Behavioral Ecology Vol. 10 No. 1: 91-96
© 1999 International Society for Behavioral Ecology
Mate choice based on static versus dynamic secondary sexual traits in the dark-eyed junco
a Department of Biology, University of New Mexico, Albuquerque, NM 87131, USA b Department of Biology and Center for the Integrative Study of Animal Behavior, Indiana University, Bloomington, IN 47405, USA c Department of Mathematics, James Madison University, Harrisonburg, VA 22801, USA
D. A. Enstrom is currently at the Center for Biodiversity, Illinois Natural History Survey, Champaign IL 61820, USA.
Received 7 July 1997; accepted 9 July 1998.
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ABSTRACT |
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Some secondary sexual traits (SSTs) such as structural characteristics are semi-permanent or static, while others, such as courtship display, are more labile or dynamic. In this paper we report results from two experiments designed to test the relative attractiveness to female dark-eyed juncos (Junco hyemalis, Passeriformes, Aves) of a relatively static plumage trait, the amount of white in the tail, and a relatively dynamic behavioral trait, courtship intensity. The experiments derived from a study showing that female juncos prefer males that court more vigorously. We asked whether females also base their preferences on plumage traits and how they respond when presented with a choice between attractive traits that are either static (plumage) or dynamic (courtship) in nature. In the first experiment we presented males to females in paired mate-choice trials and found that males enhanced with more white in their tails were more attractive to females than controls with unenhanced tails. Females spent more time with enhanced males and directed more sexual displays toward them. In the second experiment we tested whether females preferred males with enhanced tails (a static SST) or males with enhanced hormone-mediated courtship behavior (a dynamic SST). In this experiment females did not demonstrate a consensus preference for either the static or the dynamic trait. Instead, some females preferred the male whose courtship performance was enhanced with testosterone, while others preferred the male with an enhanced tail. We conclude that both kinds of traits are important in junco mate choice, but that some females apparently weigh static traits more heavily than dynamic ones, while other females use opposite weightings.
Key words: darkeyed juncos, Junco hyemalis, lability, mate choice, secondary sexual traits.
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONACKNOWLEDGEMENTSREFERENCES |
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Secondary sexual traits (SSTs) vary greatly in the lability of their expression. Some are highly dynamic, their expression changing rapidly with ecological, physiological, and/or emotional state; an example is the nuptial coloration of some fish (Lanzing and Brower, 1974)
. Other SSTs are relatively static, with little or no change
in expression after their development for a particular episode of breeding, as
in antlers in ungulates or plumage in birds (Payne,
1972). Most SSTs lie somewhere between these two extremes,
exhibiting variable potential for shifts in expression as well as variable lag
periods between a change in the state of the animal and a change in the
expression of the trait.
The significance of variation in lability of expression of SSTs is unclear.
Models of intersexual selection based either on Fisherian runaway processes
(Fisher, 1958;
Lande, 1980) or on preexisting aesthetic
preferences and sensory biases (Basolo,
1990; Burley et al.,
1982; Ryan, 1990) make
no predictions about expected degree of SST lability. Models positing that
SSTs have evolved to facilitate female assessment of variation in male quality
(e.g., Hamilton and Zuk, 1982;
Kodric-Brown and Brown, 1984;
Zahavi, 1975), predict that females
should prefer traits that are the most reliable indicators of quality. There
are, however, opposing opinions regarding the relationship between reliability
of SSTs and lability of expression. On the one hand, highly dynamic SSTs might
be the most accurate indicators of male quality because they respond rapidly
to changes in male condition (e.g., Folstad and
Karter, 1992; Wingfield et al.,
1990) and, therefore, provide females with current information
regarding the condition of prospective mates. On the other hand, static SSTs
may be more reliable indicators because they are less sensitive than dynamic
traits to stochastic environmental factors that can affect trait expression
(e.g., Møller and Pomiankowski,
1993). Dynamic SSTs may also be less reliable if relatively
inferior males are able to sustain deceptively high-quality trait expression
for short periods of time.
