ANIMAL BEHAVIOUR, 2004, 67, 85e92

doi:10.1016/j.anbehav.2003.02.005

Sexual coercion in a territorial salamander:

females punish socially polygynous male partners
ETHAN D. PROSEN*, R OBER T G. JAEGER* & D ANIELLE R. LEE*

*Department of Biology and Institute of Cognitive Science, University of Louisiana, Lafayette

yMountain Lake Biological Station, University of Virginia
(Received 23 May 2002; initial acceptance 26 December 2002;
nal acceptance 24 February 2003; MS. number: A9363)

Sexual intimidation (sensu Smuts & Smuts 1993, Advances in the Study of Behavior, 22, 1e63) occurs when
members of one sex aggressively punish members of the other sex that refuse to mate with them or
that merely associate with other individuals of the opposite sex. We examined Clutton-Brock & Parkers
(1995, Animal Behaviour, 49, 1345e1365) concept that while males of many species use punishment
(intimidation) to coerce females into social or even mating monogamy, such behaviour by females towards
males should be rare. However, females in some species are territorial, and aggressive, and thus they may
play an active role in sexual intimidation. We tested this proposition in laboratory experiments with
territorial red-backed salamanders, Plethodon cinereus, that had been found as single (nonpaired)
individuals and in maleefemale pairs (we term members of a pair partners) in the forest. We manipulated
paired males such that they either had associated with another female before returning to their female
partners (socially polygynous) or had not (socially monogamous). In addition, we manipulated single
males such that they either had associated with another female before encountering a focal female for the
rst time (socially polygynous) or had not (socially nave). During the autumn courtship season, females
were signicantly more aggressive (threat displays and biting) towards socially polygynous partners
relative to those that were socially monogamous. In addition, females spent signicantly less time
touching socially polygynous partners relative to socially monogamous partners. However, females that
met a male for the rst time did not differ signicantly in their behaviour towards socially polygynous and
nave males. During the late spring, females displayed no behavioural differences towards either male
partners or strangers. Thus, female aggression was context dependent, with increased aggression directed
only towards polygynous partners and only during the autumn. We infer that females attempt to control
social polygyny by partners through aggression during the courtship season but that this coercion ceases
in the spring when the females are preoccupied with searching for nest sites for brooding their eggs.
2003 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. All rights reserved.

Darwin (1871) proposed two forms of sexual selection

(reviewed by Andersson 1994): intrasexual competition
for access to mates and intersexual mate choice. Smuts &
Smuts (1993, pp. 2e3) proposed a third form of sexual
selection: sexual coercion. Sexual coercion is the use by
a male of force, or threat of force, that functions to
increase the chances that a female will mate with him at
a time when she is likely to be fertile, and to decrease the
chances that she will mate with other males, at some
expense to the female. Sexual coercion differs from
intersexual selection in its mechanism; in sexual coercion,
males do not passively wait for females to choose them
but instead attempt to force the females to mate with
Correspondence: E. D. Prosen, Department of Biology, University of
Louisiana, Lafayette, LA 70504-2451, U.S.A. (email: heap74@msn.
com).
0003e3472/03/$30.00/0

them by (1) forced copulation, (2) harassment (repeated

attempts to mate with the female) and (3) intimidation
(males punish females that refuse to mate with them)
(Clutton-Brock & Parker 1995). Clutton-Brock & Parker
(1995) also expanded intimidation to include males
punishing females with various forms of violence when
they merely associate with other males.
There are several possible female responses to sexually
coercive males (Smuts & Smuts 1993; Clutton-Brock &
Parker 1995). Females may move to avoid male aggression,
avoid areas that males frequent, join a territorial male
for protection, attempt to avoid harassment but accept
matings from a harasser if she cannot escape, or form
coalitions for protection against males. All of these
proposed responses result in females behaving in such
ways as to avoid or to mollify male aggression in species
where males use sexual coercion. Although a lack of size

85
2003 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. All rights reserved.

