Behavioral Ecology Vol. 11 No. 3: 319-325
© 2000 International Society for Behavioral Ecology
Can minor males of Dawson's burrowing bee, Amegilla dawsoni (Hymenoptera: Anthophorini) compensate for reduced access to virgin females through sperm competition?
a Evolutionary Biology Research Group, Department of Zoology, The University of Western Australia, Nedlands, WA 6907, Australia b Department of Biology, Arizona State University, Tempe, AZ 85287-1501, USA
Address correspondence to L. W. Simmons. E-mail: lsimmons{at}cyllene.uwa.edu.au .
Received 15 February 1999; revised 17 September 1999; accepted 4 October 1999.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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Dawson's burrowing bees (Amegilla dawsoni) exhibit a conditional mating strategy with two alternative tactics. Large (major) males exclusively patrol emergence sites in search of about-to-emerge females, whereas small (minor) males usually search the periphery of emergence sites for females that escape patrollers. About 80% of the male population are minors, despite the fact that patrolling emergence sites is apparently the more profitable mating tactic. We tested the hypothesis that minor males gain fitness by mating with nonvirgin females and engaging in sperm competition with rival ejaculates. If the sperm competition hypothesis applied, it would help explain why nesting females produce so many minor sons. Contrary to this hypothesis, however, we found that minor males do not exhibit traits frequently associated with sperm competition. Minor and major males did not differ in testis mass after controlling for body size. Neither did they differ significantly in the duration or pattern of copulation nor in the volume of ejaculate transferred. In addition, and also contrary to the sperm competition hypothesis, females apparently mated only once. Loss of female sexual receptivity occurred quickly after the onset of copulation, and nesting females appeared completely unreceptive. Thus, all aspects of the bee's mating system strongly indicate that sperm competition does not occur in Dawson's burrowing bee, so that minors cannot compensate even partially via sperm competition for their mating disadvantage with virgin females.
Key words: alternative mating tactics, Amegilla dawsoni, bees, sperm competition.
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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Studies of animal mating systems have revealed considerable intraspecific variability in mate-securing tactics (Andersson, 1994
;
Thornhill and Alcock, 1983).
In many cases males have various morphological and/or life-history traits that
facilitate their alternative mating behavior. Although the evolutionary
maintenance of alternative phenotypes has been the subject of intense
theoretical investigation, few empirical studies have examined fitness
parameters associated with alternative tactics in natural populations
(Gross, 1996).
The mating system of Dawson's burrowing bee, Amegilla dawsoni, is
characterized by a conditional mating strategy with two alternative tactics.
Two size classes of male exist, small minors and large majors, with male size
dependent on the amount of brood provisions received from their mother
(Alcock, 1997a,
1999;
Houston, 1991). The two size
classes of males adopt alternative mating tactics
(Alcock, 1997a). Males emerge
earlier than females (Alcock,
1997b), and major males patrol the emergence site for
about-to-emerge females. Competition for access to emerging females is
intense, and larger males have a competitive advantage over smaller males
(Alcock, 1996c). Minor males
thus search the peripheral zone of emergence sites for females that escape
patrolling majors or search at flower patches where females forage
(Alcock, 1997a). Patrolling
emergence sites is the more profitable tactic, with nearly 90% of all virgin
females mating with patrollers immediately upon their emergence
(Alcock, 1996c). Although minor
males patrol emergence areas when the intensity of competition is low, usually
they are forced into the low-payoff tactic, yet they represent 66-80% of the
male population (Alcock,
1997a).
Field studies of this bee have attempted to discover how the production of
such high frequencies of minor males by nesting females can be maintained
(Alcock, 1996c). First, male
size dimorphism cannot represent an incidental by-product of environmental
constraints because dimorphisms persist across generations, vary little
between populations, and are specific to male offspring. Second, male
dimorphism does not arise because of the occurrence of two classes of female
that exhibit two different condition-dependent provisioning tactics, because
putative siblings can be of either major or minor phenotype. A third
hypothesis is that individual females produce minors that on average return
the same net fitness benefit as major male offspring; although minors are
constrained to adopt a much less profitable tactic, they are about half as
costly to produce as majors, based on the quantity of provisions they require,
and survive on average 22% longer at the emergence area
(Alcock, 1996a). Nonetheless,
because minors obtain less than half the observed copulations while
constituting substantially more than half the male population, a balance in
the cost:benefit ratio for the two morphs seems unlikely
(Alcock, 1996b). However, to
date payoffs have been estimated only on matings observed at emergence sites.
