Journal of Insect Behavior, Vol. 12, No. 4, 1999
Agonistic Displays and the Benefits of Fighting in
the Field Cricket, Gryllus bimaculatus
Gabrielle Tachon,1 Anne-Marie Murray,1,2 David A. Gray,1 and
William H. Cade1,3
Accepted March 16, 1999; revised April 6, 1999
Fighting is often composed of discrete agonistic displays. Few studies have
partitioned fighting behavior into its component agonistic displays and evaluated
the relationships between the frequency of the displays and the potential benefits
of fighting, particularly mating success. In this study, we quantified the frequency
of male field cricket, Gryllus bimaculatus, agonistic displays. The displays were
quantified under three social environments which varied in the potential benefits
of fighting: males with other males only, males with other males and female scents,
and males with other males and females. We found that (1) the presence of females
elicited an increase in agonistic displays characteristic of intermediate levels of
escalation, (2) female scents did not produce a similar increase in the frequency
of agonistic displays, and (3) in the presence of females, the frequency of agonistic
displays was positively correlated with mating success. Aggressive stridulation, an
energetically low-cost display, was more strongly associated with mating success
than were more costly displays. The results are discussed in the context of the
evolutionary theory of aggression and in the context of cricket mating systems.
KEY WORDS: field crickets; fighting; agonistic displays; mating success; sexual selection;
male-male competition; Gryllus bimaculatus.
INTRODUCTION
Aggressive conflict between members of the same sex over mates is a common
factor influencing reproductive success in many animal species (Archer, 1988).
1
Department of Biological Sciences, Brock University, St. Catharines, Ontario L2S 3A1, Canada.
Present address: Department of Biological Sciences, McEver Hall, Arkansas Tech University, Russellville, Arkansas 72801.
3
To whom correspondence should be addressed.
2
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0892-7553/99/0700-0533$16.00/0 © 1999 Plenum Publishing Corporation
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Tachon, Murray, Gray, and Cade
Contests between individuals are adaptive only if the benefits of winning exceed
the costs of energetically expensive displays and the risk of injury (Maynard
Smith, 1974). Agonistic displays are thought to express the resource holding
potential of an individual (e.g., Parker, 1974; Maynard Smith and Parker, 1976;
Davies and Halliday, 1978; Clutton-Brock et al., 1979). Most empirical studies
of male-male competition have examined the effects of variation in male morphology on the outcome of fights and/or mating success, e.g., male size or size
of weaponry (reviewed by Andersson, 1994). Fewer studies have examined the
relationship between mating success and behavioral components of fighting.
Agonistic displays are frequently exhibited in male field crickets (Alexander, 1961). Field cricket fights consist of a number of discrete components:
antennation (used in sex and species recognition), juddering (a rapid rocking
back and forth of the body), aggressive stridulation (a loud abrupt acoustic signal
distinct from the calling song used to attract females), flaring of the mandibles,
and grappling or wrestling (Alexander, 1961). Within an agonistic encounter,
escalation generally occurs from antennation to juddering to mandible flaring
to grappling, although individuals may revert from a higher level display to
a lower one (Alexander, 1961; Adamo and Hoy, 1995). In Gryllus bimaculatus, aggressive stridulation depends on the social environment: males isolated
as adults from conspecifics stridulate aggressively only at the end of a fight,
and only the winning male does so; males housed in social groups may produce
aggressive stridulation throughout a fight, but primarily do so at an intermediate
level of escalation—both eventual winners and eventual losers of fights stridulate (Adamo and Hoy, 1995). Encounters may be terminated at any point within
this sequence; most fights conclude with aggressive stridulation or do not proceed beyond aggressive stridulation (Alexander, 1961; Simmons, 1986a; Adamo
and Hoy, 1995).
