I
Differences in age structure among field
cricket populations (Orthoptera; Gryllidae):
possible influence of a sex-biased
parasitoid
I
Can. J. Zool. Downloaded from www.nrcresearchpress.com by University of Lethbridge on 07/13/13
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Anne-Marie Murray and William H. Cade
Abstract: This study examined age structure in adult populations of three species of field cricket,
Gryllus veletis, G. pennsylvanicus, and G. integer. Adults were aged by counting growth layers in cross
sections of tibiae. The study species differ in several life-history traits including the likelihood of
parasitism by Ormia ochracea, a tachinid that orients to calling males. Gryllus integer is parasitized
whereas G. veletis and G. pennsylvanicus are not. Such differences between the species should result
in different age patterns. Data from field collections demonstrated that adult G. veletis and
G. pennsylvanicus had similar maximum life-spans of about 4 weeks, and males were similar in
age or slightly older than females. The maximum age for female G. integer was also about 4 weeks,
but few males >20 days old were encountered. Moreover, male G. integer were significantly younger
than females in five out of six samples. This pattern in G. integer, evident in 2 successive years, could
be consistent with sex-biased mortality by Ormia ochracea. The results are discussed in relation to
differential longevities and the intensity of sexual selection on male mating behaviour.
Resume : Nous avons ktudik la structure selon l'ige de populations adultes de trois espkces de grillons,
Gryllus veletis, G. pennsylvanicus et G. integer. L'ige a kt6 dktermink par dknombrement des couches
de croissance dans des coupes transversales de tibias. Les espkces ktudikes different par plusieurs
aspects de leur biologie, notamment par leur susceptibilitk au parasitisme d'Ormia ochracea, un
tachinide qui recherche les miles chanteurs. Gryllus integer sert d'h8te au tachinide, alors que les deux
autres espkces ne sont pas parasitkes. I1 est lkgitime de s'attendre alors ce que ces espkces diffkrent
aussi par la structure selon 1'8ge de leurs populations. Les rksultats des rkcoltes sur le terrain ont
dkmontrk que les adultes de G. veletis et de G. pennsylvanicus ont des longkvitks maximales semblables
d'environ 4 semaines et que les miles sont d'iges kquivalents et lkgkrement plus igks que les femelles.
L'ige maximal des femelles de G. integer a kgalement kt6 kvaluk a 4 semaines, mais peu de miles de
plus de 20 jours ont kt6 rencontrks. De plus les males de G. integer se sont avkrks significativement
plus jeunes que les femelles dans cinq des six kchantillons. Cette tendance, observke chez G. integer au
cours de 2 annkes conskcutives, est compatible avec la mortalitk causke par 0 . ochracea qui affecte un
sexe plus que l'autre. Ces rksultats sont examinks a la lumikre des effets de la longkvitk diffkrentielle et
de l'intensitk de la sklection sexuelle sur le comportement reproducteur des miles.
[Traduit par la Rkdaction]
Introduction
Knowledge of age structure is important in many ecological
and behavioural studies. Differential mortality rates within
and between populations can select for different life history
patterns (Stearns 1976, 1992). Comparisons of age distributions between males and females can detect sexual bimaturism, an important component of sexual selection (Thornhill
and Alcock 1983) and age has also been implicated as an
important factor in female choice (Halliday 1978, 1983).
Received November 11, 1994. Accepted March 3 1, 1995.
A.-M. Murray1 and W.H. Cade. Department of Biological
Sciences, Brock University, St. Catharines, ON L2S 3A1,
Canada.
I
Author to whom all correspondence should be addressed.
Can. J. Zool. 73: 1207 - 1213 (1995). Printed in Canada / ImprimC au Canada
Considering its significance to a wide range of theoretical
and applied biology, relatively little is known about age
structure in insect populations. This is due in large part to
a lack of quantitative methodology. Qualitative methods
abound (reviewed in Southwood 1978), but allow only broad
age categories to be defined. Neville (1963, 1965) was the
first to use a simple but accurate way to determine adult
insect age. He described growth layers in locust cuticle that
were deposited daily in response to circadian rhythm and
photoperiod. Similar growth layers have since been
documented in representatives of &any orders (reviewed by
Neville 1983).