Multiple mating by females and subsequent sperm competition from minor males
could alter the fitness payoffs to nesting females from producing minor sons
and thereby at least partially compensate for the poor mating success of
minors at emergence sites (Alcock,
1996b).
If sperm competition is an important aspect of the mating system of
Dawson's burrowing bee, a number of testable predictions emerge. First, recent
game theoretical models of sperm competition predict that males adopting
alternative, less profitable mating tactics should invest more heavily in
traits that promote success in sperm competition
(Parker, 1990). Minor males
searching away from emergence areas will always be subject to sperm
competition given the high probability that a female will have already mated
at the emergence site. In contrast, major males should be subject to low
probability of sperm competition, dependent on the encounter rate of females
with minors away from emergence sites. With this expected asymmetry in sperm
competition risk, Parker's models predict that minor males should compensate
for low mating probability by allocating more resources to sperm production,
ejaculating greater volumes of sperm during copulation, and/or spending longer
in copulatory activities than major males
(de Fraipont et al., 1993;
Gage et al., 1995;
Simmons et al., 1999;
Taborsky, 1998).
Second, some females should exhibit a tendency to mate with more than one
male. In at least one anthophorine, the solitary bee Centris pallida,
some females will mate a second time if they have received incomplete
copulatory and postcopulatory stimulation
(Alcock and Buchmann, 1985). We
show here that copulatory and postcopulatory courtship also occur in A.
dawsoni, raising the possibility that those females that do not receive
sufficient stimulation from their first mate may copulate a second time,
possibly with a minor male away from the emergence site.
We tested the predictions concerning male investment in ejaculate production and male and female copulatory behavior to assess the general significance of sperm competition as a factor in maintaining the high frequency of minor males in populations of Dawson's burrowing bee.
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METHODS |
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The study was conducted during the 1997 reproductive season at an emergence site 10 km north of Carnarvon, Western Australia (see Alcock, 1996c
). All
observations were made between 1030 and 1600 h, the peak period of bee
activity. We collected males as they patrolled the emergence site searching
for about-to-emerge females or from the periphery of the emergence site. When
patrolling males alighted on the ground by an emergence tunnel, a small vial
was placed over the entrance to collect the emerging female. We also collected
nesting females as they returned to their burrows from foraging trips.
Variation in testis mass
We captured patrolling and searching males and placed them immediately into
a refrigerator in our field vehicle. Males were later weighed and the width of
their head capsule determined (head capsule width is the standard measure of
body size used for bees; Stubblefield and
Seger, 1994) before being frozen in liquid nitrogen for
transportation back to the laboratory. Testes were later dissected and weighed
to the nearest 0.01 mg.
Variation in male mating behavior
We placed newly emerged females into an insect net and isolated them in a
small pouch approximately 30 cm3 by gathering and twisting the net
beneath the female. A patrolling male was captured and placed immediately into
the pouch with the female. Males typically pounced on the female as soon as
they came into contact, and their copulatory behavior was then recorded. The
bee's copulatory behavior is characterized by three distinct phases. In phase
1, the male positions himself onto the female's back and flicks his wings
forward a number of times. Phase 2 begins immediately upon intromission,
during which the male produces a continuous series of rapid, shallow body
thrusts that are accompanied by an audible "zip" to which the
female responds with a buzz (Figure
1). During phase 3, the male disengages his genitalia but
continues to "zip". Zips are interspersed with deeper backward
movements, during which the male probes the female's external genitalia with
his own genitalia and flutters his wings. We recorded (1) the number of flicks
during phase 1; (2) the number of zips within each minute of copulation during
phase 2; and (3) the number of zips and the number of flutters within each
minute of phase 3. All animals were placed in the refrigerator and weights and
head capsule widths determined before freezing the bees in liquid
nitrogen.