Traits of differing lability may also convey different information
regarding condition or status (Sorenson and
Derrickson, 1994). For example, avian plumage development (molt)
is an expensive physiological process (e.g., Payne,
1972), and plumage expression (morphology and color) has been
shown to be affected by condition during molt (e.g.,
Johnsen et al., 1996). Thus, plumage
expression, by virtue of its physiological cost, may provide an excellent
index of the bearer's genetic quality or long-term viability. However, because
molt usually occurs between breeding seasons, plumage may not provide a good
measure of current condition at the time of mating. Females that focused
solely on plumage might be mislead; whereas females that relied on
plumage during mate choice as well as on more dynamic SSTs (such as song or
courtship display) might obtain a more complete picture of male quality.
To establish experimentally the relative importance to mate choice of
traits of different labilities, it is necessary to simultaneously manipulate
dynamic and static SSTs and then measure their effect on male attractiveness.
We investigated the effect of two male secondary sex characteristics, one
relatively static and one dynamic, on female mating preferences in the
dark-eyed-junco, Junco hyemalis carolinensis. The juncos we study are
socially monogamous North American buntings (Emberizinae) that are ideally
suited for this investigation for two reasons. First, experimentally
manipulated testosterone (T) is known to affect male courtship intensity and
attractiveness (Enstrom et al., 1997).
Males maintained at peak levels of testosterone (T-males) throughout the
breeding season court more vigorously (Enstrom et
al., 1997) and sing more frequently
(Ketterson et al., 1992) than control
males with basal breeding season levels of the hormone, and in matechoice
experiments females prefer T-males to controls
(Enstrom et al., 1997). Thus, T-mediated
courtship behavior can be viewed as a dynamic SST in this species. Second,
results from a preliminary set of experiments suggested that females respond
to the amount of white color in male tail feathers (rectrices), a relatively
static SST (Hill et al., unpublished observations). Courting males spread
their tails and exhibit the white in their outer rectrices, and increasing the
amount of white by replacing dark feathers with white ones appears to make
them more attractive to females. Thus, in juncos, it should be possible to
investigate male attractiveness by independently altering both dynamic and
static SSTs.
Here we report two experiments. In the first, we manipulated the amount of white in male tail feathers to confirm that this plumage character affects male attractiveness and female mate choice. In the second, we manipulated both the amount of white in the tail and the testosterone level to test the relative importance of both traits to female mate choice.
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METHODS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONACKNOWLEDGEMENTSREFERENCES |
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Study species
J. h. carolinensis is a common breeder above 1000 m in the vicinity of Mountain Lake Biological Station (MLBS) of the University of Virginia, Giles County, Virginia, USA, where we work (see Chandler et al., 1994
, for a description
of the study site). Winter flocks break up and juncos establish territories in
April. Pairs from during April and early May. Females build the nests and
incubate, and both sexes care for offspring. Juncos are socially monogamous,
but extrapair fertilizations are fairly common, and males sire only
60-75% of the offspring they help to rear
(Ketterson et al., 1996,
1997;
Raouf et al., 1997). Male success at
siring young through extrapair copulations varies, indicating that the
potential for sexual selection is high (Ketterson et
al., 1996, 1997;
Raouf et al., 1997).
Male junco courtship displays consist of song, erection of body plumage
(ptiloerection), pulsatile spreading of tail feathers, and manipulation of
nest material (Enstrom et al.,
1997; Titus et al.,
1997). Performance of these behaviors is at least in part
controlled by T (Enstrom et al., 1997)
and so can be highly labile, potentially affected by such factors as social
status, condition, and age.
In adult juncos of both sexes, prebasic molt occurs in autumn and is
complete; thus the wing and tail feathers are replaced. In yearlings
these feathers are produced while young are still dependent on their parents
and are retained through the following breeding season. The spring
prealternate molt in all ages and both sexes is slight and does not involve
flight feathers (Pyle et al., 1987;
Nolan et al., 1992). Thus, plumage color
is static, fixed for the year (except for slight fading) at least 6 months
before the onset of breeding.
