Behavioral Ecology Vol. 12 No. 4: 402-406
© 2001 International Society for Behavioral Ecology
Male pipefish prefer dominant over attractive females
a Department of Animal Ecology, Uppsala University, Norbyvägen 18d, S-752 36 Uppsala, Sweden b Department of Zoology, Norwegian University of Science and Technology, N-7491 Trondheim, Norway
Address correspondence to A. Berglund. E-mail: anders.berglund{at}ebc.uu.se .
Received 14 April 2000; revised 1 September 2000; accepted 7 September 2000.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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Animals may obtain information guiding their choice between potential partners from observing competitive interactions and displays between them, or from displays directed at the choosing individual. In the sex-role reversed pipefish Syngnathus typhle females display a temporary ornament (a color pattern) to other females as well as to males. We have previously shown that display of female ornaments per se is attractive to males. Here we show that information from competitive displays can override such direct attraction displays as signals in the partner choice process. In a mate choice experiment, an enclosed male could choose between two females. On the first experimental day, females could interact freely, while on the second day they were isolated from each other. When female-female competition was allowed, the ornament display was directed more to the other female than to the male: Time competing, rather than time courting the male, correlated with ornament display duration. However, ornament display under competition and ornament display in the absence of competition did not correlate significantly. In fact, females competing more intensively on day one displayed the ornament less on day two. Furthermore, the ornament display during the first, but not the second, day predicted male mate choice on the second day. Thus, males remembered previous information from competitive displays and used it rather than immediate information from displays in the absence of female-female competition. We suggest that competitive displays more reliably signal female quality as compared to noncompetitive ones, and that males benefit from mating with dominant females.
Key words: mate choice, mate competition, ornament, pipefish, sexual selection, signal honesty, Syngnathus typhle.
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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A sexually selected signal usually serves both as an armament (a weapon or a status badge) and as an ornament (a mate attractant; Berglund et al., 1996
).
However, this may not be invariably true for all sexually selected signals
(Forsgren, 1997;
Moore and Moore, 1999;
Qvarnström
and Forsgren, 1998), because messages like "high fighting
ability" and "tender parental care" may be difficult to
communicate convincingly through the same signal (Zahavi A, personal
communication). Nevertheless, in a majority of cases the same signal has been
found to function in both contexts
(Berglund et al., 1996; Mateos
and Carranza, 1997,
1999). Furthermore, signals of
competitive ability can be expected to be attractive in themselves. Given that
such information is used in mate choice, will a direct observation of
competitive interactions/displays be more important to a choosing individual
than observations of some ornamental display meant to attract the chooser?
Since not necessarily all individuals signal their quality honestly, we expect
direct observations of competitive displays to yield more reliable information
about the condition of the potential partner than do purely attractive
displays. This is because condition is immediately put to trial in a contest
situation (through potentially costly fights), whereas the punishment for
discovery of a faked signal of attraction is much less severe (a lost mating
opportunity; see e.g., Berglund et al.,
1996; West and King,
1980; West et al.,
1981). Because a low frequency of dishonest signals of attraction
may be evolutionarily stable (Kokko,
1997; Viljugrein,
1997), a preference for sources of information that have passed a
test may be common in animals. This is further corroborated by the frequent
observation that competitive encounters in many species seem to be staged or
incited by the choosing sex (Bisazza et al.,
1989a,b;
Borgia, 1981;
Cox and LeBoeuf, 1977;
Farr and Travis, 1986;
Thornhill, 1988). In this article we show that in a sex-role reversed species, the pipefish Syngnathus typhle L., a male's mate choice is influenced more by a female's competitive display than by her attraction display. We also show that males are able to remember and utilize earlier information about competitive ability in preference to more recent information from attraction display in their choice of mates, indicating the overriding value of information from competitive interactions for mate choice in this species.
The pipefish
A lengthy and ritualized mutual dance precedes copulation in all pipefish.