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To determine whether males behaved normally in the net, we recorded copulations that were initiated by patrolling males at the emergence site. Males mount females as they emerge and ride on their backs across the open ground of the emergence site to vegetation at its periphery. We followed six pairs and recorded their copulatory behavior in the peripheral vegetation.
Variation in sperm transfer
We monitored sperm transfer by interrupting copulations after varying
periods: 1 zip (about 1s), 5 zips (about 5 s), 15 s of zips, 30 s of zips, 2
min of zips, or 4 min of zips. Males and females were transferred immediately
to the refrigerator before being measured and frozen. Females were later
dissected and the spermatheca placed onto a hemocytometer and covered with a
cover slip so that it was compressed to a standard thickness of 0.1 mm. The
spermatheca was viewed at 200x magnification. Any sperm were clearly
visible through the transparent spermathecal walls. We could not make direct
sperm counts because sperm could not be dispersed from previously frozen
material. Instead, we obtained an estimate of the amount of sperm contained
within the spermatheca by measuring its optical density using the gray scale
function on the image analysis package Optimas. The gray scale ranges from 0
(black) to a maximum of 255 (white). The optical density was obtained from the
log of inverse gray scale scores and is dimensionless. We determined the
optical density of the spermathecal walls per se by measuring the spermathecae
of virgin females. We also controlled for potential differences in sperm
density due to differences in spermathecal capacity by dividing our measure of
sperm density by spermathecal volume, which was determined using the area
morphometry function on Optimas and the known depth of the hemocytometer. The
bursa copulatrix was also mounted onto a hemocytometer and examined for sperm.
The volume present was determined from its area and the depth of the
hemocytometer. Testis weights of males were determined as above.
Female remating tendency
We determined the propensity for females to remate after their first
copulation had either been interrupted after 1 s, 5 s, 15 s, 30 s, or 60 s or
when they had been allowed to complete their first copulation without
interference. First, freshly emerged females were placed in a net with a male
captured at random from those patrolling the emergence site or its periphery.
After a randomly allocated period of copulation, we removed the first male and
immediately placed a second male with the female. The copulatory behavior of
the second male was recorded as above. We also captured 10 females that had
begun building nests at the emergence site and provided each with a series of
three randomly captured males. Each male was held with a female and the pair
repeatedly brought into contact. Pairs that failed to initiate mating within
about 2 min were separated, the male discarded, and another male
introduced.
We screened data to confirm underlying assumptions of parametric statistics. Where these were violated, nonparametric equivalents were used. All means are presented ±1 SE.
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RESULTS |
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Variation in testes mass
The distribution of head widths of males used in our experiments is shown in Figure 2A. All males with head widths
6.3 were classified as majors, and those with head widths
<6.3 were classified as minors. The distribution of male sizes is
discontinuous; males of head widths between 6.1 and 6.25 are consistently rare
or absent in all populations studied
(Alcock, 1996b;
Houston, 1991). Note that this
was a nonrandom sample of the population. Among males that emerged during this
study, minors represented 78% (Alcock, unpublished data).
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Analysis of covariance revealed that testis mass increased with body mass (F1, 94 = 12.29, p =.0007) but did not differ between male morphs (F1, 94 = 2.59, p =.111). There was no body mass by morph interaction (F1, 94 = 0.56, p =.456). The allometry of testis mass is shown in Figure 2B. Within morphs, testis mass increased with body mass with an allometric exponent <1.0 (common within morph slope b = 0.77 ± 0.20).
