspective, the complex
foreclaw displays known as titillation are considered
unique to the Deirochelyinae (Seidel and Fritz 1997)
although titillation has been lost by some members of this
subfamily. Some Mesoamerican sliders (Trachemys), such
as Trachemys gaigeae, do not use foreclaw displays
in their courtship (Seidel and Fritz 1997; Stuart and
Miyashiro 1998). Stuart and Miyashiro (1998) suggested
that nose squirting may have replaced titillation in T.
gaigeae. Deirochelys reticularia uses the whole arm in a
waving display during courtship, which is presumably a
plesiomorphic version of this behavior (Seidel 2010). A
meta-analysis can determine whether foreclaw display
is phylogenetically constrained in freshwater turtles.
Figure 1 maps foreclaw display on the phylogeny of
freshwater turtles (Seddon et al. 1997; Barley et al. 2010);
foreclaw display occurs in a phylogenetically dependent
pattern (Pearson’s chi-square test: x
521.27, df 56,
p,0.01). Further, titillation, or a rudimentary form of it,
evolves exclusively in Deirochelyinae (15 of 22 species;
68%) compared with its sister group Emydinae (1 of 6
species; 17%) (Fisher Exact Probability Test [FEPT]: 1-
tailed, p50.036; all of the percentage data can be
directly counted and calculated from Table 2).
Head movements, which are common in chelonid
courtship, may be involved with visual, tactile, and
chemical signals. Head movements can be placed in 3
general categories: 1) head bobbing (vibrating the head
and neck vertically); 2) swaying (swinging the head and
neck horizontally without contacting the female); and 3)
head movement on the female’s carapace (Fig. 2). Table 3
lists variations on courtship-related head movements.
Although types of head movement vary interspecif-
ically, this behavior is most likely used to identify
potential mates (e.g., Murphy and Lamoreaux 1978;
Baker and Gillingham 1983; Liu et al. 2008). Head
movements can function in mate recognition in several
ways. Some head movements may serve as a visual
signal, displaying important markings or colorations, for
example, as in E. blandingii (Baker and Gillingham 1983)
and S. quadriocellata (Liu et al. 2008). Although evidence
is not yet available for freshwater turtles, head bobbing
may also play a role in chemical signaling. Auffenberg
(1977) suggested that head-bobbing tortoises release
chemicals into the air for reception via rostral pores
(Winokur and Legler 1974) and mental glands (Winokur
LIU ET AL. — Courtship Behavior in Freshwater Turtles 89
and Legler 1975; Hidalgo 1982). Similar pheromone
release may also occur in freshwater turtles. Head
movements that involve contact with the female’s
carapace may also function as a tactile signal (Liu et al.
2008), and such movements may be compound signals
that have multiple functions (Bradbury and Vehrencamp
1998). Where a potential mate is successfully recognized,
head movements also function as a trigger to subsequent
behaviors (Hidalgo 1982).
In addition to head movements, E. blandingii releases
air bubbles while ‘‘frantically head-bobbing’’ (Graham
and Doyle 1979). Harrel et al. (1996) observed a similar
behavior in Macrochelys temminckii. Both species have
been observed mating both with and without bubble-
blowing (e.g., Baker and Gillingham 1983), and the
function and frequency of bubble blowing requires
clarification. It seems unlikely that the bubbles are
involved in chemical signaling, because substances
confined in the air bubbles will rapidly ascend to the
The 3 types of head movement (head bobbing,
swaying, and swaying and head bobbing on the female’s
carapace or vibrating the head and neck horizontally on
the female’s carapace) appear to have evolved indepen-
dently in freshwater turtles, and each event is phyloge-
netically constrained (Fig. 1; Pearson’s chi-square test:
519.45, d 57, p,0.01). In Pleurodira, the fre-
quency of head movement differs between Australian
species (5 of 5 species; 100%) and South American
species (3 of 9 species; 33%) (FEPT: 1-tailed,
p50.028). Similarly, the frequency of head movement
differs between species of Graptemys (6 of 10 species;
60%) and the remaining species in Deirochelyinae (2 of
16 species; 13%) (FEPT: 1-tailed, p50.017). Finally,
geoemydines (all 5 species; 100%) seem to have evolved
head movement independently from other clades (7 of 23
species; 30%) (FEPT: 1-tailed, p50.008). In addition, a
strong negative correlation occurs between the occurrence
of foreclaw display and head movement based on available
data (Phi Coefficient: Phi 520.701, p,0.001). Because
both of these behaviors were suggested to function to calm
females and facilitate mounting (Murphy and Lamoreaux
1978; Hidalgo 1982; Baker and Gillingham 1983; Liu et al.
2008), these 2 behaviors may have evolved independently
in different taxa for the same function. Further work is
required to explore this possibility.
Biting is common in the social interactions of turtles.
It has been reported in most species of freshwater turtles,
but it is not involved in courtship in all species (Table 2).
