Understanding sexual size dimorphism in snakes: wearing the snake's shoes

Abstract

S exual size dimorphism (SSD) is widespread in almost every group of animals, generating great scientific interest (Andersson 1994). Most research has been on species in which males are larger than females. Expla-nations tend to focus on the advantages of size for direct male–male competition over access to fertile females or resources needed by females for reproduction. However, this explanation has been more difficult to apply to snakes where SSD is often extreme and female biased and in which intraspecific aggression, dominance hierarchies and territoriality are rare. Although relatively large males have been shown to have a greater mating success in some species (Shine 1978; Shine 1993; Madsen & Shine 1994), they have not in others (Madsen & Shine 1993; Madsen et al. 1993; Weatherhead et al. 1995). Recently Shine et al. (2000) and Crews (2000) discussed conflicting evidence on the role of male body size in mating success in common garter snakes, Thamnophis sirtalis, in this forum, but were unable to resolve the different empirical results. Sometimes scientific assumptions or ingrained points of view may hinder recognition of other possibili-ties. Here we discuss an alternative approach to generat-ing testable hypotheses: critical anthropomorphism (Burghardt 1991). By using critical anthropomorphism we propose a new hypothesis that has the potential to settle this controversy. Jacob von Uexküll (1909/1985) advocated studying the behaviour of animals by considering both their inner world (Innenwelt) and how they perceived and responded to their environment (Umwelt). A major aspect of this approach was to evaluate differences among species in the salience of biologically relevant perceptual cues (Tinbergen 1951; Burghardt 1985). Recent proposals to study animal cognition focus on the ways that animals perceive, interpret and experience the world (Griffin 1978; Cheney & Seyfarth 1992; Glotzbach 1992; Burghardt 1997; Bekoff & Allen 1997). An important component of this approach, although often understated, is to consider the animal being studied as an active participant, with the researcher trying to put him or herself in the animal's situation. This is especially true for those studying primate behaviour (Herzog & Galvin 1997). Timberlake & Delamater (1991) proposed that to understand the behaviour of an animal 'Experimenters not only need to put themselves in the subject's shoes, they need to wear them—walk, watch, hear, touch and act like the subject' (page 39). One approach to doing this and still maintaining scientific rigour is to apply a critical anthropomorphism in which hypotheses are based on existing scientific knowledge about the species being studied as well as considering the 'shoes' (point of view) of other organisms (Burghardt 1991). We apply this method to the maintenance of female biased SSD in snakes, where males compete physically for access to females in the context of actual mating. In most snake species females are larger than males, reversing the typical terrestrial vertebrate pattern where males are of equivalent or larger size than females (Shine 1994). Large size in female snakes is considered adaptive in species that grow throughout life with little or no parental care, and in which larger females produce more and/or larger offspring. Larger offspring have higher survival rates and can store more yolk or fat for their development (see Ford & Seigel 1989 for a review). Natural selection should, therefore, favour large size in females. Male snakes, on the other hand, benefit from traits that enhance their ability to find and successfully court females (Table 1). Thus, refined chemosensory senses, high mobility, being inconspicuous to predators, early maturation, small size and decreased costs of loco-motion would be adaptive (Duvall et al. 1993; Madsen et al. 1993; Shine 1993; Andersson 1994).