This work was undertaken to examine age structure within
three species of field crickets (Orthoptera, Gryllidae). We
used the method originally described by Neville and first
applied to field crickets by Zuk (1987a, 1987b, 1988).
d ~ l l u sveletis and G. pennsylvanicus are common in the
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Can. J. Zool. Vol. 73, 1995
Niagara region. Both are univoltine with an obligative diapause. Gryllus veletis overwinters as a nymph and the primarily micropterous adults are found from late May to late
July. Gryllus pennsylvanicus overwinters as an egg and
adults are evident from late July to October. Macropterous
individuals occur infrequently (Alexander and Bigelow
1960; Alexander and Meral 1967; Alexander 1968). Gryllus
integer occurs in central Texas, has a high frequency of
macropterous individuals, requires no obligative diapause,
and seems to have two population peaks a year (Alexander
1968; Cade 1979a).
The three species also differ with respect to selection by
a sex-specific parasitoid. Males of all three species call and
attract receptive females for mating. Calling carries a heavy
cost in the Texas species, G. integer, as calling males also
attract an acoustically orienting dipteran parasitoid, Ormia
ochracea. Infested males die within 7 - 10 days and infestation rates as high as 80% have been recorded (Cade 1975,
1979b, 1984). Female G. integer are very rarely parasitized
(Cade 1979b; A. -M. Murray, unpublished data). Gryllus
veletis and G. pennsylvanicus are not affected by such a sexspecific parasitoid, and this might influence male-female
age patterns among the species. It is predicted that males of
G. integer will have significantly shorter life-spans than conspecific females and that such differential longevities may
not be apparent between the sexes in either G. veletis or
G. pennsylvanicus.
Methods
Age was estimated by counting chitin layers in cross sections
of tibiae. Individuals of known age from laboratory cultures
were first examined to establish the accuracy of the method
for the study species. Samples of crickets were then gathered
across the 1991 and 1992 field seasons and compared.
Ageing method
The hind leg, from the distal end of the femur down, was
excised and held between the fingers, and thin sections of
tibia were cut using a razor blade under a binocular microscope. Six to 10 sections were taken per adult. Tibia1 sections
were arranged in a drop of water on a slide, allowed to dry,
and then mounted in Canada Balsam. The growth layers visible in 4-6 of these sections were later counted using a Leitz
light microscope ( x 400). The maximum number of layers in
any one section was used in subsequent analysis.
Accuracy of the ageing method
To test the accuracy of the method, large groups of nymphs
were reared to adulthood in the laboratory under a temperature and photoperiod regime similar to ambient conditions.
Individuals were then killed at a known adult age (1 -34
days) and preserved in 70% ethanol until they were sectioned. Slides were assigned a random number by a third
party so that subsequent estimations of age by the authors
were carried out without prior knowledge of the actual age
of the insect. Estimated age was later regressed on actual age
to examine the relationship.
Age patterns in field populations
Samples of G. veletis and G. pennsylvanicus were taken in
and around the campus of Brock University, St. Catharines,
and in various locations in the Niagara region of southern
Ontario. Gryllus veletis adults were collected between 2 June
and 8 July 1992. Most males collected were calling just prior
to capture. Samples of G. pennsylvanicus were captured
between 25 July and 17 September 1991. Males were
labelled callers if they were calling just prior to capture and
noncallers if they were silent. Data from calling males and
noncalling males were analysed separately.