Biting in CBFT differs from aggressive male–male biting;
it most likely functions to subdue females and get them to
contract their head and limbs into the shell (Mahmoud
1967; Hidalgo 1982). Because female quiescence is
essential for copulation (Hidalgo 1982; Liu et al. 2008),
biting may play an essential role in successful mating
where it occurs. When males snap at females, they give
both visual and tactile signals. Male bites may be feigned
and end with a touch or light hit, or males may also bite
with sufficient vigor to leave scars on the females (pers.
Biting in courtship is a conserved behavior (Fig. 1).
In contrast to foreclaw display and head movement, its
evolution involves degeneration instead of diversification.
Biting is phylogenetically constrained (Pearson’s chi-
square test: x
525.72, df 56, p,0.001). In pleur-
odires, biting is conserved in South American species (6
of 9 species; 67%) but completely lost in Australian
species (0%) (FEPT: 1-tailed, p50.028). Biting is
conserved in the families Chelydridae and Kinosternidae
(15 of 19 species; 79%) but usually lost in the subfamily
Geoemydinae (1 of 5 species; 20%) (FEPT: 1-tailed,
p50.028). Finally, in the family Emydidae, biting has
degraded in the Deirochelyinae (4 of 22 species; 18%) but
may be retained in the Emydinae (4 of 6 species; 67%)
(FEPT: 1-tailed, p50.038); this is uncertain because of
the low percentage of taxon sampling. Regardless, the
statistically significant trend serves as a hypothesis for
Figure 1. Phylogenetic patterns of male courtship behavior in
freshwater turtles. The 5-point star represents biting; square
represents premounting; circle represents larger female body
size; diamond represents head movement; and triangle repre-
sents foreclaw display. Filled shapes indicate that the behavior
exists in the lineage, whereas unfilled shapes indicate absence of
the behavior from the lineage.
90 CHELONIAN CONSERVATION AND BIOLOGY,Volume 12, Number 1 – 2013
future testing. Because we have data from 4 species of
Trionychidae only, in which biting behavior occurs in 2, it
is not possible to determine the evolution of biting in this
taxon. Future work on the courtship behavior in
the Trionychidae and other groups is necessary to gain
confident insights into the evolution of biting behavior.
WATER PROPULSION: NASAL SQUIRTING
Propulsion of water toward the female or the creation
of currents around her eyes and face may function as a
tactile signal (Manton 1979). Some species show gulping
behaviors, in which water is quickly taken in and pushed
out of the mouth (Table 2). Baker and Gillingham (1983)
suggested that such behavior might be involved with
chemical signaling in conjunction with courtship in
several species of freshwater turtles. Turtles can detect
conspecific scent secretions dissolved in water (e.g.,
Mun˜oz 2004; Poschadel et al. 2006). When taken out of
the context of courtship, gular pumping in turtles may
function in olfaction (Root 1949; Manton 1979). There-
fore, it seems most likely that gular pumping is involved
with receipt (and possibly the dissemination) of olfactory
signals, as suggested by Baker and Gillingham (1983).
CHEMICAL (OLFACTORY) SIGNALS
Turtles commonly produce scents and musk, which
have multiple functions (Mertens 1946; Madison 1977;
Manton 1979). Olfactory signals can be energetically
costly, and they may provide unintentional information to
potential predators (Bradbury and Vehrencamp 1998).
Several regions of the body are associated with the
production of scent in freshwater turtles, including the
mouth, axillary and inguinal regions, cloaca, and chin
(e.g., Taylor 1933; Mahmoud 1967; Murphy and
Lamoreaux 1978; Graham and Doyle 1979; Harrel et al.
1996; Shi et al. 2002). Because very little is known about
the function of scent in CBFT, we have not produced an
exhaustive list of species known to produce scent.
However, chemical cues likely function in mate recogni-
tion, and some works have shed light on this relationship.
Differences in scent production occur between males
and females of some species (Worrell 1963; Goode 1967;
Schmidt 1970; Sachsse and Schmidt 1976). Mahmoud
(1967) has observed that males of four kinosternid species
can correctly distinguish females from males and
determine whether or not to attempt courtship and mating
behavior by sniffing at the cloaca. Hidalgo (1982) found
that the cloacal scent produced by female R. p. incisa can
Figure 2. Three types of head movement associated with premounting courtship displays in freshwater turtles. A) Head bobbing:
vibrating the head and neck vertically (modified from Hidalgo 1982). B) Swaying: vibrating the head and neck horizontally (modified
from Bels and Crama 1994). C) Swaying on the female’s carapace: vibrating the head and neck horizontally on the female’s carapace
(modified from Baker and Gillingham 1983).