Junco plumage is gray with sharply contrasting white on the breast and
tail. Sex- and age-related dichromatism is detectable by experienced field
workers (Balph et al., 1979;
Ketterson, 1979): males are darker
than females and have more extensive white in their tail
(Figure 1). Among males, adults are darker
than yearlings and also have whiter tails. Rectrices (six pairs, the innermost
pair numbered 1, the outermost 6) vary in color: the proportion of the
feather that is white usually is greatest on pair 6, intermediate on pair 5,
and least on pair 4; a trace of white is occasionally found on pair 3.
Feathers belonging to pairs 6 and 5 are often entirely or mostly white on
males and on some females; pair 4 is usually largely white in adult
males, less so in yearling males, and still less so in females.
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Capture and housing
We captured (at baited mist nets) 30 females and 22 males between 14 and 16
April 1995. Before mate-choice trials, males were housed singly in cages (0.6
x 1.2 x 2.4 m) in an outdoor aviary; females were housed
singly or in groups of two in identical cages. Birds were fed mealworms,
water, and a variety of seeds ad libitum.
We weighed all birds, measured wing (flattened), tail, and tarsus length, and scored the darkness of the gray of the crown (using the Munsell neutral value scale) and the amount of white in the tail (hereafter "tail white"). We scored tail white by estimating the proportion of white (in 0.1 increments) on rectrices 6-3 on the right side of the tail and summing these proportions. For example, three completely white tail feathers would result in a score of 3, which is higher than occurs in nature (see Figure 1).
Hormonal treatment of females
We implanted females subcutaneously with one 8-mm length (1.47 mm i.d.,
1.96 mm o.d.) of silastic tubing containing crystalline ß-17-estradiol to
stimulate expression of unambiguous precopulatory displays. In previous
experiments Enstrom et al. (1997) showed
that this treatment increases the tendency of female juncos to give
precopulatory displays, but has no influence on their preferences for males in
mate choice trials.
General experimental protocol
Each mate-choice experiment consisted of trials in which a single female
was allowed to choose between two simultaneously presented males of different
phenotypes. Males were presented to females in a Y-shaped aviary described and
depicted in Enstrom et al. (1997). On the
afternoon before their presentation to females, males were placed in
enclosures in the arms of the Y-aviary and allowed to acclimate. The following
morning, the preferences of three females, one at a time, were tested with
this male pair. Each female was first held in a small assessment cage (0.31
x 0.31 x 0.62 m), from which she could view both males, and then
released into the larger aviary and allowed to express her preference as
described below. After the third trial male positions were switched from one
arm of the Y to the other in preparation for the next day, when three more
females were tested. In experiment 1, four male dyads were presented to six
females each, and two dyads were presented to three females each. In
experiment 2, each of five different male dyads was presented to six females.
We tested potential effects of dyad and male position on female attendance
time (see below) and found no effect of either variable in either experiment
(ANOVAs; experiment 1: F3,8 = 1.87, p
=.14; experiment 2: F3,7 = 0.74, p
=.67).
In both experiments 1 and 2, each trial consisted of two parts: a
20-min period of assessment by the female and a 30-min period of active female
choice. Males courted females both during the assessment period and during the
period of active choice. During the assessment period, the female could see
and hear both males from a distance of 1.6 m (0.5 m closer than described in
Enstrom et al., 1997). Following the
assessment period, the female was released into the Y for the period of active
choice. During this period, the female could approach and interact with one or
the other male through the hardware-cloth front walls of his cage. When a
female was within 0.9 m of the wall of either male's cage, a wooden barrier
prevented her from seeing the other male; and time spent by the female
within 0.6 m of a male cage was scored as attendance time in the choice area
of that male (see Enstrom et al.,
1997).