In S. typhle, females transfer eggs to a brood pouch under the male's
tail, where he then fertilizes them. Subsequently, embryos are nourished and
oxygenated in the pouch until birth several weeks later (Berglund et al.,
1986a,b).
Males consequently enjoy a paternity confidence of exactly 100%, as confirmed
by a recent microsatellite analysis of maternity and paternity in this species
(Jones et al., 1999). From
many laboratory experiments and field observations we already know that S.
typhle is sex-role reversed: males are typically more choosy and females
compete more intensely than males for access to mates (Berglund,
1999,
2000; Berglund and Rosenqvist,
1990,
1993; Berglund et al.,
1986a,b;
Vincent et al., 1994,
1995). Fecundity increases
with body size in both males and females, and given a choice both prefer to
mate with larger partners (Berglund et
al., 1986a).
The ornament
Female S. typhle display a temporary ornament when interacting
either with other females or with males. The ornament is a striped contrasting
dark color pattern resembling a row of capital B's along the female's side
(Fiedler, 1954). Ornament
appearance is rapid, occurring within a minute, and the display may also
vanish just as fast. Both males and females are normally extremely cryptic
because their color, shape, and movements look like eelgrass (Zostera
marina L.; Vincent et al.,
1994,
1995). Therefore, the ornament
display decreases crypsis in females, which consequently are reluctant to
display under perceived predation threat
(Bernet et al., 1998).
We have previously shown that females who spontaneously display the
ornament for a longer time enjoy a higher mating success than females giving
briefer display (Bernet et al.,
1998). Furthermore, when kept with a male, females are more likely
to display the ornament under female-female competition than in the absence of
competition (Bernet et al.,
1998). Moreover, females displaying more are also more fecund than
similar-sized females displaying less
(Berglund et al., 1997). In
addition, males have been found to prefer ornamented females over
nonornamented ones: an experiment where females were manipulated (painted) to
differ in ornamentation but not in behavior (females were sedated and
mechanically moved up and down by a motor) confirmed that males pay attention
to the ornament even when female behavior was kept constant
(Berglund and Rosenqvist,
2001).
Pipefish mating competition
Overt aggression is less apparent in these slow-moving, joint-jawed, and
toothless fishes. Female S. typhle compete for males indirectly
through dominance hierarchies, and large females may interfere with and
substantially decrease reproduction in small ones
(Berglund, 1991). Competition
may, however, also be overt. In nature male S. typhle actively search
for, choose among, and reject some females, while females vigorously display,
often in temporary groups in a lek-like fashion. Males typically swim
cryptically within the eelgrass in search of females. Females display by
swimming up and down and in and out of the eelgrass, with their ornaments in
full bloom. Once such a displaying group of females is encountered by a male,
he may start dancing and mating with one of them, usually a large individual
(Vincent et al., 1994,
1995). Females actively
compete among themselves for matings during such group displays, and may try
to herd other females away from the male
(Vincent et al., 1995). When
this happens, mating is interrupted, and indeed attempts to copulate can be
thwarted for a long time by interference from other females (Berglund A and
Rosenqvist G, own field and aquaria observations, unpublished data).
Displaying, dancing, and mating are risky behaviors in the otherwise
reticent life of pipefish (Berglund,
1993; Bernet et al.,
1998; Fuller and Berglund,
1996). Therefore, it may well pay males to select dominant
females, which are able to discourage other females from courtship
interference, as this will reduce the time spent on potentially risky
behaviors. Moreover, males do not have to worry about the potential conflict
between female signals of dominance and signals of caring ability, as females
contribute no care, only eggs. Moreover, we have never observed female
aggression towards males. Thus, our prediction is that males should treasure
dominance and competitive ability highly in females, and that direct
observations by males of such abilities in females may be more important than
attraction displays in the male's mate choice process. Indeed, any female can
display her ornament, but females having done so under actual female-female
competition have demonstrated their power and competitive ability in a
potentially costly situation. Therefore, males mating with such evidently
dominant females can expect a smooth courtship and copulation process, gaining
direct benefits for themselves in terms of reduced risk, as well as possible
direct and/or genetic benefits for their offspring from mating with high
quality females.