LIU ET AL. — Courtship Behavior in Freshwater Turtles 91
elicit trailing behavior in males. Thus, the current
evidence suggests that at least some female turtles
produce secretions that can induce sniffing behavior,
potentially enabling them to signal receptivity. Many
other species also precede courtship with the male trailing
the female and sniffing at her cloaca, apparently to detect
a chemical releaser (e.g. Marchand 1944; Jackson and
Davis 1972; Plummer 1977; Kramer and Fritz 1989;
Norris 1996; Liu et al. 2008).
Experimental evidence provides support for olfactory
signals functioning in intersexual and interindividual
discrimination. Poschadel et al. (2006) demonstrated that,
although female E. orbicularis show no preference to
scents from other turtles, males prefer the scent of females
to that of other males or unscented water. Furthermore,
these males prefer the scent of larger females to that of
smaller females, and males prefer water scented by smaller
males to that scented by larger males. Mun˜oz (2004) has
reported similar results for Mauremys leprosa. Lewis et al.
(2007) found that male Sternotherus odoratus prefer water
scented by females to water scented by themselves, other
males, or no turtles. Thus, these species can use chemical
signals, both to seek out mates and to avoid competition.
Presumably other species can do the same.
Chemical signals are difficult to detect and quantify,
but the assumption that species not displaying a set of pre
mounting behaviors (e.g., some kinosternids) have a
simpler courtship ritual than species that use many visual
or tactile signals (e.g., Miller and Dinkelacker 2008)
should be avoided. It is possible that these ‘‘simpler’’
courtship rituals involve very complex but less easily
detected olfactory signals. Thus, we recommend that the
categorizations ‘‘simple’’ or ‘‘complex’’ be avoided, at
least until a greater understanding of signaling is in hand.
Likewise, the assumption that turtles smell when touching
or approaching objects is justifiable but difficult to test
(Manton 1979). Nosing and touching are universally
interpreted as a chemical collection functions in CBFT
(e.g., Hidalgo 1982; Bels and Crama 1994; Liu et al.
2008). We recommend the use of chemical manipulation
experiments to reveal the function of chemical signals in
Auditory signals in CBFT are virtually unknown, and
turtle vocalizations have only recently become a topic of
organized research. Vocalizations have been reported in
Table 3. Variable forms of head movement in male freshwater species. Head movements are classified into 3 types: HB, head-
bobbing; S, swaying; and SOFC, swaying on the female’s carapace. Details of the classification and descriptions are provided in text
and Fig. 2.
Species Form of head movement Type Source
Acanthochelys pallidipectoris Prodding female’s head and neck from top of her back SOFC Horne 1993
Chelodina expansa Dorsoventral movement of fully extended head HB Legler 1978
Chelodina longicollis Swaying on female’s carapace SOFC Murphy and Lamoreaux 1978
Chelus fimbriatus Swaying in front of female S Drajeske 1983
Chelydra serpentina Swaying head sided to side in front of female S Ernst and Lovich 2009
Mauremys caspica Vibrating the ventral neck on female’s dorsal head HB Eglis 1962
Emydoidea blandingii Swaying while mounted on the female’s carapace SOFC Baker and Gillingham 1983
Frantic head bobbing HB Graham and Doyle 1979
Elseya latisternum Dorsoventral head bobbing HB Murphy and Lamoreaux 1978
Emydura macquarii Vigorous head-bobbing in a dorsoventral plane HB Murphy and Lamoreaux 1978
Emydura subglobosa Head bob in dorsa-ventral plane HB Norris 1996
Glyptemys insculpta Face the female bob or sway its head (?) ? Carr 1952; Ernst and Lovich 2009
Graptemys ernsti Rapidly vibrates head vertically against the female’s
snout, alternating sides
HB Ernst and Lovich 2009
Graptemys geographica Makes snout-to-snout contact, then rapidly bobs
head up and down
HB Ernst and Lovich 2009
Graptemys kohni Bobbing head on either side of female’s jaws HB Murphy and Lamoreaux 1978
Graptemys ouachitensis Vertical head bobbing followed by nose-to-nose
HB Ernst and Lovich 2009
Graptemys pulchra Vibrating vertically in a snout-to-snout position HB Shealy 1976
Lissemys punctata Bob head in vertical plane HB Duda and Gupta 1981
Platemys platycephala Brush head across the female while mounted, swinging
head rapidly on the top of female’s back
SOFC Harding 1983; Medem 1983
Pelomedusa subrufa Swinging head on the top of female’s back SOFC Harding 1981
Rhinoclemmys funerea Vibrating the head in a sagittal plane HB Iverson 1975
Rhinoclemmys pulcherrima Head and neck vibration HB Hidalgo 1982
Sacalia quadriocellata Vibrating its head and fore-body in a vertical plane HB Liu et al. 2008
Kinosternon baurii Extending neck and bobbing head up and down at
about one bob per second
HB Wilson et al. 2006
Sternotherus minor Facing female, swinging the head from side to side S Bels and Crama 1994
Trachemys gaigeae Rapid, jerky nodding or bobbing, accompanied with
side-to-side wagging head motion
S Stuart and Miyashiro 1998
Malaclemys terrapin Head bobbing in front of female HB Seigel 1980
Mesoclemmys vanderhaegei Sliding his head from one side to the other in short
and fast movements on the top of female’s back
SOFC Brito et al. 2009
92 CHELONIAN CONSERVATION AND BIOLOGY,Volume 12, Number 1 – 2013
Pseudemys concinna suwanniensis (Rose 1950), but at the
time of this publication, turtles were generally considered
incapable of giving or receiving auditory stimuli (Pope
1955). Weaver and Vernon (1956) confirmed that many
turtle species are, in fact, sensitive to airborne sounds,
particularly sounds below 1000 Hz. Vocalizations are
well-known in male tortoises and can play an important
role in mate choice (Auffenberg 1977; Galeotti et al.