Recent work with Acheta domesticus (Hack, 1997a,b) examined the energetic costs of cricket agonistic displays. The energetic costs of the displays,
measured as oxygen consumption versus resting on a per second or per repetition basis, can be ranked from least costly to most costly as follows: aggressive
stridulation (approximately 1.1 resting), mandible flare (approximately 1.5 resting), juddering (shake in Hack's terminology; approximately 5.2 resting), and
grappling (wrestling in Hack's terminology; approximately 8 resting). Antennation as defined in this study is not equivalent to "antennae lashing" as used
by Hack, thus we do not have an estimate of the energetic cost of antennation
but anticipate that it is a low to very-low cost of display. The total energetic
costs of individual agonistic displays may substantially exceed these estimates
as elements are repeated throughout a fight. Hack (1997b) estimated the total
energetic cost of fighting as averaging 2.8 resting, 1.3–4.8). Given that agonistic displays are energetically costly, we would predict that the frequency of the
displays would increase as the benefits of fighting increase.
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To test these predictions we manipulated the potential benefits of fighting by
changing the social environment. Three treatments were used: no females, female
scents, and females present. Additionally, in treatments with females present, we
examined the relationships between agonistic displays and male mating success.
METHODS
Crickets
Adults were isolated from laboratory stock and weighed within 48 h of
the adult molt. Mass near the time of the adult molt, as measured here, is a
very good indicator of structural body size: for this species, r = 0.89, N =
26, and P < 0.01 (M. Fitzpatrick, D. A. Gray, and W. H. Cade, unpublished
data; for a related species see Gray, 1997). Only intact crickets possessing all
appendages were used. The laboratory stock originated from adults collected
east of Harare, Zimbabwe, in 1994. The laboratory stock was maintained in
84-L plastic garbage bins containing cotton-plugged water-filled vials, cat food,
and egg cartons for shelter. The cultures were at room temperature (generally
20–24°C) on a 14L: 10D light cycle.
Isolated crickets were individually marked with paint on the pronotum and
placed in individual clear plastic containers (16 x 9 x 9 cm, l x w x h) on a
reversed photoperiod of 12D: 12L. Cotton-plugged water vials and cat food were
provided. Males and females were kept in separate rooms to prevent males from
having any visual or olfactory contact with females prior to trials. When used
in experiments, males were 5-9 days post adult molt and females were 8-15
days. The crickets' flight wings were removed 1-2 days prior to experiments.
This was done to ensure that crickets remained within the arena. A 1- to 2-day
recovery time was judged sufficient.
Males were divided into 10 groups of five males each. All males within a
group were of similar mass [mean + SD of the coefficient of variation in male
mass within groups (N = 10 groups), 8.9 + 4.1%; mean + SD male mass (N = 50
males), 555 ± 63 mg]. Each set of five males was tested under three experimental
treatments: males only (MO), males with females scent-conditioned paper (MP),
and males with two females (MF). The scent-conditioned paper was made by
lining a terrarium containing four to six virgin females with filter paper for 2-5
days. Scent-conditioned paper made in a similar manner has been shown to be
effective in eliciting behavioral responses in at least three previous studies of
crickets (Otte and Cade, 1976; Paul, 1976; Hardy and Shaw, 1983).
Behavioral Trials
Behavioral observations were conducted at 20-22°C during the observer's
daytime (the cricket's night) in a 30-cm-high glass terrarium with 2.5 cm of sand.
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Tachon, Murray, Gray, and Cade
Movable glass partitions were used to maintain the density of crickets at 19.4
crickets/m2. In trials with females (five males and two females), the terrarium
size was 60 x 60 cm; in trials without females, the glass partitions decreased
the arena to 50.7 x 50.7 cm. The density used here was within the range used in
previous studies (Simmons, 1986a; Nagao and Shimozawa, 1987) and is within
the range observed in the field (W. H. Cade, personal observation). Black Bristolboard was placed around three sides of the terrarium to reduce light levels
while still making observation possible. Five glass vials (2.7 cm in diameter x
8 cm long) were placed horizontally on the sand to act as burrows. Burrows
increase the probability of aggressive encounters in G. bimaculatus (Simmons,
1986a). The burrows were kept in the same position relative to the arena walls in
all trials. Between each experimental treatment the sand was replaced to eliminate possible scents which may have collected. Between observation periods the
terrarium was covered to prevent outside contaminants from entering.