86

ANIMAL BEHAVIOUR, 67, 1

dimorphism may inuence the success of sexual coercion

in a species, females are predicted to be passive participants in systems with coercive males (Smuts & Smuts
1993; Clutton-Brock & Parker 1995).
Our research has focused on Clutton-Brock & Parkers
(1995) concept that punishment (intimidation) should be
largely conned to males (but seldom females) attempting
to control, through aggression, the behaviour of members
of the opposite sex. While Clutton-Brock & Parker (1995)
provided many examples of such behaviour by males, we
suggest situations in which selection may act on females
to punish males aggressively. For example, in socially
monogamous species (Wickler & Seibt 1983), females may
be able to punish potentially polygynous partners if
polygyny impacts the tness of the females and the
females are not at a disadvantage in morphology (size or
strength) relative to males. The tness of females might be
impacted by polygynous partners reducing investment in
a females offspring in species with biparental care (e.g. the
longnose lesh, Oxymonacanthus longirostris: Kokita &
Nakazono 2001) or by polygynous males allowing other
females to use scarce resources (e.g. food) needed by the
partner. Females of some species apparently mate-guard
partners by attacking intruding females (e.g. the coral-reef
sh, Valenciennea strigata: Reavis & Barlow 1998; the
terrestrial red-backed salamander, Plethodon cinereus: Lang
& Jaeger 2000). However, punishment (with various
forms of violence: Clutton-Brock & Parker 1995) of
potentially polygynous males by females is also theoretically possible if aggression by mated females prevents
males from acquiring additional mates and, thus, results
in male monogamy (Wittenberger & Tilson 1980).
We tested the hypothesis that female red-backed salamanders would be aggressive towards polygynous male
partners because of the following conditions. At least some
members of this species engage in social monogamy
(Gillette et al. 2000) with maleefemale pairs sharing
territories on the forest oor even during the noncourtship
season ( Jaeger et al. 1995). Food in these territories is often
scarce ( Jaeger 1980; Jaeger et al. 1995) such that females are
food-limited in terms of yolking ova (biennial reproduction: Sayler 1966). Females are aggressive towards territorial
intruding females (Lang & Jaeger 2000). The sexes are not
signicantly dimorphic in size (Sayler 1966), and males are
aggressive (intimidation) towards female partners that
return from socially polyandrous outings from the territory
( Jaeger et al. 2002). Our rationale for the hypothesis of
aggressive punishment of males by females is that social
polygyny by male partners might allow extrapartner
females into the territory who would then compete with
the residential female partner for scarce prey.
Red-backed salamanders inhabit the leaf litter of forests
across eastern North America (Highton 1972) and occur at
densities up to 2.8 salamanders/m2 at our research site in
Virginia, U.S.A. (Mathis 1991a). Plethodon cinereus displays
a complex social system; like many other species of
plethodontid salamanders, they have a well-developed
visual system and use visual communication, in the form
of displays and movements that convey information
about aggression and submission (reviewed by Jaeger &
Forester 1993). Plethodon cinereus also uses chemicals in

communication and information gathering ( Jaeger et al.

1986; Jaeger & Forester 1993). Pheromones deposited on
substrates and faecal pellets allow individuals to assess
species identity ( Jaeger & Gergits 1979), gender (Mathis
1990, 1991a), size (Mathis 1991a, b) and diet quality
(Walls et al. 1989) of the depositor. Individuals of both
sexes defend territories under cover objects such as rocks
and logs (Mathis 1991a) that serve to sequester prey
( Jaeger 1980; Jaeger & Forester 1993) and may also serve
in courtship (Mathis 1991a). Courtship occurs during the
autumn (Sayler 1966; Gergits & Jaeger 1990) and spring
(Sayler 1966; Sever 1997) and maleefemale pairs are often
found cohabitating under the same cover object during
both the courtship and noncourtship seasons (Jaeger
1979; Jaeger et al. 1995).
Gillette et al. (2000) found that some maleefemale pairs
of P. cinereus engage in social monogamy (Wickler & Seibt
1983). Both males and females found together in the
forest preferred to associate with each other in the
laboratory relative to associating with a novel individual
from another pair. This preference disappeared when the
novel salamander was not from another pair (i.e. was
single), suggesting that both males and females are open
to the possibility of polygamy. Jaeger et al. (2002) found
that paired males intimidate their partners towards
monogamy by punishing them with aggression when
they associate with other males. However, males do not
behave differently towards novel (unfamiliar) females that
have or have not associated with other males.
We tested the null hypothesis that females of P. cinereus
do not signicantly differ in aggression towards socially
polygynous relative to socially monogamous partners.
Alternatively, if females of P. cinereus punish socially polygynous partners, as do males ( Jaeger et al. 2002), they will
be signicantly more aggressive towards socially polygynous partners than towards socially monogamous partners.
A logical (but unlikely) third hypothesis is that females are
signicantly less aggressive towards socially polygynous
versus socially monogamous partners. We dened a natural
pair as an adult male and female found within 30 cm of each
other under the same cover object in the forest, and termed
members of a pair partners (Gillette et al. 2000). We
considered any adult salamander found alone under a cover
object to be single. We also tested the hypothesis, based on
prior data for males (Jaeger et al. 2002), that females will not
be signicantly more aggressive towards socially polygynous male strangers than towards socially nave male
strangers because the social history of a strange male should
not impact a females tness when she meets him for the
rst time. We tested these hypotheses in two experiments,
one during the autumn courtship season and the other
during the end of the spring courtship season (about 14
days before gravid females began to lay and brood their
clutches of eggs at our research site).
To clarify our experimental designs, we use the following denitions from Jaeger et al. (2002). A socially polygynous male partner is one that forages in both the partners
territory and the territory of another single female.
A socially monogamous male partner is one that does
not forage in another females territory even if he departs
from his partners territory to forage alone elsewhere.