2005). However, the first published recordings of
underwater turtle vocalizations are from Chelodina
oblonga (Giles et al. 2009). These include a large
repertoire of calls including a potential advertisement
call that was recorded only during the breeding season.
Other anecdotal evidence for auditory signals in fresh-
water turtle courtship includes the whistles sometimes
produced by Glyptemys insculpta (Kaufmann 1992)
and vocalizations reported by Liu et al. (2009) in S.
quadriocellata. Both of these occurrences appear to be
infrequent; therefore, the role vocalizations may play in
CBFT is unknown. The potential importance of auditory
signals in CBFT, and in general communication, is in
need of study.
OTHER ACTIVE BEHAVIORS
Three other behaviors are involved in CBFT.
Although all of them are distinguishable in courtship,
they occur in few species, and their functions remain
Barbel Contact. — Murphy and Lamoreaux (1978)
have observed barbel contact and barbel stroking during
courtship in E. latisternum and E. macquarii. Males of
both species attempt to align their barbels with those of
the females and stroke the female’s barbels with their
forefeet and claws. The barbels are thought to be
extremely sensitive, but their exact function(s) remains
unknown. Barbel contact and stroking are most likely
tactile signals, but what information they might transmit
Blinking. — Blinking of the eyes appears to be a
courtship signal in female T. scripta (Lovich et al. 1990a)
and in male Emydura subglobosa (Norris 1996). In both
cases, blinking occurs during premounting orientation
and display. The authors of these two studies consider
blinking to be a visual signal, although its function
Shell Clapping. — Shell clapping occurs in G.
insculpta (Evans 1961; Kaufmann 1992; Tronzo 1993;
Mitchell and Mueller 1996). After mounting, the male
grasps the female’s carapace with all 4 feet. By extending
his legs and then quickly pulling himself down toward the
female, the male’s plastron crashes against the female’s
carapace making a loud ‘‘clapping’’ noise. This aggres-
sive behavior may exhaust the female and coerce her into
accepting intromission. However, biting, shaking, and
thumping do not guarantee insemination (Kaufmann
1992). Alternatively, this behavior may provide a signal
of the male’s fitness based upon which the female accepts
or rejects his intentions.
Shell clapping is potentially a tactile and/or auditory
signal. Further, the repeated rapid contact between the
male’s plastron and the female’s carapace may cause the
male to produce scent from the glands in his inguinal and
axillary areas, providing a possible olfactory signal.
Unfortunately, the function of shell clapping has not yet
The releasing of behavior normally depends on a
combination of signals, and CBFT is not an exception. In
this section, we reviewed the signals that might be used to
communicate between two sexes. However, the signal
from external environment, which is almost totally
ignored in this field, also plays an important role to
trigger courtship. A well-known fact among researchers
and turtle breeders alike is that an influx of fresh water,
for example from rainfall or snowmelt, can stimulate
courtship and mating behaviors. This phenomenon has
been observed in a variety of species, including
kinosternids (Mahmoud 1967), Lissemys punctata (Duda
and Gupta 1981), and Acanthochelys pallidipectoris
(Horne 1993). Environmental stimuli such as rainfall or
snowmelt may trigger hormonal changes that elicit
courtship behaviors (Woolley et al. 2004). Therefore,
future work should also pay attention to the interaction
between courtship behavior and environmental signals.
MOUNTING AND COPULATORY POSITIONS
Mounting is a critical stage in courtship because
refusal by the female will result in failure. When a female
tries to dislodge the male by moving away, he may lose
his position on the carapace (Mahmoud 1967; Murphy
and Lamoreaux 1978; Hidalgo 1982; Baker and Gilling-
ham 1983; Bels and Crama 1994). Mounting is frequently
followed not by copulation but by female refusal (e.g.,
Murphy and Lamoreaux 1978; Baker and Gillingham
1983; Liu et al. 2008). Males can mount females from any
direction, and males typically adjust their position after
mounting (Mahmoud 1967; Murphy and Lamoreaux
1978; Hidalgo 1982; Bels and Crama 1994; Liu et al.