We evaluated each female's preference on the basis of two a priori criteria. The first criterion was attendance time with each male. The second was the number of precopulatory displays given to each male from within his choice area. Behavior and time spent in other parts of the cage were considered neutral. We treated a trial as successful (i.e., indicative of a preference) if the female spent at least 7.5 min (one quarter of her active choice time) in either of the male choice areas (combined). Females that failed to meet this criterion were retested after at least 3 days had elapsed. Females were tested as many as three times; an individual that still showed no choice was removed from the experiment. We considered a trial as ending in a tie if the difference in attendance time with each male was less than 10% of the total time spent associating with both males (e.g., if a female spent 6 min with one male and 5 min with the other, the difference in time spent, 1 min, would be less than 10% of the total 11 min of attendance time; trial declared a tie). Although the results including ties were similar, the criterion for ties was established a priori, and ties are not reported in the results.
We compared the behavior of the two male treatment groups by quantifying
song rates and the extent of ptiloerection, an index of courtship intensity
(Enstrom et al., 1997). The most
exaggerated ptiloerection in each minute of the period was ranked on a scale
of 1 (lowest) to 3. Scores were averaged over the entire period to determine a
mean ptiloerection score. Male behavior was recorded during a 30-min
observation period at the start of each day before the introduction of the
first female and during the assessment period of each trial. We did not
quantify male behavior during the period of active choice because the
proximity of the female largely determines male behavior at that time (see
Enstrom et al., 1997).
Experiment 1: Increased tail white and male attractiveness
In experiment 1 (29 April-19 May 1995) we tested female preference for
males with experimentally increased tail-white compared to control males whose
tail white was within the normal adult male range. Male dyads were matched for
age (yearling or older), size, and body mass (within 2.2 mm wing length and
within 2.3 g mass).
We manipulated tail white according to the methods described by Holberton
et al. (1989). We cut retrices 3 and 4
approximately 1 cm from the pygostyle, hollowed out the remaining feather
shaft with a needle, and inserted and glued (super glue) a new feather
(trimmed at its distal end to match the size and shape of the natural
feather). Before manipulation the mean male tail-white score was 2.45
(Figure 1). In experimental males, we
replaced rectrices 3 and 4 on each side with four white feathers, producing
tail white scores of about 4. In control males we replaced rectrices 3 and 4
with feathers similar in color to those that were removed, producing a mean
score of 2.4 (i.e., unchanged).
Experiment 2: Female preference for extent of tail white and
intensity of courtship behavior
In this experiment we tested (31 May-15 June 1995) whether females
preferred males with increased tail white or males with enhanced
hormone-mediated courtship behavior. One treatment group, which we refer to as
ES for enhanced static trait, consisted of males with increased tail white
that had participated in experiment 1; these males were implanted for
the purposes of experiment 2 with two empty 10-mm silastic tubes. The other
group, which we refer to as the enhanced dynamic trait (ED) group, was
composed of control males (normal tail-white scores) from experiment 1, now
implanted with two 10-mm lengths of silastic tubing packed with crystalline
testosterone (for implanting details, see Ketterson
et al., 1992, 1996). As
stated earlier, these treatments created two classes of males: (1) those
with T levels similar to free-living males after the spring peak (empty
implants) and with increased white in their tails (ES males), and (2) those
with elevated T levels resembling the spring peak (T implants) and with
naturally colored tails (ED males). Males remained in the same dyads they had
belonged to in experiment 1; however, no female saw the same dyad in
experiment 2 that she had seen in experiment 1.
Analysis
We compared central tendency in attendance time using Wilcoxon
paired-sample tests; numbers of females preferring one or the other type
in each experiment were compared using binomial tests. P values are
two-tailed for all tests except those in which we made a priori predictions,
which are indicated.
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RESULTS |
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Experiment 1
Male behavior
In the absence of females, the behavior of males did not differ according to treatment. Males did not engage in courtship behaviors before the introduction of females, and song rates of experimental (increased tail white) males (mean = 0.01 songs/min) and control males (mean = 0.02) did not differ significantly (Wilcoxon paired-sample test: Z = -1.0, n = 6, p =.37).