Variation in male mating behavior
Major and minor males behaved similarly while copulating. Phase 1 lasted on
average 16.2 ± 3.9 s (comparison between morphs: Mann-Whitney
U = 152, n = 33, p =.196), and males achieved
intromission after performing an average of two wing flicks (comparison
between morphs: U = 170, n = 36, p =.75;
Figure 3A). We performed a
repeated-measures ANOVA on the number of zips produced within each minute of
phases 2 and 3 of copulation. The rate of zips produced declined significantly
over the course of copulation, but there was no difference due to male morph
and no interaction between morph and time (morph: F1, 19 =
0.479, p =.497; repeated measure (minute): F5, 95
= 41.891, p <.001; interaction: F5, 95 =
0.522, p =.759; Figure
3B).
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Phase 2 ceased after 2.45 ± 0.35 min on average when the male
withdrew his genitalia; mean time of withdrawal did not differ between morphs
(U = 153, n = 36, p =.552). The morphs did differ
in the number of flutters performed per minute of phase 3 of copulation (taken
as minute 3 onward; see Figure
3A), with minors performing more flutters than majors (morph:
F1, 11 = 7.35; p =.02; repeated measure (minute):
F3, 33 =.32, p =.81; interaction:
F3, 33 = 1.84, p =.16). However, this difference
was not significant at the experiment-wide Bonferroni adjusted probability of
0.008 (sequential adjustment with 
= 0.05 for comparison of six related
behavioral events). Total copula duration was 7.88 ± 0.77 min and did
not differ between morphs (U = 191, n = 36, p
=.349). Matings observed in the net did not differ from those observed in the
peripheral vegetation of the emergence site for any parameter measured [e.g.,
for natural matings total copula duration was 5.7 ± 0.8 min (n
= 6) compared with matings in the net, U = 107.5, n = 38,
p =.280; phase 2 was 2.04 ± 0.40 min (n = 5) compared
with matings in the net, U = 76, n = 35, p
=.604].
Variation in sperm transfer
All experimental females were found to have sperm in the bursa copulatrix,
irrespective of the duration of copulation (n = 50). The volume of
ejaculate found in the bursa copulatrix (0.69 ± 0.11 mm3,
n = 11) was much greater than the volume of the spermatheca (5.31
± 0.09 x 10-3 mm3, n = 52),
suggesting that males transfer more ejaculate than females can store. To
determine how much ejaculate is transferred, we combined our data on testes
weights for males that had not been allowed to copulate with those obtained
from our sample of males used in experimental copulations and regressed log
testes weight on log body weight as before. Residuals from this analysis
showed that mated males had lighter mean residual testes weight (-0.17
± 0.02 mg) than unmated males (0.00 ± 0.01 mg; t =
7.47, df = 136, p <.001). Thus, residual testes mass provides us
with an approximate estimate of the amount of ejaculate transferred in
copulation.
Among mated males, there was no relation between the duration of copulation and residual testes mass (F1, 38 =.008, p =.930), suggesting that sperm are transferred immediately at the onset of copulation (Figure 4A). Neither was there a significant difference between major and minor males (t = 1.35, df = 38, p =.186), suggesting that males of both morphs transfer the same amount of ejaculate.
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The spermatheca filled rapidly with sperm. The optical density of the spermatheca was significantly greater in mated females than in virgins because of the presence of sperm (t = 5.07, df = 50, p <.001). Moreover, the optical density of the spermathecae of mated females increased over the course of copulation (F1, 46 = 4.08, p =.049; Figure 4B).
Female remating tendency
The probability that a female would mate with a second male (allowing
intromission and entering phase 2) decreased rapidly with the duration of the
first male's copulation (
2 = 36.33, df = 5, p
<.001; Figure 5B). The
behavior of second males is shown in Figure
5. Females rarely mated with a second male if they had experienced
an initial copulation that exceeded five zips (5 s in duration). When a
female's first mate had performed 
5 zips, the second male performed a
normal copulation, with no differences in the numbers of flicks in phase 1
(contrasting with first male in natural copulations; Kruskal Wallis H
= 1.479, df = 2, p =.48, n = 24; see
Figure 5A) or total number of
zips in phases 2 and 3 (H = 0.08, df = 2, p =.961,
n = 24; Figure
5B).