Full text

ANIMAL BEHAVIOUR, 2001, 62, F1–F6
doi:10.1006/anbe.2001.1755, available online at http://www.idealibrary.com on
FORUM
Understanding sexual size dimorphism in snakes: wearing the
snake’s shoes
JESUuS A. RIVAS* & GORDON M. BURGHARDT*†
*Department of Ecology and Evolutionary Biology and †Department of Psychology, University of Tennessee
(Received 24 December 2000; initial acceptance 3 January 2001;
final acceptance 30 January 2001; MS. number: AF-14)
Sexual size dimorphism (SSD) is widespread in almost
every group of animals, generating great scientific
interest (Andersson 1994). Most research has been on
species in which males are larger than females. Expla-
nations tend to focus on the advantages of size for direct
male–male competition over access to fertile females or
resources needed by females for reproduction. However,
this explanation has been more difficult to apply to
snakes where SSD is often extreme and female biased and
in which intraspecific aggression, dominance hierarchies
and territoriality are rare. Although relatively large males
have been shown to have a greater mating success in
some species (Shine 1978;Shine 1993;Madsen & Shine
1994), they have not in others (Madsen & Shine 1993;
Madsen et al. 1993;Weatherhead et al. 1995). Recently
Shine et al. (2000) and Crews (2000) discussed conflicting
evidence on the role of male body size in mating success
in common garter snakes, Thamnophis sirtalis, in this
forum, but were unable to resolve the different empirical
results. Sometimes scientific assumptions or ingrained
points of view may hinder recognition of other possibili-
ties. Here we discuss an alternative approach to generat-
ing testable hypotheses: critical anthropomorphism
(Burghardt 1991). By using critical anthropomorphism
we propose a new hypothesis that has the potential to
settle this controversy.
Jacob von Uexku¨ ll (1909/1985) advocated studying the
behaviour of animals by considering both their inner
world (Innenwelt) and how they perceived and
responded to their environment (Umwelt). A major
aspect of this approach was to evaluate differences among
species in the salience of biologically relevant perceptual
cues (Tinbergen 1951;Burghardt 1985). Recent proposals
to study animal cognition focus on the ways that animals
perceive, interpret and experience the world (Griffin
1978;Cheney & Seyfarth 1992;Glotzbach 1992;
Burghardt 1997;Bekoff & Allen 1997). An important
component of this approach, although often understated,
is to consider the animal being studied as an active
participant, with the researcher trying to put him or
herself in the animal’s situation. This is especially true for
those studying primate behaviour (Herzog & Galvin
1997). Timberlake & Delamater (1991) proposed that to
understand the behaviour of an animal ‘Experimenters
not only need to put themselves in the subject’s shoes,
they need to wear them—walk, watch, hear, touch and
act like the subject’ (page 39). One approach to doing this
and still maintaining scientific rigour is to apply a critical
anthropomorphism in which hypotheses are based on
existing scientific knowledge about the species being
studied as well as considering the ‘shoes’ (point of view)
of other organisms (Burghardt 1991). We apply this
method to the maintenance of female biased SSD in
snakes, where males compete physically for access to
females in the context of actual mating.
In most snake species females are larger than males,
reversing the typical terrestrial vertebrate pattern where
males are of equivalent or larger size than females (Shine
1994). Large size in female snakes is considered adaptive
in species that grow throughout life with little or no
parental care, and in which larger females produce more
and/or larger offspring. Larger offspring have higher
survival rates and can store more yolk or fat for their
development (see Ford & Seigel 1989 for a review).
Natural selection should, therefore, favour large size in
females. Male snakes, on the other hand, benefit from
traits that enhance their ability to find and successfully
court females (Table 1). Thus, refined chemosensory
senses, high mobility, being inconspicuous to predators,
early maturation, small size and decreased costs of loco-
motion would be adaptive (Duvall et al. 1993;Madsen
et al. 1993;Shine 1993;Andersson 1994).
Correspondence and present address: J. A. Rivas, 17126 Lawson
Valley Road, Jamul, CA 91935, U.S.A. G. M. Burghardt is at
the Department of Psychology, University of Tennessee, Knoxville,
TN 37996-0900, U.S.A.
0003–3472/01/0900F1+06 $35.00/0 2001 The Association for the Study of Animal BehaviourF1

Female biased SSD is probably the ancestral condition
of snakes as a group (Rivas 2000). Thus, smaller size in
males can be explained by the lack of selection pressure
towards large body size (Semlitsch & Gibbons 1982).