PROSEN ET AL.: SALAMANDER SEXUAL COERCION

Punishment includes threat displays or biting. A socially

polygynous male stranger is one who enters the territory of
a single female for the rst time after having foraged
previously in the territory of another single female. A
socially nave male stranger is one who enters the territory
of a single female for the rst time after having foraged
alone previously. These denitions pertain only to the relationships that we manipulated in our experiments, because
all of the salamanders that we collected for these experiments were adults and, thus, had at least 4 years of previous
social experience in the natural habitat (Sayler 1966).

MATERIALS AND METHODS

Collection and Maintenance of Animals

We collected 37 pairs, 55 single males and 101 single
females, of P. cinereus near Mountain Lake Biological
Station (MLBS), Giles County, Virginia, U.S.A., in midOctober 1999. In mid-April 2001, we collected 40 pairs, 40
single males and 80 single females, from the same
location. All salamanders were returned to the collection
site when the experiments were completed. We placed
each pair into one jar and each single salamander into
a jar for transportation to our laboratory in Lafayette,
Louisiana, U.S.A.
In the laboratory, we placed each single salamander into
a 154-cm2 petri dish (14 ! 1:5 cm) containing a single
sheet of lter paper moistened with spring water. We
placed each pair into a 576-cm2 Nunc bioassay dish
(24 ! 24 ! 2 cm: Cole-Parmer, Vernon Hills, Illinois,
U.S.A.) lined with damp (spring water) paper towels. Our
chambers were similar in size to the home areas of the
salamanders; Mathis (1989) found that, in the eld, cover
objects inhabited by a single salamander averaged 388
cm2 and cover objects cohabited by two salamanders (of
unknown relationship) averaged 776 cm2. The laboratory
was maintained at 18G1 (C with a 12:12 h light:dark
cycle. The salamanders were fed Drosophila virilis ad
libitum weekly, and the housing dishes were cleaned
biweekly until the experiments began.
We determined that all salamanders were adults (O32
mm snoutevent length: Sayler 1966). We determined the
sex of each salamander by placing it in a clear plastic bag
and holding it up to a bright light to determine the
presence or absence of testes, which can be seen through
the abdominal wall (Gillette & Peterson 2001).

Experimental Protocols
We performed two experiments that were identical
except that one used salamanders collected in the autumn
courtship season (mid-October) and the other used
animals collected near the end of the spring courtship
season (mid-April). We conducted the autumn courtship
season experiment during 17 Novembere15 December
1999 and the spring courtship season experiment during
12e18 May 2001. Both experiments were conducted as
follows, with the four treatments per experiment completely randomized. Each pair, single female and single

male, was used only once in each experiment, and single

animals were randomly allocated. The four treatments
that follow were conducted identically to those in Jaeger
et al. (2002) except that the social experience of males, not
females, was manipulated.