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METHODS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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We caught the pipefish in shallow eelgrass meadows in the Gullmar Fjord on the Swedish west coast during the latter half of May 1997, before the breeding season commenced. We kept sexually mature males and females in separate aquaria to assure that individuals would be reproductively active. Stock aquaria contained plastic plants and continuously renewed sea water (natural temperature, salinity, and light regime). Fishes were fed brine shrimps (Artemia), small, wild-caught crustaceans, and frozen mysids ad lib.
To explore the importance of competitive versus purely attractive displays we ran a mate choice experiment 28 May-20 June. Each of 24 trials was run for 2 days, with one male choosing between two females. The females came from different stock aquaria. The male was separated from the females by a transparent plastic divider. During the first day females could interact freely with one another, but during the second day they were separated from one another by an opaque divider (Figure 1). Separated females could not see or smell each other, but the male could see and smell both females both days as water flowed from the female compartment(s) into the male's and then out of the aquarium. Thus, males could observe and dance with females on the first day, and females could compete, dance and display their ornament on that day. On day one, we placed the females in the rear compartment and the male in the front compartment (Figure 1), and videotaped them for 10 h. On this day, we measured the time each fish spent dancing, how long females displayed their ornaments and whether females competed or not. A male and a female were defined as dancing when they simultaneously bobbed up and down in close proximity while facing one another. We considered females to be competing when they pursued each other round in the aquarium for more than a minute.
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On the second day, we measured male choice of a female in the absence of
female-female competition by placing the opaque divider between the females
and filming for another 10 h. Females were allocated to either chamber
randomly. After that males and females were released back into the wild. No
mortality occurred during trials. We measured the duration of female resting,
swimming, dancing, and ornament display, and the duration of male resting,
swimming, and dancing before either female. The female with which the male
spent the longest time was considered as the chosen one (a longer time with
the female has earlier been shown to accurately predict mate choice;
Berglund, 1994).
We filmed two trials simultaneously in 125 1 aquaria (45 x 50 x
60 [height] cm). The aquaria were continuously provided with surface sea
water. Temperature and light conditions followed natural conditions. We
planted fresh eelgrass in beach sand in the aquaria for shelter. Fish were not
fed during trials. We selected females of similar standard length (within 10
mm of each other) and of the same contrast score (the vaguely striped basic
pattern from which the ornament is formed, as estimated by eye on a five-grade
scale; see Bernet et al., 1998
for details), but individually recognizable by color (estimated by eye). New
males and females were used in each trial. Males were smaller than females
(males 177 ± 21 mm, n = 24, females 226 ± 27 mm,
n = 48, t70 = 8.00, p <.001), as in
the natural situation (in our 1997 field samples males were on average 161
± 28 mm, females 191 ± 38 mm).
Videotaping was done with Hitachi Hi-8 WM-H80E video cameras connected to Panasonic AG-6730 time-lapse super-VHS video recorders equipped with AG-IA670 time code generators/computer interfaces, using the 24 h time-lapse mode (which employs 1/8 normal speed). Intense light (a 100W spot and a 20W luminescent lamp placed 1/2 m above each aquarium) was used during filming, in addition to natural light from windows. Videotapes were analyzed using the Observer 3.0 VTA software, and persons scoring videos were unaware of the objective of the study. The Observer software kept track of duration and latency of behaviors with a precision of less than a second, which is an accuracy far more than enough for these slow-moving fishes.