Unlike lizards, their sister squamate taxa, territoriality has
not been reported in snakes, and male–male fighting is
also uncommon. Thus, selection forces for large male size
are generally lacking (Shine 1993). However, in con-
ditions of high density, where females are very easy to
track, or where females do not breed every year, several
males would encounter each other while courting a
female and male–male combat is likely to evolve (Shine
1978,1993;Duvall et al. 1992). The relationship between
male–male fighting and male size in snakes has been
discussed broadly (Shine 1978,1993;Madsen et al. 1993;
Madsen & Shine 1994). If larger males are more successful
in combat and obtain more matings than smaller males,
large size in males would be favoured by selection. Male
combat is much more frequent in snake species where
males are larger than females or where SSD is absent
(Shine 1994).
There are, however, some species where sexual selec-
tion appears to favour male biased SSD, yet males are not
larger than females (Madsen et al. 1993;Madsen & Shine
1993;Weatherhead et al. 1995). Grass snakes, Natrix
natrix, breed in mating balls where males wrestle with the
tail in subtle combat and larger males obtain more mat-
ings than small males (Madsen & Shine 1993). A similar
scenario has been found in northern water snakes, Nero-
dia sipedon, where larger males accomplish more matings
than smaller males in multiple-male breeding aggre-
gations (Weatherhead et al. 1995;Brown & Weatherhead
1999). On the other hand, there are data showing that
male common garter snakes, T. sirtalis, do not obtain an
advantage by being larger (Joy & Crews 1988). However,
recent studies on the same population reveal that larger
male garter snakes do obtain more matings than smaller
males (Shine et al. 2000). Madsen & Shine (1993) argue
that if females obtain more benefits from large size than
males, males may remain smaller than females. However,
the selection gradient for increased size for males obtain-
ing multiple matings is both proportional to, and higher
than, the comparable selection gradient for females due
to the increased fecundity of larger females (Duvall et al.
1993;Madsen et al. 1993;Shine & Fitzgerald 1995;
Weatherhead et al. 1995). Thus, it is not clear how an
increase in the fecundity of larger females would not
increase even more the fitness of males that can obtain
more matings in the polygynous system considered the
dominant mating system in snakes (Duvall et al. 1992,
1993; but see Rivas 2000). Furthermore, homologous
morphological traits in males and females are expected to
show high genetic correlations (Halliday & Arnold 1987);
if true, any selection for large size in females should also
increase the size of the males. Predictions from these
models do not appear plausible when faced with the
extent of the dimorphism seen. Perhaps we have been
overly influenced by the behaviour of lizards, birds and
mammals, in which size and strength seem to be major
determinants in mating success, and have inappropri-
ately applied the evolutionary logic proposed for these
groups to snakes.
In the literature regarding SSD it has not been hitherto
proposed that males could suffer a sexual selection dis-
advantage from being too large. Consider the problems of
being a male snake in search of potential mates, putting
ourselves in the ‘animals shoes’. Being too large could
actually be a disadvantage in multimale breeding aggre-
gations. Males search with their tails for the female’s
cloaca (as described by Gillingham 1979,1987;Madsen &
Shine 1993;Weatherhead et al. 1995). With their heads
(and chemoreceptors) facing away from the female’s
cloaca, vision and chemoreception are of limited use to
males. Males are more likely to rely heavily on tactile cues
to identify the female and secure intromission, as has
been demonstrated in some species (Pisani 1976;
Perry-Richarson et al. 1990). Thus, a male as large and
thick as the female could mislead other males into mating
Table 1. Possible benefits and disadvantages of large size in males and females; the benefits and disadvantages of
small size can be inferred from the opposite reasons mentioned
Benefits of large size Disadvantage of large size
Both sexes 1. Increased number of potential prey
species
1. More easily detected by predators
2. Ability to subdue prey 2. Greater energetic needs
3. Less frequent feeding on often risky prey 3. More conspicuous to their prey
4. Fewer predators 4. Higher costs of locomotion
5. Lower energetic cost per unit of body
mass
6. Greater body temperature stability
Females only 1. Increased fecundity due to increased
coelomic capacity that allows larger
clutches
2. Possibility of larger offspring with
greater chances of survival
Males only 1. Increased number of matings and fitness
in males if there is male–male physical
competition for mating access
1. Higher costs for locomotion and track-
ing of females during mating season
F2 ANIMAL BEHAVIOUR, 62, 3

with him. The result would be that a very large male
might have to spend time and effort fighting off other
males that might attempt to mate with him. If this is so,
in species that mate in large multimale breeding aggre-
gations, smaller male body size could be a cue for sex
recognition for other males as well as for the female. A
courted male, as well as the males that court him, would
be at a disadvantage compared with smaller males that do
not mislead other males. This constraint on large male
body size may lead to a local size optimum, where males
are large enough to win combats with other males in the
breeding aggregation, and yet be small enough to be
distinguished from breeding females. In those snake
species that do show male–male combat, breeding aggre-
gations are not common and sex recognition during
courtship is not a selection pressure limiting male size.