Copulatory positions in turtles involve 2 male
postures (Fig. 3). Males grasp a female’s carapace either
with all 4 limbs or with the forelimbs while placing the
hind limbs firmly on the substrate. Generally, species in
the Chelidae, Emydidae, and Kinosternidae do the former
and the other species the latter (Table 2). Mounting and
copulation may involve specialized grasping structures.
For example, Mahmoud (1967) reported that smaller
males of sexually dimorphic kinosternids use scaly
patches on their hind limbs to fix the female’s tail in
place and has suggested that this makes the female’s
cloaca accessible for copulation. However, Gibbons and
Lovich (1990) pointed out that these structures are more
likely to ease the physical difficulty of attaining
LIU ET AL. — Courtship Behavior in Freshwater Turtles 93
intromission than to forcibly hold the female in any given
position. Usually when aquatic turtles copulate, the
male’s plastron contacts the female’s carapace, but this
is not always the case. Copulatory postures may differ
within species. For example, Kaufmann (1992) reports
plastron-to-carapace mating in a population of G.
insculpta, whereas Tronzo (1993) and Mitchell and
Mueller (1996) observed plastron-to-plastron mating.
The same variation occurs in Chelydra serpentina (Pisani
2004; Ernst and Lovich 2009). Recently, Joyce et al.
(2012) published the first observation of mating in a fossil
turtle (or in any fossilized vertebrate). Regrettably, the
condition of the fossils made it impossible to determine
whether the turtles (Allaeochelys crassesculpta) were
mating in the plastron-to-plastron or plastron-to-carapace
FEMALE PARTICIPATION IN COURTSHIP
Typically, female courtship behavior in turtles is less
obvious to a human observer than that of males, and as a
result, details are often wanting. However, several
interesting female courtship and mating behaviors have
been reported. For example, Murphy and Lamoreaux
(1978) observed female E. latisternum pivoting 180usuch
that males and females end up side by side facing in
opposite directions, and female head-bobs follow those
of males. Hidalgo (1982) reported active nose-to-nose
contact and biting by female R. p. incisa. Lovich et al.
(1990a) have observed female T. scripta orienting toward
males, performing foreclaw displays, and eye-blinking at
Some authors assert that females may play passive
roles during courtship (Taylor 1933; Jackson and Davis
1972), whereas others dispute this claim. Harless (1979)
stated that the success or failure of an attempted mating
ultimately rests on the female because copulation is not
possible if the female turtle does not allow it. Several
observations support this suggestion. For example, although
male E. blandingii initiate courtship, ultimately females
decide to accept or reject the male’s advances (Baker and
Gillingham 1983). Failure to extend her tail after the male’s
swaying behavior results in unsuccessful mating, despite the
sometimes quite agitated persistence by rejected males.
Several authors suggested that coercion and forcible
insemination may play important roles in some species
(Berry and Shine 1980; Lee and Hays 2004; Refsnider
2009), but as discussed below, this is difficult to test.
Males of some species appear to be especially
aggressive toward females. When copulation occurs
following apparently aggressive signals, such as biting
or shell clapping, it can be difficult to objectively identify
the specific signal(s) that led to the female’s acceptance
of the male. Furthermore, it is impossible to determine
whether the female is ‘‘choosing’’ to mate or simply
‘‘giving in’’ to coercion. Female turtles disinclined to
mate typically flee, bite the suitor, or bite and chase the
pursuer (Plummer 1977; Murphy and Lamoreaux 1978;
Liu et al. 2008). Murphy and Lamoreaux (1978) reported
that female E. macquarii often bite courting males;
successful copulation does not follow biting. Liu et al.
(2008) reported that female S. quadriocellata sometimes
actively turn to face approaching males and occasionally
bite at courting males. Given the absence of mounting or
copulation, it is uncertain whether these signals are
related to courtship, nonreceptivity, or receptivity fol-
lowed by termination of courtship in response to some
Berry and Shine (1980) suggested that females may
require suitors to coerce or slowly convince them to mate
and that this may be a form of selection in which females
maximize their reproductive fitness by mating only with
extremely persistent males. Refsnider (2009) suggested
that female E. blandingii exhibit ‘‘convenience polyan-
dry’’, in which they accept a mate simply to avoid further
harassment. A similar argument has been made by Lee
and Hays (2004) to explain patterns of polyandry in the
marine green turtle, Chelonia mydas. However, the
hypotheses that every female wants to mate but requires
the male to prove himself first, or that females are
acquiescing to avoid harassment, are untestable because
motivation of the female is unknown and untestable. For
Figure 3. The 2 major copulation postures used by freshwater turtles. A) Male grasps the female’s carapace with all 4 feet (modified
from Mahmoud 1967). B) Male grasps the female’s carapace with his forelimbs and supports his body with his hind limbs planted on
the substrate (modified from Hidalgo 1982).