Treatment 1: socially polygynous male partner

On day 1, we placed randomly chosen maleefemale
pairs (N 19 autumn, N 20 spring) each into a clear
Nunc bioassay dish lined with a dampened (spring water)
paper towel (hereafter, chamber). On the same day, we
placed single females (N 19 and 20, respectively) each in
a separate chamber. We fed each salamander 10 D. virilis
and allowed 5 days for the salamanders to establish
territories, which is sufcient time for P. cinereus to deposit
pheromones on the substrate (Jaeger et al. 1986; Horne &
Jaeger 1988) and establish territories (Nunes & Jaeger
1989). On day 6, we transferred each male partner, using
a short piece of clear plastic tube to minimize handling
(hereafter moved), from the pairs chamber into the
chamber of a randomly selected single female, leaving the
female partner in the pairs original chamber, and fed all of
the salamanders D. virilis again. On day 11, we moved
each male back to his partners chamber. A clear plastic
cup (9 ! 1 cm) was placed over each individual for a
15-min habituation period, then the cups were removed
and a 15-min observational trial began.

Treatment 2: socially monogamous male partner

Procedures were identical to treatment 1 except that no
single females were used. Instead, we moved each paired
male into a clean, unoccupied chamber on day 6. We
tested 18 maleefemale pairs during the autumn experiment and 20 maleefemale pairs during the spring
experiment.

Treatment 3: socially nave male stranger

On day 1, we placed single females (N 28 autumn,
N 20 spring) and single males (N 28 and 20, respectively) each into separate chambers. We also set up
empty (N 28 and 20, respectively) chambers. We fed all
the salamanders D. virilis. On day 6, we moved each male
into an empty chamber and fed all the salamanders again.
On day 11, we moved each male into a randomly chosen
single females chamber. The observational trials followed
the procedures described in treatment 1.

Treatment 4: socially polygynous male stranger

On day 1, we set up single focal females (N 27
autumn, N 20 spring), single males (N 27 and 20,
respectively) and single stimulus females (N 27 and 20,
respectively) each in a separate chamber and fed all the
salamanders. On day 6, we moved each male into the
chamber of a randomly chosen stimulus female and fed all
the salamanders again. On day 11, we moved each male
into the chamber of a randomly chosen focal female; thus,
the focal females were the females in the observation
trials. The procedures for the observation trials were
identical to those in treatment 1.

87

88

ANIMAL BEHAVIOUR, 67, 1

Behavioural Patterns Recorded

(two-tailed ManneWhitney U test) between the times that

females spent threatening partners and strangers and used
a reduced a of 0.025 for female ATR in the autumn (see
footnote in Table 1).

During each observational trial, we recorded the

following behavioural patterns: time (in seconds) spent
in the all-trunk-raised (ATR) threat posture (Jaeger 1984;
Jaeger & Schwarz 1991) and touching the other salamander (Jaeger & Gabor 1993). The time spent touching was
awarded to the individual that initiated the touch. We also
recorded the number of bites administered by each
salamander (Jaeger 1984) and the number of nose taps
(touching the nasolabial cirri to the substrate; a chemoinvestigatory behaviour) performed by each salamander
(Arnold 1976; Jaeger 1984).

RESULTS

Autumn Courtship Season: Partners

Females spent signicantly (a 0:025) more time in the
threat (ATR) posture in response to socially polygynous
partners than in response to socially monogamous
partners (Table 1). They also spent signicantly less time
touching socially polygynous partners than they did
socially monogamous partners. Females nose-tapped the
substrate and bit their male partner signicantly more
often when their partner was socially polygynous than
when their partner was socially monogamous (Table 1).
No bites were directed towards socially monogamous
partners.
There were no signicant differences in behaviour
between socially polygynous and monogamous male
partners (Table 2). There were no bites delivered by any
male partner (polygynous or monogamous) during the
autumn courtship experiment (Table 2).

Ethical Note
In this species, bites consist of a rapid nip with the
anterior part of the mouth, which does not cause physical
damage to the skin of the bitten animal, or a full mouth
hold, which may lacerate the skin. We decided, a priori, to
intervene if a full mouth hold were to occur. We were
required to intervene on ve occasions due to the
occurrence of full mouth holds. We could distinguish
the paired salamanders by unique colour patterns so there
was no need to mark the salamanders individually.

Statistical Analyses
Autumn Courtship Season: Strangers

We statistically compared each of the behavioural

patterns between treatments 1 and 2, and separately
between treatments 3 and 4. We used two-tailed Manne
Whitney U tests (a 0:05) for independent nonparametric data (SAS Institute 1990). We did not adjust alpha
because each data set was only used once (rationale in
Gillette et al. 2000; Jaeger et al. 2002). However, because
we found differences in the times that females spent
threatening (ATR) both socially polygynous partners and
strangers in the autumn, we made a post hoc comparison

Females spent more time in ATR in response to socially

polygynous male strangers relative to socially nave male
strangers (Table 1), but this difference was not signicant
(a 0:025). Females showed no other signicant behavioural differences. There were no signicant differences in
behaviour between socially polygynous and nave male
strangers (Table 2). There were no bites delivered by any
male strangers (polygynous or nave) during the autumn
courtship experiment (Table 2).