Thus, selection for large male size in species that engage
in male–male combat is fully expressed.
To seek and court large bulkier animals is adaptive for a
male, since larger and thicker females have more off-
spring (Ford & Seigel 1989) and are more likely to breed
(Rivas 2000). Such females are also older and more ex-
perienced. Hence, it would benefit males to court the
animals with the largest girth, both for certainty of
courting the right sex (and individual) and for increase of
fitness. Thus, SSD could be the key for sex identification
in situations where the chemosensory organs are not
involved or the pheromones of the females and scents
of the males have impregnated all the animals in the
seething breeding ball. Success may belong to the
male who can best discriminate males from females,
manoeuvre into position for copulation, and simul-
taneously thwart other males from doing likewise.
The above scenario can be applied and partially tested
by studies of green anacondas, Eunectes murinus, which
also breed in multiple-male aggregations where a female
is courted by several males. In these aggregations males
coil around the female and search for her cloaca with
their tails; visual or chemical cues do not appear to be
involved (Fig. 1;Rivas 2000). If one male is very large it
can be mistaken for a female by other males and be
courted (Fig. 2). Selection would favour large size in males
in order to outcompete other males, as larger males are
more likely to be found mating with the larger and more
fecund females (Rivas 2000). However, there is an optimal
size where males start being confused with females by
other males; this imposes a limit on male size. The result
would be stabilizing selection on males, producing a
population structure where all the males have a very
similar adult size and the overlap of size between males
and females is minimal (Fig. 3). We predict that this sort
of confusion between large males and females could be
present in most, if not all multimale breeding aggre-
gations. In particular it seems to apply to the experiment
of Madsen & Shine (1993) with grass snakes (N. natrix),
where they report that ‘Males seemed to become con-
fused between the female’s tail and those of other males,
and the tails of rival males often became entwined’(page
Figure 1. Breeding female anaconda (Ashley, 475 cm TL) at the shore of a lagoon in the Venezuelan llanos, being courted by 11 males. Photo
Jesus Rivas.
F3FORUM

562). That size cues by males to the female’s presence is
also suggested in the report of Noble (1937) on two small
male T. sirtalis that, for half an hour, courted a large
male from another region where the animals were not
reproductively active at the time. In his recent reply to
Shine et al. (2000),Crews (2000) argued that the number
of males involved in a breeding aggregation may lead to
different outcomes in the competition between males;
this could be the reason why his results (Joy & Crews
1988) differ from those of Shine et al. (2000). Shine et al.
used only a relatively small number of males (perhaps a
more common scenario in the mating system of garter
snakes throughout North America), whereas Crews
worked with a larger number of males per aggregation
(simulating the scenario of the particular dense breeding
aggregations found in southern Canada). We believe that
in large breeding aggregations males may, in fact, be more
likely to be mistaken for females, thereby decreasing the
benefit of large male size. In small aggregations, however,
the size advantage in displacing other males from the
female’s vent is more effective and larger males tend to be
more successful.