94 CHELONIAN CONSERVATION AND BIOLOGY,Volume 12, Number 1 – 2013
example, although fleeing may indicate nonreceptivity, in
some cases a fleeing female may move away from the
courting male and then return to him and resume walking
away (Harless 1979). Therefore, there is potential for an
observer to confuse a fleeing female with one attempting
to elicit a following response from a male. The argument
that coercion is prevalent in the CBFT is common (Berry
and Shine 1980; Refsnider 2009), but we suggest that
acceptance of this untestable premise may lead to a biased
interpretation of observed courtship behavior.
Behavioral evidence for coercion is unconvincing,
at least in the case of E. blandingii. Males are not
particularly aggressive to females, and biting is far less
prevalent in their mating ritual than in some other species
(e.g., kinosternids). Mating is costly to female turtles
because they lose foraging time, run an increased risk of
predation during mating, and risk injury from aggressive
males; thus, females may not benefit from multiple
mating (Uller and Olsson 2008). The frequency with
which studies of courtship behavior report repeated
courtship attempts but fail to observe that a single
copulation suggests that females of at least some species
are perfectly capable of being choosy (Ernst 1974; Arndt
1977; Murphy and Lamoreaux 1978, for E. macquarii;
Kramer and Fritz 1989; Norris 1996). For some
chelonians, polyandry and multiple paternities are more
common than not (Uller and Olsson 2008; Davy et al.
2011). The benefits seem to outweigh the risks, and this
suggests that coercion is not involved.
The question of female choice may be easier to
address in groups such as the Trionychidae, where
females are significantly larger than males and males of
some species apparently are not aggressive toward
females (e.g., Apalone mutica and L. punctata). In this
family, coercion of females by males is unlikely.
Unreceptive female trionychids bite viciously, and males
run a risk of serious injury (Plummer 1977; Ernst and
Lovich 2009). In both A. mutica and L. punctata, males
are physically incapable of mounting and attaining
intromission if the female does not settle calmly on the
substrate (Duda and Gupta 1981, Ernst and Lovich 2009).
Thus, biting of males by females appears to signal
nonreceptivity in these species, and they may be good
models for experimental investigation of factors influ-
encing female mate choice.
Successful courtship requires the participation of
both sexes. Thus, the courtship behaviors of female turtles
are of great importance. Ultimately, females may
determine successful copulation. Ignorance of the fe-
male’s role in courtship precludes an understanding of
male behaviors; a signal must have a receiver to function,
and the efficacy of the signal depends largely on its
reception (Bradbury and Vehrencamp 1998). Thus,
complete models of courtship behavior must involve
consideration of both sexes’ behaviors and the interac-
tions between them. Such models will allow us to
investigate the evolution of different mating behaviors.
EVOLUTION OF MALE COURTSHIP BEHAVIOR
IN FRESHWATER TURTLES
Berry and Shine (1980) provided the first study of the
evolution of male courtship behavior. They suggested that
less courtship and coercion or forceful insemination of
females should occur in species where males are the
larger, whereas smaller males should display more
elaborate courtship behaviors. Gibbons and Lovich
(1990) reject this suggestion in part because forcible
insemination is not plausible because of difficulties a
male turtle would encounter for achieving intromission
with an unreceptive female, and we agree. However, if an
aggressive behavior such as biting either calms females or
functions in mate choice and subsequent mounting
behavior, then aggression may be an effective strategy
for successful mating. Bels and Crama (1994) also
rejected the model on the basis that mate choice cannot
be objectively inferred from observed behaviors because
they can be interpreted in more than one way. They
divided male courtship behavior into 3 categories:
premounting courtship, intermediate courtship, and
mounting courtship. However, Bels and Crama’s (1994)
3 categories and Berry and Shine’s (1980) argument are
not mutually exclusive. Thus, we performed a set of meta-
analyses to better understand the evolution of male CBFT.
Biting, foreclaw display, and head movement appear
to calm females and facilitate mounting (Murphy and
Lamoreaux 1978; Hidalgo 1982; Baker and Gillingham
1983; Liu et al. 2008). Foreclaw display and head
movement have evolved independently in certain taxa,
whereas biting degenerated in some branches of the
phylogenetic tree, as discussed above. To determine
whether the evolution of foreclaw display and head
movement coincides with the degeneration of biting
behavior, we tested whether foreclaw display and head
movement replace biting from a phylogenetic perspective.
Our meta-analysis obtained a very strong, highly
significant negative correlation between these two
strategies (Phi coefficient: Phi 520.713, p,0.001),
which suggests that foreclaw displays and head movement
have evolved to replace biting in certain lineages of
We cannot directly test the female-choice model
of Berry and Shine (1980), yet we can independently
evaluate the three display types described by Bels and
Crama (1994) relative to Berry and Shine’s (1980) model.