During the period of female assessment, male ptiloerection did not vary significantly with treatment (experimental males, mean = 22.12; control males, mean = 19.53; Z = -0.74, n = 6, p >.46). There was also no significant difference in song rate between experimental (mean = 0.01) and control males (mean = 0.37; Z = 1.54, n = 6, p =.15).
Female behavior
During the 30-min active choice period, females spent significantly more
time with experimental males (mean = 11.42 min) than with control males (mean
= 5.19; Z = -2.40, n = 24, one-tailed p
<.01). Nineteen of 24 females preferred experimental males (binomial
test: n = 24, p <.01;
Figure 2).
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Nine of the 24 females tested gave 39 precopulatory displays during experiment 1. The rate of display toward experimental males (mean = 1.33 displays/trial) was significantly greater than that toward controls (mean = 0.46; Wilcoxon paired-sample test: Z = -1.93, n = 24, one-tailed p =.03). Seven females displayed only to the experimental male; two displayed to both the experimental male and the control.
Experiment 2
Male behavior
In the absence of females, ED males sang at a significantly higher rate
(mean = 0.19 songs/min) than ES males (mean = 0.01; Z = -1.60,
n = 5, one-tailed p =.05).
During the period of female assessment, ED males again sang at a significantly higher rate (mean = 0.83 songs/min) than ES males (mean = 0.25; Z = 1.83, n = 5, one-tailed p =.03), and they had higher average ptiloerection scores (mean ED males = 7.9) than ES males (mean = 4.8; n = 5, one-tailed p =.04).
Female behavior
Females spent similar amounts of time with ED males (mean = 7.16 min) and
ES males (mean = 9.67 min) during activechoice (Z = -1.15, n
= 20, two-tailed p =.2; power = 0.43 at 
= 0.05).
Fourteen of the 20 females spent more time with the ES males than with the ED
males (binomial: n = 20, p =.06;
Figure 3).
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Five of the 20 females tested gave 15 precopulatory displays during experiment 2: 10 of the displays were given to the ES males and 5 to the ED males. Two females displayed only to the ES male, one displayed only to the ED male, and two displayed to both males.
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONACKNOWLEDGEMENTSREFERENCES |
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Female juncos appear to rely on both static (plumage) and dynamic (courtship intensity) SSTs to assess potential mates In our first experiment, females demonstrated a significant preference for males with whiter tails, suggesting that evaluation of plumage may be sufficient to influence the assessment of male attractiveness. Enstrom et al. (1997)
had previously established that
female juncos can base their choice of mate on a dynamic SST, courtship
intensity. Together, these results provide further support for the possibility
that female preference for male SSTs can drive sexual selection in socially
monogamous, relatively monomorphic species (Ketterson
et al., 1997; Johnson and Burley,
1997). Consistent with this view, genetic paternity analysis of
this study population suggests that the potential for sexual selection is high
(Ketterson et al., 1997).
In experiment 2 we found that females did not show a significant consensus
preference for either the ED (testosterone-enhanced courtship) or the ES
(increased tail white) male. Power was low in this experiment, however, and
more females did prefer the ES male (14) over the ED male (6). Furthermore,
the choice we presented was between an enhanced dynamic trait within the range
of natural variation (our T manipulation mimicked natural peak levels, see
Enstrom et al., 1997) and an enhanced
static trait that was exaggerated beyond the range of natural variation (our
manipulation increased the amount of white in the tail by at least one
third; Figure 1). It is therefore
possible that our ES treatment acted as a supernormal stimulus and that our
result does not reflect the relative appeal of these two SSTs during normal
mate choice. However, individual females did express a clear preference for
one or the other treatment, and we conclude that both behavior and plumage are
important during mate choice in this species.
The apparent tendency for some females to focus on plumage while others focus on behavior is consistent with a result from experiments investigating age-based mate choice in juncos (Enstrom et al., in preparation). In that study we found that females overwhelmingly preferred older males to yearlings (older males naturally court more vigorously and have "brighter" plumage than yearlings, including whiter tails). However, when yearlings were implanted with T and older males received empty implants (causing the yearlings to court more vigorously than the older males), some females preferred the yearlings (11), while others preferred the older males (14). Here again, some individuals appeared to favor the bright plumage, while others evidently favored the behavioral effects produced by enhanced T.