Gryllus integer adults were collected around the Brackenridge biology field station in Austin, Texas, over the periods
25 June - 22 September 1991 and 20 May - 8 October
1992. Most individuals were captured by attracting flying
males and females to broadcasts of tape-recorded conspecific
male song (for a description of song broadcasting see Cade
1989). Phonotactic individuals landed near the loudspeaker
and were then collected. Calling males in the vicinity were
also captured. Samples collected using the different methods
were analysed separately.
Three to five samples were taken across the season for
each species so that seasonal trends in age structure could be
determined. Each sample consisted of 8 - 100 individuals
captured over a short time interval (1 -6 days). All specimens were immediately labelled and preserved in 70%
ethanol until they were sectioned.
Ages in days are given as means f 1 SD. Data proved normal and homoscedastic for variance, so subsequent data analyses were carried out using standard parametric methods.
Two-way ANOVAs were used to determine the effects of
date and sex on age variation. Post hoc Tukey's tests were
used for multiple comparisons.
Results
Accuracy of the ageing method
Figure 1 illustrates the significant linear, relationships
between number of growth layers in cross sections of tibiae
and actual age in days for laboratory-reared adult G. veletis,
G. pennsylvanicus, and G. integer. Curvilinear relationships
were also examined but did not improve the relationships.
Results for males and females were pooled, as there were no
significant differences between the sexes in either slope
(G. veletis, t = 0.24, p > 0.05; G. pennsylvanicus, t =
0 . 2 5 , ~> 0.05; G. integer, t = 0 . 2 4 , ~> 0.05) or elevation
(G. veletis, t = 0.3 1, p > 0.05; G. pennsylvanicus, t =
1.77, p > 0.05; G. integer, t = 0.13, p > 0.05) of lines.
The slopes and elevations of the three regression lines do not
differ among ,the three species (F[2,2361= 0.3 1, p > 0.05;
F[2,236,
= 1.87, p > 0.05).
Age distributions in field populations
Figure 2 illustrates frequency distributions of ages of males
and females for all G. veletis captured over the study period.
Both sexes ranged in age from 2 to 28 days. Figure 3 illustrates similar data for G. pennsylvanicus categorized into
three groups, calling males, noncalling males, and females.
All three categories had similar maximum ages of about 4
weeks. Newly moulted adults (1 -3 days) were found in the
field until mid-August. All calling males were estimated as
9 days old or more. Frequency distributions for G. integer
captured in 1991 and 1992 are presented in Figs. 4 and 5,
Murray and Cade
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Fig. 1. Relationship between number of growth layers in
cross sections of tibiae and actual age in days of laboratoryreared crickets. (A) G. veletis, r = 0.60, p = 0.0001; n =
60. ( B ) G. pennsylvanicus, r = 0.89, p = 0.0001; n = 110.
( C ) G. integer, r = 0.89, p = 0.0001; n = 7 2 .
Fig. 2. Frequency distributions of estimated age for all adult
male and female G. veletis collected over the 1992 study
period.
u
m
6
1
FEMALES
I
ADLILT AGE
(DAYS)
Fig. 3. Frequency distributions of estimated age for all adult
G. pennsylvanicus (calling males, noncalling males, and
females) collected over the 1991 study period.
6
1
MALES
ADULT AGE ( D A Y S )
respectively. All individuals in both years were at least
5 days old when captured. Males had a maximum age of 20
(1991)or 23 (1992)days and females 27 days.
Table 1 illustrates variations in mean age for male and
female G. veletis in three separate periods across the field
season. Age varied with date (F[2,1091
= 59.85, p =
0.0001).Adults captured in early June were younger than
those captured in late June (q = 15.4,p < 0.001)and early
July (q = 1 1.12,p < 0.001),with no difference in mean age
between the last two dates (q = 1.37,p > 0.50).Age did
not vary between the sexes (F,l,lo9,
= 2.85,p = 0.09),
neither was there an interaction between date and sex
(F[2,1091
= 0.56,p = 0.57).
Data on within-season trends in mean age for the three
categories of adult G. pennsylvanicus are given in Table 2.