This mechanism of sex identification may have evolved
through the differential sexual maturation of males and
females. Females often delay sexual maturation and
become relatively larger before breeding, allowing larger
clutches. Males start breeding earlier and at a smaller size,
increasing their reproductive output since the fecundity-
independent costs of reproduction are lower (Bell 1980;
Madsen & Shine 1994) and territorial defence and estab-
lishing dominance are not prerequisites for mating. This
differential maturation sets the scenario for natural selec-
tion to act and SSD could thus be selected as a method for
sex discrimination.
To this point we have approached the actual courtship
events from the male’s perspective; the female’s perspec-
tive must also be considered. Since larger males are either
older or more successful foragers, females should prefer
larger males over smaller males. Females are known to be
selective in mating aggregations. Perry-Richardson et al.
(1990) found that female T. marcianus rejected some
males, even after intromission had occurred. In breeding
Figure 2. Mating aggregation of anacondas involving a very large female (Ashley) and 11 males. The female moved out of the water and
dragged with her some of the males that were coiled around her (A). Other males were removed from their positions and tried to find the
female again to continue courtship. However, some smaller males have mistakenly coiled around a very large male and are courting him (B).
60
Number of individuals
Size class (kg)
0
70
2
20
40
10
30
50
4 6 8 10 12 14 20 30 40 50 60 70 80
Females
Males
Figure 3. Size distribution of the adult population of anacondas from
the Venezuelan llanos. The criteria to determine adulthood was
finding them involved in a breeding aggregation. Notice the change
in the scale of the Xaxis after 14 kg.
F4 ANIMAL BEHAVIOUR, 62, 3

several generations of T. melanogaster in our laboratory,
we also have noted females accepting some males and not
others. Joy & Crews (1988) suggested that some individ-
ual males may be consistently more successful than
others. Female choice might make a large difference in
the fitness of offspring. Drickamer et al. (2000) report that
female house mice, Mus domesticus, mated with males
they preferred and, as a result, had more fit offspring than
females that mated with nonpreferred males. Comparable
phenomena may occur in snakes. What decision pro-
cesses are female snakes using to accept or reject a male’s
advances? In a breeding ball several males court a female
at the same time. It is very likely that the only way she
can discriminate and choose among the males is, again,
by relying on tactile cues. Does she have the ability to
differentiate from the displays given by the anterior end
of the snake (typically directed at the dorsum of her
neck), to determine which tail is worthy of her favours? It
may be necessary to observe a mating ball three dimen-
sionally from the interior to better understand the pro-
cesses involved. A focus on mechanisms of female choice
is needed.
Female ethologists have correctly emphasized the value
that taking a female perspective has added to our under-
standing of social behaviour, especially in primates (Small
1993;Gowaty 1994;Cunningham & Birkhead 1997). If a
von Uexku¨llian approach to behaviour had been applied
in the past, errors such as neglecting, presumably un-
consciously, the role of females in social systems might
never have occurred. Similarly, we feel that through
applying a critical anthropomorphism it is possible to
analyse the snake’s Umwelt, and obtain testable, and
perhaps more valid, insights about both the processes
involved in these events and how sexual selection might
be operating. Unfortunately, we currently have little data
on the specific stimuli used by females to select males or
the extent of female choice in snakes.
Too often ethologists and herpetologists regard snakes
and other reptiles as robot-like machines or as animals so
alien from us that attempting to put ourselves into their
world, even heuristically, is both useless and a scientifi-
cally dangerous conceit. On the contrary, approaching
unresolved issues by considering the perceptual world
and the perspective of the target animal may generate
testable hypotheses that were previously unconsidered.
This may prove to be true in research on snake mating
systems as well as on the evolution and maintenance
of SSD.