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Conversely, when a female's first mate had performed >5 zips, the second male failed to gain intromission and enter phase 2; second males performed an average of 23 wing flicks before dismounting (Figure 5A). There were two exceptions. One male gained intromission with a female that had experienced 15 s of zips, and another with a female that had experienced 30 s of zips. These males performed 8 and 55 zips, respectively, much less than in a normal copulation.
These results suggest that females are unlikely to mate more than once on emergence. Moreover, of 30 males tested in a net with 10 different females that had returned to the site to nest, none attempted to mount the female. The density of sperm in the spermatheca of nesting females did not differ from that in females experiencing a single complete copulation on emergence (nesting: 1.57 ± 0.10; once mated: 1.58 ± 0.02; t = 0.13, df = 37, p =.899). Finally, nesting females were never found with sperm in the bursa copulatrix (n = 30).
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DISCUSSION |
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Do minor males exhibit adaptation for sperm competition?
The puzzle posed by the abundance of small minor males in a species in which large major males apparently experience much greater reproductive success might be partly resolved if minor males compensated for reduced access to virgins by inseminating already mated females. The sperm competition hypothesis generates the predictions that minor males should differ from major males in producing more sperm (via proportionally larger testes) or providing more copulatory courtship designed to influence cryptic female choice or transferring a greater volume of sperm. None of these predictions were confirmed.
Studies of ejaculation strategies associated with alternative mating
tactics have come predominantly from research on fish. Typically, sneaker
males have a higher gonosomatic index (GSI) than guarding or territorial males
(reviewed in Taborsky, 1994),
and this is taken as evidence for selection via sperm competition. GSI is
calculated as the weight of the testes divided by body weight. The problem
with GSI is that it fails to take account of allometric scaling; when traits
scale with an allometric exponent <1.0, there is an a priori expectation
for smaller individuals to have relatively larger traits. The allometric
exponent for testis mass was 0.77. If we had calculated GSI for Dawson's
burrowing bees, we would therefore have concluded that minor males invested
relatively more heavily in testes. However, such a pattern is clearly not
indicative of a greater investment in sperm production; the two morphs did not
differ in their copulatory behavior or in the amount of ejaculate transferred
per copulation. Instead, we adopted the analysis of covariance approach as
recommended by Packard and Boardman
(1988). This approach
correctly revealed that after controlling for body mass, the two morphs did
not differ in testes mass. Thus, minor males of Dawson's burrowing bee show no
evidence of adaptation to sperm competition. In fish, sneakers are also
typically smaller individuals who are unable to compete successfully with
their larger conspecifics. Our data for Dawson's burrowing bee suggest that in
general it is difficult to determine the extent to which patterns of GSI
represent adaptations to sperm competition
(Parker, 1990) or patterns of
relative growth (Huxley,
1936), a problem recently highlighted in the study by Simmons et
al. (1999) of dimorphic male
beetles.
Do females tend to mate more than once?
The sperm competition hypothesis generates another key
prediction—namely, that females will mate with more than one male.
However, several lines of evidence suggest that female Amegilla
dawsoni rarely mate more than once. First, our mating experiments showed
that newly emerged females became highly unreceptive quickly after even a
brief period of intromission. Second, females returning to the emergence site
to begin nesting were also not sexually receptive, and indeed were ignored by
sexually active males. Third, our dissections showed that the density of sperm
in the spermatheca of females mated once under experimental conditions did not
differ from the density of sperm in nesting females.
Page (1986), and more
recently Boomsma and Ratnieks
(1996), have reviewed the
incidence of multiple mating in eusocial insects, pointing out problems
associated with the available methods for assessing female mating frequencies.
For example, observational data on monandry are difficult to verify because
females could regain sexual receptivity some time after an initial copulation.
However, we found that postemergent females are ignored by mate-searching
males, suggesting that loss of receptivity is permanent and that males are
capable of recognizing and avoiding unreceptive females.