Age varied with date (F[2,2291
= 109.6,p = 0.0001).Adults
showed successive increases in mean age from first to last
samples (July vs. August, q = 8.2,p < 0.001; August vs.
September, q = 13.2, p < 0.001).Mean age also varied
with category (F[2,2291
= 10.55,p = 0.001),females being
younger than both calling (q = 5.2,p < 0.001)and noncall-
L
3
10
1
FEMALES
2
6
I
10
n = 120
14
18
22
26
ADLILT AGE ( D A Y S )
30
Can. J. Zool. Vol. 73, 1995
Table 1. Ages of male and female field-captured Gryllus veletis.
2 June
n
Males
Females
29
22
25 June
n
Mean k SD Range
8.8k3.8
6.8k3.4
2-16
2-14
8 July
Mean k SD Range
19
32
n Mean f SD
9-27
8-28
16.2f4.4
14.7k4.7
5
9
17.8f 3.7
15.3k3.0
Range
14-23
11-19
Table 2. Ages of male and female field-captured Gryllus pennsylvanicus.
13 August
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25 July
n
Calling males
Noncalling males
Females
15
22
47
Mean
+
SD Range
12.8f3.3
10.3+_4.1
7.7f3.2
n
9-19
3-19
2-18
12 September
Mean f SD Range
14.4k3.5
14.2k5.8
12.3k4.2
22
31
44
n
9-25
1-25
2-20
Mean
8
17
29
SD
+_
19.4k4.9
20.4f 3.4
20.2f4.0
Range
13-27
14-25
12-32
Table 3. Ages of male and female field-captured Gryllus integer from 1991.
25 June
n
Calling males
Flying males
Flying females
Mean
+
3 August
SD Range
-
-
16
22
11.3k2.4
13.5k3.6
n
Mean f SD Range
16
28
32
-
8-15
7-21
22 September
11.4k3.2
13.2k2.6
18.1f 4.5
Fig. 4. Frequency distributions of estimated age for all adult
G. integer (calling males, flying males, and flying females)
collected over the 1991 study period.
n
7-18
7-17
7-27
+ SD
Range
-
-
-
50
50
11.1k2.6
13.5k2.7
7-18
7-20
Fig. 5. Frequency distributions of estimated age for all adult
G. integer (calling males, flying males, and flying females)
collected over the 1992 study period.
12-
FLYING
MALES
Mean
FLYING
10- MALES
n = 94
n = 62
8v,
1
4
3
n
-
>
-
CALLING
MALES
6-
42-
6
2
6
I
I
h
I
n = 16
10
14
18
22
26
1
I
FLYING
FEMALES
n = 43
30
ADLILT AGE ( D A Y S )
2
6
10
14
ADULT AGE
18
22
(DAYS)
26
30
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Murray and Cade
ing males (q = 4.5, p < 0.005). No difference in age was
detected between the two categories of males (q = 0.81,
p > 0.50). A significant interaction was found between date
= 3.4, p = 0.03). Further analysis
and category (F[2,2291
revealed that in the first sample, both calling (q = 6.9, p <
0.001) and noncalling (q = 4.1, p < 0.001) male groups
were significantly older than females but this difference was
not seen in later samples. Over 42% of females in the first
sample were estimated to be less than 7 days old compared
with 13.5% of males.
Data for G. integer from the 1991 season are reported in
Table 3. Flying individuals varied in age across the season
(F[2,1921
= 20.71, p = 0.0001). Individuals captured in
August were significantly older than those caught in either
June (q = 5.1, p < 0.001) or September (q = 6.1, p <
0.001). Age also varied with sex (F11,1921
= 35.71, p =
0.0001), males being younger than females, and there was a
significant interaction between date and sex (F[2,1921 = 5.37,
p = 0.005). Males were significantly younger than females
in August (q = 8.6, p < 0.001) and September (q = 4.77,
p < 0.01) but not in June (q = 3.6, p < 0.05). Both calling
and flying males were captured in August, but there was no
difference in mean age between these categories of males
(t = 1.7, p > 0.05).