We thank R. Owens, M. Bealor, P. Andreadis and referees
for comments on the manuscript. We also thank the
Wildlife Conservation Society, National Geographic
Society, University of Tennessee Science Alliance and the
National Science Foundation for financial support. We
are also in debt to The Corporacio´n Venezolana de
Ganaderi´a and Estacion Cientifica Hato El Frio for logistic
support in the field.
References
Andersson, M. 1994. Sexual Selection. Princeton, New Jersey:
Princeton University Press.
Bekoff, M. & Allen, C. 1997. Cognitive ethology: slayers, skeptics
and proponents. In: Anthropomorphism, Anecdotes, and Animals
(Ed. by R. W. Mitchell, N. S. Thompson & H. L. Miles),
pp. 313–334. New York: State University of New York Press.
Bell, G. 1980. The costs of reproduction and their consequences.
American Naturalist,116, 45–76.
Brown, G. P. & Weatherhead, P. J. 1999. Demography and sexual
size dimorphism in northern water snakes, Nerodia sipedon.
Canadian Journal of Zoology,77, 1358–1366.
Burghardt, G. M. (Ed.) 1985. Foundations of Comparative Ethology.
New York: Van Nostrand Reinhold.
Burghardt, G. M. 1991. Cognitive ethology and critical anthropo-
morphism: a snake with two heads and hognose snakes that play
dead. In: Cognitive Ethology: the Minds of Other Animals (Ed. by
C. A. Ristau), pp. 53–90. San Francisco: L. Erlbaum.
Burghardt, G. M. 1997. Amending Tinbergen: a fifth aim for
ethology. In: Anthropomorphism, Anecdotes, and Animals (Ed. by
R. W. Mitchell, N. S. Thompson & H. L. Miles), pp. 254–276.
New York: State University of New York Press.
Cheney, D. L. & Seyfarth, R. M. 1992. Pre´cis of How Monkeys See
the World: Inside the Mind of Another Species.Behavioral and Brain
Sciences,15, 135–182.
Crews, D. 2000. Reply to Shine et al. (2000). Animal Behaviour,59,
F12: http://www.academicpress.com/anbehav.
Cunningham, E. & Birkhead, T. 1997. Female roles in perspective.
Trends in Ecology and Evolution,12, 337–339.
Drickamer, L. C., Gowaty, P. A. & Holmes, C. M. 2000. Free female
mate choice in house mice affects reproductive success and
offspring viability and performance. Animal Behaviour,59, 371–
378.
Duvall, D., Arnold, S. J. & Schuett, G. W. 1992. Pitviper mating
systems: ecological potential, sexual selection and microevolution.
In: Biology of the Pitvipers (Ed. by J. A. Campbell & E. D. Brodie, Jr),
pp. 321–336. Arlington, Texas: Selva.
Duvall, D., Schuett, G. W. & Arnold, S. J. 1993. Ecology and
evolution of snake mating systems. In: Snakes, Ecology and Behav-
ior (Ed. by R. A. Seigel & J. T. Collins), pp. 165–200. New York:
McGraw-Hill.
Ford,N.B.&Seigel,R.A.1989. Relationships among body size,
clutch size, and egg size in three species of oviparous snakes.
Herpetologica,45, 75–83.
Gillingham, J. C. 1979. Reproductive behavior of the rat
snakes of eastern North America, genus Elaphe.Copeia,1979,
319–331.
Gillingham, J. C. 1987. Social behavior. In: Snakes: Ecology and
Evolutionary Biology (Ed. by R. A. Seigel, J. T. Collins & S. S. Novak),
pp. 184–209. New York: McGraw-Hill.
Glotzbach, P. A. 1992. Perception theory and the attribution of
mental states. Behavioral and Brain Sciences,15, 157–158.
Gowaty, P. A. 1994. Architects of sperm competition. Trends in
Ecology and Evolution,9, 160–162.
Griffin, D. R. 1978. Prospects for a cognitive ethology. Behavioral
and Brain Sciences,1, 527–538.
Halliday, T. & Arnold, S. J. 1987. Multiple mating by females: a
perspective from quantitative genetics. Animal Behaviour,35,
939–941.