Males were placed in upright glass vials in the terrarium for 5 min of
acclimation prior to each trial. The vials were removed and the software program Event-PC/MAC (Ha, 1990) was used to record the frequency of displays
on a Macintosh LC. Practice observations were undertaken prior to trials to
reduce observer error. The number of matings and the identity of the individuals involved were recorded during observations with females present (MF treatment).
Each trial was 2 h in length. Two trials were carried out per day, one in
the morning and one in the afternoon. The order in which the MP and MF treatments were presented to each group of males was reversed for one-half of the
experimental trials. Different virgin females were used in the morning and afternoon trials to maintain receptivity levels. Between daily trials, male crickets were
returned to their isolation containers and placed in a separate dark room for
no less than 1 h. G. bimaculatus males require a 1-h interval between matings
(Nagao and Shimozawa, 1987). At the end of each day, all crickets were returned
to their individual containers.
Data Analysis
The mean frequency of each behavior for the two observation periods was
calculated for each male. These means were used as the raw data. The raw data
were not normally distributed, and we were unable to transform them such that
they met the requirements of parametric tests; therefore nonparametric statistics
were used. A squared-ranks test for variances (Conover, 1980) determined that
the different male groups had equal variance and, thus, could be pooled in subsequent analyses. A Mann–Whitney U test determined that the order in which the
treatments MP and MF were presented did not affect male behavior. Repeatedmeasures one-way ANOVA on ranks was used to analyze the data (Conover,
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Fighting in Crickets
1980). A Bonferroni-adjusted multiple-comparisons test was used to establish
the number of significant differences and their location (Zar, 1984). A multiple rank-correlation test with Bonferroni correction was performed to establish
any correlation among the five displays, male mass and mating frequency. All
probability values are based on two-tailed tests.
RESULTS
Antennation
Figure 1a shows the median and interquartile range (IQR) frequency of
antennation in each of the three social environments. Social environment significantly affected the frequency of antennation [F(2,98) = 16.95, P < 0.0001].
Antennation was significantly less frequent when females were present than in
the other two social environments (MF < (MO = MP)).
Judder
Figure 1b shows the median and IQR frequency of juddering in each of
the three social environments. Social environment significantly affected the frequency of juddering [F(2,98) = 6.50, P < 0.0022]. Juddering was most frequent
when females were present (MF > (MO = MP)).
Mandible Flaring
Figure 1c shows the median and IQR frequency of mandible flaring in each
of the three social environments. Social environment significantly affected the
frequency of mandible flaring [F(2,98) = 17.75, P < 0.0001]. Mandible flaring
was significantly more frequent when females were present (MF > (MO = MP)).
Grappling
Grappling was extremely rare. The only social environment in which the
median level of grappling was greater than zero was males with females present
(Fig. 1d). Social environment did not significantly affect the frequency of grappling, although the results were suggestive [F(2,98) = 2.67, P = 0.0745].
Aggressive Stridulation
Figure 1e shows the median and IQR frequency of aggressive stridulation in
each of the three social environments. Social environment significantly affected
the frequency of aggressive stridulation [F(2,98) = 10.11, P < 0.0001]. Aggressive stridulation was significantly more frequent when females were present (MF
> (MO = MP)).
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Tachon, Murray, Gray, and Cade
Fig. 1. The frequency of agonistic displays as a function of the
social environment: (a) antennation; (b) juddering: (c) mandible flaring; (d) grappling; (e) aggressive stridulation. Median frequency and
interquartile ranges are shown for N = 50 males. The social environments are males only (MO), males with female-scented paper (MP),
and males with females (MF). Medians which share the same letter
above the histogram bars were not significantly different from each
other.