Data on G. integer captured in 1992 are given in Table 4.
Flying adults of both sexes were captured on three dates, in
June, August, and October, but no variation in age with date
was evident (F[2,861= 1.68, p = 0.20). However, differences did exist between the sexes (F[1,861= 19.65, p =
0.0001), males being significantly younger than females.
There was no interaction between sex and date (F[2,861=
0.02, p = 0.98). Samples of calling males were collected in
May, July, and October. Mean age varied across dates for
callers (F[2,401= 4.3, p = 0.02), but post hoc comparisons
failed to detect discrete differences between pairs of means.
Two samples in 1992 contained both flying and calling
males. No significant difference in age was apparent between
males exhibiting either behaviour prior to capture in either
July (t = 0.88, p > 0.20) or October (t = 1.5, p = 0.15).
Discussion
All three species exhibited significant positive relationships
between growth layers in the tibiae and actual age in days.
Similar regressions suggest no differences among the species
with respect to the rate of deposition of such layers, though
considerable scatter was evident for G. veletis. Increased
variance was evident when ageing older specimens of all
three species, a trend also noted by Zuk (1987~)and by
workers on other insects (Ellison and Hampton 1982). This
increase in variance may be due to the difficulty of discerning individual layers in thicker, older sections. It is also
likely that growth layer deposition ceases after a certain time.
Neville (1963) found that in locusts, cuticular maturation,
and thus growth layer deposition, was completed after about
3 weeks. A maximum of 39 layers were counted in this
study, correlating with a 35-day-old G. pennsylvanicus male.
If we had examined crickets older than 35 days, a levelling
off might have been seen, corresponding to the maximum
number of layers laid down in the cuticle. This limit to the
deposition of layers does not alter the results presented here,
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Can. J. Zool. Vol. 73, 1995
however, as very few individuals over 25 days were encountered. Counting growth layers in adult tibiae is a useful
method for ageing field crickets. However, the method
should be calibrated each time a different species is examined, as predictability may vary among species.
New teneral adults of both northern species were encountered in the field. All G. integer captured were 5 days or
older, as most were trapped phonotactically . Laboratory
trials suggest that crickets do not begin to exhibit phonotaxis
to male song until they are > 4 days past eclosion (Sakaluk
1982; personal observation). The maximum age recorded
from field adults was about 4 weeks.
Distinct differences in age patterns were evident among
the three species under study, both within and across seasons. The mean age of both males and females increased
across the season for G. veletis and G. pennsylvanicus,
reflecting the fact that both species are univoltine. The mean
age of male and female G. integer showed no consistent trend
within the seasons. Gryllus integer is a more or less continuous breeder and seasonal fluctuations in age reflect this.
No difference in age was discernible between the sexes in
G. veletis, but male G. pennsylvanicus tended to be older
than females. This difference was especially pronounced
early in the season. In fact, by a week or two into the field
season, only female nymphs were observed, most males
having already reached adulthood (personal observation). No
such disparity between the sexes was reported by Zuk
(1987~)for her population of G. pennsylvanicus in Michigan. However, Zuk combined data across the entire season
when comparing the sexes, and within-season patterns might
have been masked.