In general, female birds appear to base their choice of mates on a variety
of SSTs. Numerous studies have demonstrated female preferences for static
traits, such as tail length (Andersson,
1982; Saino et al.,
1997) and plumage coloration (e.g., Hill,
1990), for moderately labile traits, such as comb color and
morphology (e.g., Zuk et al., 1990,
1992) and song repertoires (e.g.,
Searcy and Brenowitz, 1988), and for
highly dynamic behavioral traits, such as courtship performance and bower
decoration (e.g., Borgia, 1993;
Enstrom et al., 1997;
Houtman, 1992). In addition, suites of
SSTs of differing labilities appear to be involved in mate choice in several
species (e.g., Gibson and Bradbury,
1985; Zuk et. al.,
1992). For example, male jungle fowl (Gallus gallus) have
relatively static SSTs (plumage color and morphology), somewhat dynamic SSTs
(comb color and morphology), and highly dynamic SSTs (courtship behavior)
(Zuk et al., 1990). That more than one
SST may affect mate choice is shown by studies demonstrating choice based on
multiple criteria, which can include both static and dynamic SSTs
(Burley, 1981;
Gibson and Bradbury, 1985;
Johnsen and Zuk, 1996;
Sorenson and Derrickson, 1994;
Zuk et al., 1992).
Choice based on several traits of differing labilities might evolve if
these traits convey information about different aspects of a male's quality
(Møller et al., 1998;
Sorensen and Derrickson, 1994). For
example, courtship intensity may provide accurate information regarding a
male's current condition, whereas plumage expression may better reflect
longterm condition or viability. Females may also use plumage to determine the
age of potential mates (e.g., Enstrom,
1993; Enstrom et al., in preparation) but use courtship
intensity to assess health or viability. It is also possible that individual
female condition or experience affects which traits are salient for her during
mate choice. These questions call for experiments that quantify variation in
mating preferences (Arnold, 1983) in
relation to changing female condition (e.g., age, previous mating success,
hormonal state).
Our results are also consistent with models of intersexual selection that
do not predict particular patterns of lability in SST expression. Indeed, our
finding that females prefer tail white exaggerated beyond the range of natural
variation supports the hypothesis that female preferences originate before,
and subsequently drive, the evolution of male SSTs
(Basolo, 1990;
Burley et al., 1982;
Ryan, 1990). This preference for
supernormal tail-white expression is not consistent with the view that females
discriminate against phenotypic extremes and implies that females are not the
selective factor that limits tail-white expression in males.
Our results suggest that female mating decisions may be based on simultaneous assessment of two or more SSTs of differing labilities and reveal that female juncos have no strong preference for either the static or the dynamic trait. Current understanding of how selection might affect lability of expression of SSTs is poor. Continued research into the decisions females make when faced with both dynamic and static SSTs and the forces that shape those decisions is needed. This will require focusing not only on variation in relevant male traits, but also on variation among females in their preferences for these traits.
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ACKNOWLEDGEMENTS |
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We thank Mountain Lake Biological Station (MLBS) of the University of Virginia and the Mountain Lake Resort Hotel for their support for this project. H. M. Wilbur provided statistical advice and invaluable logistical support. We also appreciate the contributions of those intimately involved in the junco project (K. Bruner, L. Christensen, S. Hudman, T. Kast, S. Lynn, D. Morris, S. A. Raouf, M. Rosenshield, E. Snajdr, and R. C. Titus). We thank R. A. and D. S. Johnson for general "life" support. This research was supported by the National Science Foundation (BSR-911498 and IBN-94-08061 to E.D.K. and V.N. Jr.), by the Center for the Integrative Study of Animal Behavior at Indiana University (D.E.), and by an MLBS Walton Fellowship (J.A.H.).
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