A second problem in establishing mating frequencies arises because single
insemination cannot be determined by dissection data alone. Although females
may have a limited storage capacity, they may still store small amounts of
sperm from several different males or be subject to sperm displacement by each
of their mating partners. Thus, our dissection data can only be taken as
consistent with monandry. Nevertheless, recent microsatellite analysis of
parentage in bumble bees (Estoup et al.,
1995) has demonstrated that combined observational and dissection
data (reviewed in Page, 1986)
are accurate in assigning monandry in this genus. In addition, monandry is not
uncommon in the Hymenoptera (Boomsma and
Ratnieks, 1996; Page,
1986; Page and Metcalf,
1982) and indeed may be typical of slitary bees and wasps
(Thornhill and Alcock,
1983).
Dawson's burrowing bees also exhibit a variety of life-history and behavior
patterns that are consistent with monandry. Selection should favor adaptations
in males that enable them to find and inseminate virgin females during their
brief period of sexual receptivity. The bees show marked protandry, with males
emerging some 10 days before females, on average, and are able to detect
about-to-emerge females as soon as they break the soil surface (Alcock,
1997c). Strong protandry and rapid location of emerging females is a common
feature of monandrous bees, wasps, and other insects (reviewed in
Thornhill and Alcock,
1983).
Thus, although without molecular evidence we cannot be certain that female Dawson's burrowing bee are monandrous, the weight of evidence strongly indicates that multiple mating is rare or absent.
Copulatory and postcopulatory courtship in Dawson's burrowing
bee
A striking feature of reproduction in Dawson's burrowing bee is the
stereotypical behavior of males during copulation and also during phase 3, the
postcopulatory period after insemination. Vibration and sound communication in
the context of courtship and copulation have similarly been reported from
other solitary bees and wasps (Larsen et
al., 1986). The behavior fits precisely the criteria for
copulatory courtship outlined by Eberhard
(1996) and has been linked
with cryptic choice by females that possibly use male stimulatory performance
to decide which of several males' sperm to use to fertilize their eggs. Yet,
despite copulatory and postcopulatory courtship in Dawson's burrowing bees,
our data suggest that females rarely mate more than once. Moreover, females do
not make loss of sexual receptivity contingent upon receipt of copulatory
courtship, unlike another anthophorine bee Centris pallida
(Alcock and Buchmann, 1985).
Instead, females lose their sexual receptivity within the first 5 s of
copulation, long before completion of signaling by their copulatory partner
but coincident with receipt of sperm inasmuch as males ejaculate into the
bursa copulatrix soon after intromission has been achieved.
Although we can only speculate on the precise mechanism by which sexual
receptivity is lost, our data strongly imply the involvement of the ejaculate,
either via mechanical stimulation arising from the presence of sperm in the
female's reproductive tract or via refractory inducing substances transferred
in the seminal fluids. The fact that females became unreceptive without the
extended behavioral interactions of phases 2 and 3 of copulation suggest that
these phases are not directly responsible for altering female sexual
receptivity. Rather, the gradual accumulation of sperm in the spermatheca
suggests that the about 7 min of copulatory behavior functions in stimulating
the female to transport sperm from the bursa copulatrix to the spermatheca.
Permanent loss of female sexual receptivity may be contingent on sperm being
transferred to the spermatheca, in which case females receiving insufficient
copulatory courtship might regain receptivity some time in the future. If this
were true, the presence of copulatory courtship in Dawson's burrowing bee
would be evidence for cryptic female choice
(Eberhard, 1996).
Although certain features of the mating behavior of Dawson's burrowing bees
are incompletely understood, our data show that minor males have no obvious
adaptations for sperm competition and females do not appear to mate more than
once. As a result, we reject the hypothesis that success in sperm competition
can compensate for the costs of producing minor sons. The reason that minor
male Dawson's burrowing bee are maintaned in such high frequency must
therefore remain a puzzle (Alcock,
1996b).
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ACKNOWLEDGEMENTS |
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This study was funded by the ARC (L.W.S.) and the Royal Society (J.L.T.). We thank Sue Alcock for expert field assistance, even in the face of adversity, and Win Bailey for producing Figure 1.
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REFERENCES |
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