Earlier male eclosion, or protandry, has been described in
many insects and may benefit males in some groups through
the increased probability of mating with virgins (Wiklund
and Fagerstrom 1977) or through first male sperm precedence (Wedell 1992). Females of most gryllids mate multiply, however, and sperm mixing has been reported (Backus
and Cade 1986). Protandry may be important in competition
for territories prior to mating. Early-eclosing males of the
desert grasshopper, Liguorotettix coquilletti , occupy higher
quality territories than later eclosing males, and also exhibit
longer life-spans and higher female-encounter rates (Wang
et al. 1990). Male field crickets are territorial and male spacing patterns are achieved through acoustical and physical
interactions (Alexander 1961; Campbell and Shipp 1979;
Cade 198la; Campbell 1990). Early eclosion and acquisition
of high-quality calling sites may be important to male
G. pennsylvanicus, especially if such sites are limited.
Observations while collecting indicated that specific sites
were rapidly colonized by a new male after the capture of the
original resident (personal observation). It has also been suggested that protandry may arise because of selection on
females to delay reaching adulthood (Thornhill and Alcock
1983). Females would thus gain larger adult size, with correlated increases in fecundity.
In G. integer, a difference in age between the sexes was
also noted. But in contrast to G. pennsylvanicus, male
G. integer were younger than conspecific females. In fact,
males over 20 days old were encountered in only one of eight
samples collected over the 2-year period. A closer analysis
revealed that in five of six samples where both males and
females were collected, male G. integer were significantly
younger than females. Thus, males of this species exhibit
reduced longevity compared with conspecific females.
Gryllus integer is known to be a host of the sex-specific
parasitoid Orrnia ochracea. Gravid female flies are attracted
to calling males and deposit larvae on or near the individual
(Cade 1975, 1979b). Female G. integer are very rarely
parasitized (Cade 1979b; A.M. Murray, unpublished data)
and thus one might expect this differential parasitism to be
reflected in differential longevities between the sexes, as was
observed in this study.
Few data on age structure are available from comparable
gryllid species. Simmons and Zuk (1992) aged adults of the
European field cricket G. bimuculatus in Spain. In southern
Europe G. bimuculatus has several characteristics in common with the G. integer population studied here. It too has
an almost continuous breeding season, is characterized by
predominantly macropterous individuals, and engages in
mass dispersal flights, but it is not affected by a sex-specific
parasitoid. Male G. bimuculatus were found to be significantly older than females. More recently, populations of
Teleogryllus oceanicus were examined (Simmons and Zuk
1994). In two populations, one on mainland Australia and
one on the island of Moorea, males were significantly older
than conspecific females. The exception to the pattern
occurred on Hawaii, where males and females were similar
in age. The population on Hawaii is subject to predation by
0 . ochracea, and Simmons and Zuk (1994) suggest that the
difference in age patterns among populations is consistent
with that expected as a result of sex-biased mortality caused
by the dipteran parasitoid.
Differences in age structure were revealed both among
and within species in this study. Male G. integer consistently
exhibited reduced life-spans compared with conspecific
females and such a pattern was not evident in either G. veletis
or G. pennsylvanicus. Differential male longevities should
affect the force of selection acting on male mating behaviour,
but this has never been considered. Previous field and modelling studies on G. veletis, G. pennsylvanicus, and G. integer
have revealed similar trends in the intensity of sexual selection on males. Selection was often weak or absent and
affected by fluctuations in population density and sex ratio
(French and Cade 1987; Cade and Cade 1992; Rowel1 and
Cade 1993; Souroukis and Cade 1994). This research,
however, involved cross-sectional studies in which differences in longevity between individuals or between species
were not considered. Moreover, research has also demonstrated the significance of the age of males in choice by
females (Zuk 1987b, 1988). Future work should involve longitudinal studies of closely related species that differ in age
structure to evaluate how differences in longevity can affect
the force of selection acting on male reproductive behaviour.
Acknowledgements
This research was supported by an operating grant (No.
A6 174) to W.H.C. from the Natural Sciences and Engineering Research Council of Canada and by a postdoctoral
fellowship to A.-M.M from Brock University. We thank
J. Crutchfield and L. Gilbert for access to Brackenridge
Field Laboratory, University of Texas at Austin. We thank
Murray and Cade
E.S. Cade, M. Ciceran, K. Souroukis, D. Belme, S. Adamo,
and T. Pisaric for help in collecting crickets and two reviewers for their helpful comments.
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