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Fighting in Crickets
Table I. Rank Correlations (rs) Among Agonistic Displays, Mating Success, and Male Mass
for the Males-with-Females Social Environment (N = 50 Males)
Antennation
Matings
Antennation
Juddering
Stridulation
Mandible flaring
Grappling
*
0.436
Juddering
**
0.537
0.683**
Stridulation
**
0.658
0.662**
0.838**
Mandible
flaring
**
0.625
0.614**
0.818**
0.846**
Grappling
**
0.599
0.356
0.486*
0.575**
0.687**
Mass
0.039
0.036
-0.056
-0.035
0.089
0.078
*
**
P < 0.05, Bonferroni-adjusted probabilities for 21 comparisons.
P < 0.01, Bonferroni-adjusted probabilities for 21 comparisons.
Agonistic Displays and Mating Success (MF Social Condition)
Mating was infrequent. The median number of male matings was 0.5 (IQR
= 0-1.5). Agonistic displays were strongly and positively associated with mating success. Table I shows the rank correlations among the displays, mating
success, and male mass. All pairs of agonistic displays with the exception of
antennation-grappling were significantly positively correlated. Neither mating
success nor the frequency of agonistic displays were significantly correlated with
male mass. Aggressive Stridulation showed the strongest correlation with mating
success.
Energetics, Escalation, and the Occurrence of Displays
The relative frequency of each of the displays within each of the social
environments reflected the displays position within the sequence of escalation,
not the energetic cost of the display (Fig. 2). Irrespective of the energetic expense
of the displays, displays early in the sequence were more frequent than displays
late in the sequence.
DISCUSSION
Evolutionary theory predicts that as the benefits of a behavior increase relative to the costs, the frequency of the behavior should increase. This prediction
should be met across evolutionary time scales. This study demonstrated that levels of male-male agonistic display increased in the presence of females. Thus
behavioral plasticity allows male crickets to adjust their levels of aggressive conflict in accord with evolutionary theory at much smaller time scales. Our findings
are in agreement with previous work with field crickets (Alexander, 1961; Simmons, 1986a) and consistent with long-standing predictions regarding the costs
and benefits of fighting behavior. Not all agonistic displays increased in fre-
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Tachon, Murray, Gray, and Cade
Fig. 2. The relative frequency of each of the displays within each of the social
environments. Displays are listed according to the sequence of escalation. The
vertical line between grappling and stridulation is to indicate that stridulation
does not always directly follow grappling but occurs at the end of the fight and
may be directly preceded by any of the other displays. The solid lines through
diamonds and squares connect displays in the males-only (MO) and males-withfemale scent-conditioned paper (MP) social conditions, respectively. The dashed
line through triangles connects displays when males were with females (MF).
Ant, antennation; Jud., juddering; Mand., mandible flare; Grap., grappling; Strid.,
aggressive stridulation.
quency, however. The lowest- and highest-level displays, antennation and grappling, respectively, did not show significant increases when females were present
compared to the males only and the males with female scent-conditioned paper
treatments. Antennation was significantly reduced with females present. Antennation is a multifunctional behavior used in both sex and species recognition
(Otte and Cade, 1976; Rence and Loher, 1977). It is possible that antennation
decreased in the presence of females because antennation is not primarily an
agonistic display. Despite the overall decrease in antennation when females were
present, the frequency of antennation was positively correlated with mating success.
We found no evidence to suggest that female scents, in and of themselves,
were sufficient to provoke fighting among males. We do not believe that the
absence of an effect was due to the filter paper not presenting an olfactory stimulus. Using a methodology similar to that used here, Otte and Cade (1976) found
that female scents increased aggression in the house cricket, Acheta domesticus. Two other studies have documented effects of scent using similarly conditioned paper (Paul, 1976; Hardy and Shaw, 1983). Furthermore, it is well
Fighting in Crickets
541
established that crickets use chemical cues for species and sex recognition (Otte
and Cade, 1976; Rence and Loher, 1977; Hardy and Shaw, 1983; Tregenza and
Wedell, 1997). Thus it seems likely that males in this study failed to respond
to, rather than failed to perceive, female scents. We suggest that males may not
respond with increased aggression to female scents in the absence of other stimuli because, as females walk around at night visiting various male territories,
female scents alone may be a poor indicator of the presence of females.