Herzog, H. A. & Galvin, S. 1997. Common sense and the mental
lives of animals: an empirical approach. In: Anthropomorphism,
Anecdotes, and Animals (Ed. by R. W. Mitchell, N. S. Thompson &
H. L. Miles), pp. 237–253. New York: State University of New York
Press.
Joy, J. E. & Crews, D. 1988. Male mating success in red-sided
garter snakes: size is not important. Animal Behaviour,36,
1839–1841.
Madsen, T. & Shine, R. G. 1993. Male mating success and body size
in European grass snake. Copeia,1993, 561–564.
F5FORUM

Madsen, T. & Shine, R. G. 1994. Costs of reproduction influence
the evolution of sexual size dimorphism in snakes. Evolution,48,
1389–1397.
Madsen, T., Shine, R. G., Loman, J. & Hakansson, T. 1993.
Determinants of mating success in male adders, Vipera berus.
Animal Behaviour,45, 491–499.
Noble, G. K. 1937. The sense organs involved in the courtship of
Storeria, Thamnophis, and other snakes. Bulletin of the American
Museum of Natural History,73, 673–725.
Perry-Richardson, J. J., Schofield, C. W. & Ford, N. B. 1990.
Courtship of the garter snake, Thamnophis marcianus, with a
description of a female behavior for coitus interruption. Journal of
Herpetology,24, 76–78.
Pisani, G. R. 1976. Comments on the courtship and mating mech-
anisms of Thamnophis (Reptilia Serpentes, Colubridae). Journal of
Herpetology,10, 139–142.
Rivas, J. A. 2000. Life history of the green anaconda (Eunectes
murinus) with emphasis on its reproductive biology. Ph.D. thesis,
University of Tennessee, Knoxville.
Semlitsch, R. D. & Gibbons, W. J. 1982. Body size and sexual
selection in two species of water snakes. Copeia,1982, 974–976.
Shine, R. G. 1978. Sexual size dimorphism and male combat in
snakes. Oecologia,33, 269–277.
Shine, R. G. 1993. Sexual dimorphism in snakes. In: Snakes; Ecology
and Behavior (Ed. by R. A. Seigel & J. T. Collins), pp. 49–86. New
York: McGraw-Hill.
Shine, R. G. 1994. Sexual size dimorphism in snakes revisited.
Copeia,1994, 326–346.
Shine, R. G. & Fitzgerald, L. 1995. Variation in matings systems
and sexual size dimorphism between populations of Australian
python Morelia spilota (Serpentes: Pythonidae). Oecologia,103,
490–498.
Shine, R. G., Olsson, M. M., Moore, I. T., Lemaster, M. P., Greene,
M. & Mason, R. T. 2000. Body size enhances mating success in
male garter snakes. Animal Behaviour,59, F4–F11.
Small, M. F. 1993. Female Choices: Sexual Behavior in Female
Primates. Ithaca, New York: Cornell University Press.
Tinbergen, N. 1951. The Study of Instinct. New York: Oxford
University Press.
Tinberlake, W. & Delamater, A. R. 1991. Humility, science and
ethological behaviorism. Behavior Analyst,14, 37–41.
von Uexku¨ll, J. 1909/1985. Environment (Umwelt) and the inner
world of animals (Translated by C. J. Mellor & D. Gove). In: The
Foundations of Comparative Ethology (Ed. by G. M. Burghardt),
pp. 222–245. New York: Van Nostrand Reinhold. (Reprinted
from von Uexku¨ll, J. 1909. Umwelt and Innenwelt der Tiere. Berlin:
Jena.)
Weatherhead, P. J., Barry, F. E., Brown, G. P. & Forbes, M. R.
1995. Sex ratios, mating behavior and sexual size dimorphism of
the northern water snake, Nerodia sipedon.Behavioral Ecology and
Sociobiology,36, 301–311.
F6 ANIMAL BEHAVIOUR, 62, 3