To perform this meta-analysis, we collapsed the 3 display
types into 2: premounting displays and postmounting
displays. We redistribute species into these types based on
the timing of the behaviors (Table 2). The meta-analysis
resolved highly significant phylogenetically dependent
display types (Pearson’s chi-square test: x
df 56, p,0.001), suggesting that postmounting might
be plesiomorphic (Fig. 1). In pleurodires, postmounting
courtship is replaced by premounting courtship in
Australian species (1 of 5 species; 20%), and postmount-
LIU ET AL. — Courtship Behavior in Freshwater Turtles 95
ing courtship behaviors are conserved in South American
species (8 of 9 species; 89%; FEPT: 1-tailed, p50.023).
Postmounting displays persist in the Trionychidae,
Chelydridae, and Kinosternidae (19 of 22 species; 86%)
but are replaced by premounting in the subfamily
Geoemydinae (0%; FEPT: 1-tailed, p,0.001). In the
Emydidae, premounting has evolved in the subfamily
Deirochelyinae (postmounting in 1 of 10 species; 10%),
whereas postmounting has been retained in the Emydinae
(4 of 5 species; 80%; FEPT: 1-tailed, p50.017). The
evolution of display type coincides with the phylogenetic
degeneration of biting behavior. Our meta-analysis
detects a highly significant negative correlation between
biting and premounting (Phi coefficient: Phi 520.507,
p,0.001). In other words, premounting usually accom-
panies nonbiting courtship. Therefore, Berry and Shine’s
(1980) theory regarding mating strategy and Bels and
Crama’s (1994) theory regarding display type involve
different aspects of the evolution of CBFT but are not
Berry and Shine’s (1980) model of male mating
strategy is based on a meta-analysis that includes tortoises
and sea turtles, which we do not consider. Our meta-
analysis only considers freshwater turtles, and it incorpo-
rates a larger data set (Table 2). Because we only consider
aquatic species, habitat diversity is not a variable in the
analysis. Analyses of sexual dimorphism involve binary
data with females being larger than males or not. Display
type (pre- or postmounting) is indicative of mating
strategy because of the intrinsic correlation among display
type and other courtship behaviors, such as biting,
foreclaw displays, and head movements, as discussed
above. Our meta-analysis resolved a highly significant
positive correlation between larger female (relative to
male body size) and a less aggressive courtship strategy
involving foreclaw displays and head movements instead
of biting (Phi coefficient: Phi 50.660, p,0.001). Thus,
males tend to adopt a less aggressive mating strategy in the
taxa where adult females are larger than males. This result
is consistent with Berry and Shine’s (1980) models for
mating strategy and sexual dimorphism.
To identify the drivers of CBFT, we have analyzed
the evolution of sexual dimorphism from a phylogenetic
perspective. Sexual dimorphism data are from Berry and
Shine (1980) and Ernst and Lovich (2009). Sexual
dimorphism appears to be phylogenetically dependent
(Pearson’s chi-square test: x
536.34, df 56,
p,0.001). Thus, larger female body size appears to be
an apomorphic and homoplastic trait that evolved
independently in some taxa (Fig. 1). In Pleurodira, larger
female body size evolved in Australian species (100%)
but not in South American species (0%; FEPT: 1-tailed,
p50.014). Larger or equal body size in males is
conserved in the Chelydridae and Kinosternidae (11 of
14 species; 79%) but replaced by larger females in the
Trionychidae (0%; FEPT: 1-tailed, p50.011) and the
Geoemydinae (1 of 5 species; 20%; FEPT: 1-tailed,
p50.038). Within the Emydidae, larger female body
size evolves in the Deirochelyinae rather than the
Emydinae (FEPT: 1-tailed, p,0.001). The evolutionary
pattern for sexual dimorphism essentially parallels the
evolution of display type, mild courtship behaviors,
including foreclaw display, head movement, and the loss
of biting behavior. Further, display types are highly
significantly correlated with sexual dimorphism (Phi
coefficient: Phi 520.635, p,0.001).
Our analyses suggest that the evolution of courtship
behavior in male freshwater turtles might accompany the
evolution of sexual dimorphism, which is directly subject
to natural selection. In the evolutionary history of
freshwater turtles, larger female body size has evolved
in the more recent taxa, such as some Emydidae and
Geoemydidae. Larger female body size can increase
fecundity, whereas smaller male body size can benefit
male dispersal. Both scenarios appear to promote
reproductive efficiency (Ghiselin 1974). Accordingly,
males of species where the male is the smaller sex have
adjusted their display type from post- to premating
courtship and adjusted their mating tactic from aggressive
to mild. Because successful copulation requires a female
to acquiesce (Gibbons and Lovich 1990; Liu et al. 2008),
relatively smaller males may increase mating success by
adopting the less aggressive strategy (Berry and Shine
RECOMMENDED FUTURE DIRECTIONS
Publish Natural History Data. — Although progress
has been made in understanding the courtship behavior of
freshwater turtles, we are left with pleas made more than
30 yrs ago. Carpenter and Ferguson (1977) and Harless
(1979) discussed the need to report behavioral observa-
tions to build a knowledge base. This need remains.