The male display most strongly associated with mating success when
females were present was aggressive stridulation. We interpret this relationship
as follows. In contrast to males housed in groups, males isolated from conspecifics as adults produce aggressive stridulation only at the end of a fight,
and only the winning male does so (Adamo and Hoy, 1995) further demonstrated that the effect of isolation persists even after 5 days of daily contact with
other males, provided that the males are reisolated daily (the effect is reversible
after 5 days of continuous contact with other males). The males used in this
study were isolated from other males as adults and reisolated after daily trials. Thus our interpretation of the relationship between aggressive stridulation
and mating success is straightforward: males that won fights (and so stridulated)
mated more often. In crickets, winning fights is known to increase male mating
success via male-male competition, although female choice favoring dominant
males has also been suggested [see, e.g., Acheta domesticus (Crankshaw, 1979;
Nelson and Nolen, 1977), Teleogryllus oceanicus (Burk, 1983), Gryllus bimaculatus (Simmons, 1986)]. We did not record winners and losers of individual
fights, however, and so cannot be certain of this interpretation.
The relative frequency of each of the aggressive displays reflected its occurrence in the sequence of agonistic escalation, rather than its energetic cost. Similarly, the displays showing the greatest increase in frequency when females were
present compared to the males-only condition were not the most energetically
expensive displays (on a per second or per repetition basis). Instead, displays
characteristic of intermediate levels of escalation (juddering, mandible flaring,
and aggressive stridulation) showed the greatest increases in median frequency
(64, 250, and 240% increases, respectively). Mandible flaring showed the highest
percentage increase, although it is an energetically low-cost display. Mandible
flaring potentially carries a high social cost, however, because mandible flaring
leads to grappling, the most escalated level of fighting, approximately 40-50%
of the time (for transition probabilities see Adamo and Hoy, 1995).
Male mass was unrelated to either the frequency of agonistic displays or
mating success. This result contrasts with previous work on G. bimaculatus
(Simmons, 1986a). Larger males of several cricket species have an increased
probability of winning aggressive conflicts [Acheta domesticus (Hack, 1997a),
G. integer (Dixon and Cade, 1986), G. pennsylvanicus (Souroukis and Cade,
1993)]; female choice may also favor larger males (Simmons, 1986a,b, 1988;
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Tachon, Murray, Gray, and Cade
Gray, 1997). Mating success in the field, however, may be unrelated to male
size [e.g., G. veletis and G. pennsylvanicus (Zuk, 1987, 1988), G. integer (Cade
and Cade, 1992), and G. bimaculatus (Simmons and Zuk, 1992); but see Simmons (1992) for an example of positive size selection in G. campetris]. In this
study, we attempted to minimize differences in mass among males. Either no true
net effect of size or a restricted range of variation may account for the absence
of size effects in this study.
Overall, our results demonstrate three important features of agonistic contests in crickets: (1) behavioral plasticity allows individual crickets to match their
levels of aggressive display to the potential rewards of fighting over short time
scales; (2) fighting, and in particular winning fights, is associated with increased
mating success; and (3) with increased fighting, increases in the frequency of the
discrete behavioral components of fighting are more strongly associated with the
display's level of escalation than with its energetic costs on a per second or per
repetition basis.
ACKNOWLEDGMENTS
G. Tachon was supported by the Brock University-Guernsey Graduate
Scholarship. Both A.-M. Murray and D. A. Gray received support in the form
of Brock University Postdoctoral Fellowships. This work was supported by an
NSERC Grant to W. H. Cade (NSERC Operating Grant A6174).
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