Table 1. Responses of females (autumn courtship season) towards male partners that were either polygynous (NZ19) or monogamous
(NZ18) and towards male strangers that were either polygynous (NZ27) or nave (NZ28)
Mean
Behaviour of females towards

Median

Range

Poly

Mono

Poly

Mono

Poly

Mono

Partners
ATR (s)
Touch (s)
NT (number)
Bite (number)

540.2
3.3
8.9
0.52

181.0
21.3
2.3
0.0

540.0
0.0
6.0
0.0

45.5
1.5
1.0
0.0

0e883
0e25
0e43
0e6

0e805
0e115
0e9
d

3.42
2.02
2.62
2.00

0.0006**
0.0437*
0.0089*
0.0454*

Strangers
ATR (s)
Touch (s)
NT (number)
Bite (number)

Poly
352.1
27.8
6.2
0.07

Nave
263.6
12.4
4.1
0.04

Poly
260.0
0.0
4.0
0.0

Nave
34.5
0.0
3.0
0.0

Poly
0e867
0e272
0e40
0e1

Nave
0e869
0e138
0e18
0e1

1.99
0.89
0.83
0.60

0.0470
0.3723
0.4078
0.5491

Poly: polyandrous; Mono: monogamous; ATR: time in all-trunk-raised (threat posture); Touch: time touching the other salamander; NT: nose
taps (chemosensory behaviour). *Significant difference at aZ0:05 from ManneWhitney U test. **Significant difference at aZ0:025 from
ManneWhitney U test. Females spent significantly more time in an ATR posture in the presence of polygynous partners than in the presence of
polygynous strangers (ManneWhitney U test: ZZ2:298, PZ0:0216, aZ0:025).

PROSEN ET AL.: SALAMANDER SEXUAL COERCION

Table 2. Responses (autumn courtship season) of polygynous (NZ19) and monogamous (NZ18) males towards female partners and of
polygynous (NZ27) and nave (NZ28) males towards female strangers
Mean
Behaviour of males
towards

Median

Range

Poly

Mono

Poly

Mono

Poly

Mono

Partners
ATR (s)
Touch (s)
NT (number)
Bite (number)

303.7
56.8
6.2
0.0

305.4
27.7
8.8
0.0

46.0
32.0
4.0
0.0

26.5
9.5
4.0
0.0

0e875
0e213
0e21
d

0e850
0e141
0e30
d

1.04
1.20
0.14
d

0.2980
0.2297
0.8902
d

Strangers
ATR (s)
Touch (s)
NT (number)
Bite (number)

Poly
438.0
24.0
7.9
0.0

Nave
357.5
14.4
12.0
0.0

Poly
432.0
6.0
6.0
0.0

Nave
324.5
8.0
8.0
0.0

Poly
0e868
0e369
0e29
d

Nave
0e877
0e51
0e43
d

0.96
0.77
1.09
d

0.3362
0.4415
0.2756
d

Abbreviations as in Table 1.

Spring Courtship Season: Partners

DISCUSSION

Females showed no signicant differences in any of the

behavioural responses recorded in response to socially
polygynous partners relative to socially monogamous
partners and delivered no bites to partners during the
late spring courtship season (Table 3). Socially polygynous
and monogamous male partners showed no signicant
differences in behavioural responses (Table 4).

Spring Courtship Season: Strangers

There were no signicant differences in female responses to socially polygynous male strangers relative to
socially nave male strangers (Table 3). Socially polygynous male strangers spent signicantly less time in the
threat (ATR) posture and signicantly less time touching
than did socially nave male strangers but there were no
other signicant differences in any of the behavioural
responses (Table 4). No bites were delivered by any male
stranger (polygynous or nave) during the spring courtship experiment (Table 4).