Courtship data are available for a few species only, and
most of these observations are incomplete, because many
consist of one or two courtship episodes in one pair only.
Isolated observations of CBFT do not allow for statistical
analysis of the significance of the observation in terms of
specific hypothesis testing. However, they have great
value as the first records of either new behaviors or
previously described behaviors in species for which no
data exist. Such reports continue to suggest new directions
for study. We strongly encourage future work on species
either with no observation of courtship behavior or only
anecdotal descriptions. Observations of courtship in
cryptic species are difficult at best, and we encourage
researchers who are fortunate enough to witness such
events to publish their observations. Combined, these
observations can guide hypothesis testing into a species’
Focus on Hypothesis Testing. — Although the
literature on turtle courtship has grown significantly and
continues to do so, almost nothing is known about the
96 CHELONIAN CONSERVATION AND BIOLOGY,Volume 12, Number 1 – 2013
functions of courtship signals, their interactions, or the ways
in which courtship behavior influences mate choice or
reproductive success in turtles. Even among studies with
large sample sizes and statistical strength, most do not test
hypotheses about courtship, communication, or mate choice,
with notable exceptions, such as Garstka et al. (1991),
Thomas (2002), and Thomas and Altig (2006). Future
studies should aim to elucidate the function of courtship
signals through experiments that evaluate the response of
turtles receiving signals of different strengths and quality.
Description and Statistical Methods. — Disorder in
applying techniques hinders progress in certain research
fields, especially in behavioral studies (Liu et al. 2009).
Often the same behavior is described differently in two
papers, and this tendency leads to confusion. We have
scanned the literature, gleaned data, and applied universal
terms to identify courtship signals. Thus, we encourage
the use of these terms rather than the creation of new
terms to describe behavior. Because robust statistical
methods are available for sequential analyses, quantified
courtship studies have yielded useful behavioral models
and hypotheses (Baker and Gillingham 1983; Bels and
Crama 1994; Liu et al. 2008). We recommend improving
the quality and standardization of data by quantifying the
duration and frequency of each behavioral pattern in the
courtship sequence. These new data will be useful not
only to investigate the importance and function of certain
behaviors in courtship but also to provide data for more
robust comparison between studies.
Research into the courtship behavior of freshwater
turtles has succeeded in identifying a number of courtship
signals used by many species of turtles. Many behaviors
appear to be phylogenetically constrained; they have
evolved in the common ancestor of lineages and persist
in the descendants. However, the database is far from
complete, and hypotheses require further testing with data
from additional species. The priority in the coming years
should be to start testing hypotheses regarding the
reception and function of these signals. Three areas
require particular attention. First, hypothesis testing
requires a comparative biology perspective. A phyloge-
netic approach can lead to predictions of behavioral
patterns in species whose courtship behavior is complete-
ly unknown. Second, an experimental approach is
required to clarify further the functions of specific male
behaviors. Finally, the role played by female turtles in
courtship and mate choice requires investigation to
identify the ways in which females receive male courtship
signals and the signals they may send to the male. No
doubt, the age of genomics will open many new
opportunities (Haussler et al. 2009). Future studies may
be able to identify the genes involved in controlling
Amy Lathrop prepared all figures, and K. Bianco,
J. Fong, and J. Wang helped to glean literature. We thank
M. Dloogatch for access to back issues of the Bulletin of
the Chicago Herpetological Society. J.-C. Wang, L.-R.
Fu, M.-L. Hong, L.-J. Wang, B. He, Y.-G. Ma, M.-G. Hu,
L.-Y. He, Q. Chen, J. Zhang, C. Li, Y. An, and X.-P. Pang
provided valuable assistance. An earlier version benefited
greatly from suggestions made by R.B. Thomas and an
anonymous reviewer. This research is supported in part by
the Natural Science Foundation of China (30910103916),
Hainan Key Project of Science and Technology. Interna-
tional collaboration was supported by Cleveland Zoo.
Grants to R.W.M. were received from the Board of
Governors, Royal Ontario Museum, the Natural Sciences
and Engineering Research Council of Canada (NSERC
Discovery Grant 3148), and a Visiting Professorship
for Senior International Scientists from the Chinese
Academy of Sciences. C.M.D. received an NSERC
Canadian Graduate Scholarship.
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Received: 1 May 2010
Revised and Accepted: 6 January 2013
Handling Editors: Anders G.J. Rhodin and Jeffrey A. Seminoff
100 CHELONIAN CONSERVATION AND BIOLOGY,Volume 12, Number 1 – 2013