In the autumn courtship experiment, paired females were

signicantly more threatening (ATR) and directed significantly more bites towards socially polygynous partners
relative to socially monogamous partners. Paired females
were also signicantly more threatening towards socially
polygynous partners than single females were towards
socially polygynous male strangers (see footnote in
Table 1). Thus, we infer that females aggressively punished
socially polygynous partners (sensu Clutton-Brock &
Parker 1995). Such punishment could result in male
monogamy.
During the spring courtship experiment, females did
not appear to distinguish between socially polygynous
and monogamous partners and therefore did not punish
partners that associated with other females. This change
in female behaviour during the spring may reect a change
in the females priorities. Females brood their clutches
(Bachmann 1984; Jaeger & Forester 1993), which they
deposit in May or June (our data from MLBS). Therefore,
during the late spring, females may be preoccupied with
locating suitable nesting sites. Single females also did not

Table 3. Responses of females (spring courtship season) towards male partners that were either polygynous (NZ20) or monogamous (NZ20)
and towards male strangers that were either polygynous (NZ20) or nave (NZ20)
Mean
Behaviour of females
towards

Median

Range

Poly

Mono

Poly

Mono

Poly

Mono

Partners
ATR (s)
Touch (s)
NT (number)
Bite (number)

386.6
29.4
5.0
0.0

284.8
27.6
4.8
0.0

320.5
0.0
2.0
0.0

110.5
2.0
1.5
0.0

0e890
0e384
0e21
d

0e889
0e245
0e21
d

1.43
1.11
0.42
d

0.1532
0.2666
0.6746
d

Strangers
ATR (s)
Touch (s)
NT (number)
Bite (number)

Poly
271.1
11.2
3.5
0.10

Nave
442.0
26.2
5.6
0.40

Poly
145.5
0.0
2.0
0.0

Nave
413.5
1.5
3.0
0.0

Poly
0e882
0e93
0e19
0e1

Nave
0e900
0e306
0e30
0e4

1.36
0.93
1.03
0.59

0.1737
0.3515
0.3034
0.5561

Abbreviations as in Table 1.

89

90

ANIMAL BEHAVIOUR, 67, 1

Table 4. Responses (spring courtship season) of polygynous (NZ20) and monogamous (NZ20) males towards female partners and of
polygynous (NZ20) and nave (NZ20) males towards female strangers
Mean
Behaviour of males
towards

Median

Range

Poly

Mono

Poly

Mono

Poly

Mono

Partners
ATR (s)
Touch (s)
NT (number)
Bite (number)

425.0
60.2
5.4
0.05

390.7
69.4
4.8
0.0

328.0
31.5
5.5
0.0

318.5
15.5
3.0
0.0

0e889
0e382
0e12
0e1

0e900
0e676
0e27
d

0.20
0.61
1.03
0.95

0.8383
0.5403
0.3013
0.3421

Strangers
ATR (s)
Touch (s)
NT (number)
Bite (number)

Poly
336.6
12.8
5.0
0.0

Nave
592.4
68.2
7.0
0.0

Poly
292.0
0.0
3.0
0.0

Nave
702.5
38.5
4.5
0.0

Poly
0e866
0e97
0e23
d

Nave
0e900
0e597
0e24
d

2.64
3.25
1.24
d

0.0083*
0.0011*
0.2143
d

Abbreviations as in Table 1.

distinguish between socially polygynous and nave male

strangers during the spring courtship experiment.
Socially polygynous male partners showed no signicant differences in behaviour relative to socially monogamous male partners in either the autumn or spring
experiments; this suggests that females did not use
behavioural cues to determine whether a male had or
had not remained monogamous. Gillette (1998) found
that females could detect polygynous males based on
pheromonal information (such males wear their own
pheromone plus the pheromone of another female).
Socially nave male strangers spent signicantly more
time threatening and touching unfamiliar females than
did socially polygynous male strangers in the spring; this
suggests that a males recent social history may inuence
his behaviour towards a novel female who is ending
courtship in preparation for nesting.
Our data support our rst hypothesis that female redbacked salamanders punish, through aggression, socially
polygynous partners, at least early in the courtship period
when females begin to yolk their ova. Our data also support
(but not unambiguously: see Table 1) our second hypothesis
that females would not discriminate aggressively between
socially polygynous and nave male strangers. A third
alternative hypothesis based on chemically mediated
femaleefemale aggression is not supported by our data.
Because a socially polygynous male returns wearing two
pheromones (see above), the female may mistake him for
another female. Under the chemically mediated femalee
female aggression hypothesis, the increased aggression
directed towards the socially polygynous males would
merely be the result of the greater aggression directed
towards female relative to male intruders (Lang & Jaeger
2000). However, this hypothesis does not predict any
differences between the responses of paired and single
females; if female aggression is linked to mistaking the
males for females, the identity of the males should have no
effect on the resulting aggression. We reject this alternative
hypothesis because paired females were signicantly more
aggressive towards socially polygynous males than were
single females (see footnote in Table 1). Therefore, females
appear to punish socially polygynous partners.

How do females benet from such behaviour? We posit

four hypotheses. (1) Punishment by females may secure
paternal care. (2) Punishment of males may reduce
females exposure to sexually transmitted diseases. Recent
computer simulations have shown that the presence of
sexually transmitted diseases in a population may slow
the evolution of polygyny (Thrall et al. 2000), and Loehle
(1995) hypothesized that the avoidance of exposure to
sexually transmitted diseases is one of the advantages of
monogamy. (3) Female aggression may aid in sequestering
resources necessary for reproduction. (4) Female aggression may ensure a males aid in territorial defence. If males
and females cooperate in territorial defence, a male that
engages in extrapair interactions may reduce his effort in
defence of the current females territory.
We reject hypothesis 1 because there is no evidence that
males of P. cinereus provide any aid to females during
brooding of clutches or to neonates. Hypothesis 2 also
seems unlikely because males of P. cinereus obtain
fertilizations internally via a spermatophore (Sayler
1966). Because of the spermatophore, a male could
transmit a sexual disease to a female, but a female cannot
transmit such a disease to a male. Therefore, it seems
unlikely that a polygynous male could acquire a sexually
transmitted disease. However, we cannot rule out cutaneous infections that could be spread topically during
courtship.
We cannot reject hypothesis 3. Female reproduction is
resource limited (Sayler 1966). A male that engages in
extrapartner interactions may return with another female
and allow her to forage in his territory. This competition
for prey within the territory would directly impact the
residential females ability to yolk ova, affecting her
reproductive success. Therefore, aggression towards polygynous partners may decrease the probability of competition for necessary resources by increasing the cost of
polygyny.
Lang & Jaeger (2000) found that although red-backed
salamanders defend territories jointly against conspecic
intruders, the defence is not cooperative. Males are more
aggressive towards male intruders and females are more
aggressive towards female intruders. Thus, male partners

PROSEN ET AL.: SALAMANDER SEXUAL COERCION

tolerate female intruders who would compete with the

resident female for resources. Therefore, we reject hypothesis 4; it seems unlikely that female aggression serves to
ensure male aid in territorial defence.
Jaeger et al. (2002) found that male red-backed
salamanders intimidated, through aggression, polyandrous female partners but not polyandrous female
strangers. Their inference that males intimidate female
partners towards monogamy to protect their genetic
investment in a females ova agrees well with our
inferences about the benets of female punishment of
male partners to protect resources. Because of this and the
ndings of Lang & Jaeger (2000), we infer that social
monogamy in red-backed salamanders (Gillette et al.
2000) may be merely a consequence of (1) male and
female partners keeping same-sex intruders out of the
territory (Lang & Jaeger 2000) and (2) mutual aggression
between partners following acts of social polygamy. This
social system may serve as a model for the evolution of
social monogamy in other territorial species that lack
biparental care.
Although Smuts & Smuts (1993) acknowledged that
there are species where sexually coercive roles are reversed,
females were generally predicted to be passive participants
in sexually coercive systems. Female responses to sexual
coercion were limited to attempts to avoid or reduce male
aggression. Our data provide evidence for a system where
females actively punish males (and possibly intimidate
them towards social monogamy) in a species where males
use intimidation to enforce social monogamy on females.
Acknowledgments
We thank C. Swart and G. Meche for help in collecting the
salamanders and H. M. Wilbur for permission to conduct
research at Mountain Lake Biological Station. We thank
A. Bockelman, A. Mathis and L. Mathews for comments
on a previous draft of this manuscript. This research was
funded by Louisiana Board of Regents Doctoral Fellowship LEQSF (1999-04)-GF-26 and a Doctoral Dissertation
Improvement Grant from the National Science Foundation (IBN-0205804) to E.D.P. Salamanders were collected
under permit 017047 from the Virginia Department of
Game and Inland Fisheries, and laboratory experiments
were approved by the Animal Care and Use Committee
of The University of Louisiana at Lafayette (IACUC No.
2001-8717-004).
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