Statistical probabilities reported from these experiments are two-tailed. Nonparametric tests were used whenever the assumptions of parametric tests were not met. Experiments were performed under a license from the Swedish ethical board.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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We classified the two females in a pair as "the one displaying the ornament for a longer time" and "the one displaying for a shorter time," respectively, during day one. We found no significant differences between these two female categories in standard body length (long displaying females were on average 228 ± SD 29 mm, short displaying 221 ± 26 mm, paired t test, t19 = 1.42, p =.2) or contrast (mean 3.10 ± 2.00 for both groups of females, Wilcoxon matched-pairs test, T = 6, n = 20 pairs, p = 1). In four trials both females either constantly displayed the ornament or did not display it at all; these females were discounted. When females instead were categorized as being "chosen" or "rejected," that is, which female the male spent most or least time with on day 2, again female lengths did not differ (chosen females 229 ± 27 mm, rejected 224 ± 26 mm, t23 = 1.25, p =.2), nor did contrast (3.08 ± 0.4 in both groups, T = 85, n = 24 pairs, p = 1). Thus, our experiment included closely matching pairs of females.
Female color did not significantly influence male choice (females broadly categorized as brown or green, 17 brown and seven green females were chosen, binomial p =.152) or which female displayed the ornament for the longest duration on day one (14 brown versus six green, binomial p =.116). Pairing was not color-assortative: green males chose two green and six brown females, and brown males chose four green and 10 brown females (Fisher's Exact test p = 1). Similarly, females did not display their ornament in a color-assortative fashion: green females displayed more to two green and five brown males, and brown females more to five green and six brown males (Fisher's Exact test p =.6).
Females displaying the ornament for a longer time on day one were preferred by males on the second day, compared to females displaying for a shorter time (Figure 2). Preference is here estimated as the total time a male spent in front of a female, but if instead the dancing duration with either female on day two is used as a choice index the same result emerges (males danced with more ornamented females for 15.9 ± 15.4 min and with less ornamented for 6.2 ± 9.8 min; T = 26, n = 20 pairs, p <.01). No choice for any particular female was evident on day one (p >.3 for dancing duration), but on that day dances were both infrequent and of short durations. Females displaying their ornaments for longer on day two were, however, not preferred by males as compared to females displaying for shorter on day two (291.4 ± 144.0 versus 306.0 ± 143.4 min total time before the respective females; T = 104, n = 20 pairs, p = 1). If dancing duration day two is used instead of total time as a choice index, the same result emerges (p =.5).
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Similarly, females chosen on day two had displayed their ornaments for longer on day one (chosen females for 233.2 ± 176.7 min, rejected for 130.3 ± 151.5 min; T = 40, n = 24 pairs, p =.015) but not on day two (123.7 ± 171.8 and 99.7 ± 128.4 min, respectively; T = 85, n = 24 pairs, p =.5).
On day one, females could either display the ornament to each other, in which case the duration of ornament display would correlate with the duration of competitive interactions, or females could display the ornament to males, in which case ornament display duration would correlate with the duration of intersexual interactions (i.e., dancing duration). It turned out that ornament display correlated significantly with competition duration, but not with dancing duration (Figure 3), evidently because most females were busy competing and did not dance at all. As the competition duration by necessity was the same for both females in a pair, competition duration was regressed on the average ornamentation duration for each female pair. Similarly, the average dancing duration of each female pair was regressed on competition duration to avoid pseudoreplication. This result also emerges from a multiple correlation (regression summary F2,21 = 9.61, p =.001) for the effects of competition and dancing duration on ornament display duration: ßcompetition = 0.544 (p =.01) and ßdance = 0.215 (p =.28). Clearly competition more accurately predicted ornamentation than did dancing, and, moreover, this predominantly competition-induced ornamentation significantly predicted male mate choice the next day.
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The more intensely females engaged in competition on day one, the less likely they were to display the ornament on day two (Figure 4). Pseudoreplication is compensated for by using average ornament display duration within each pair on day two. Interestingly, this correlation is driven by the chosen females: when analyzed separately, competition duration on day one for chosen females correlated significantly with ornament display day two (Rs = -.432, n = 24, p =.035), but not so for rejected females (Rs = -.302, n = 24, p =.15).
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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When female-female competition was allowed, females displayed the ornament to one another more persistently than they did to the male. The female displaying most intensely is likely to be the dominant one within a pair. Clearly, a more intense ornament display (or other information from watching competitive interactions) made this female attractive to the male, as males used this information on the following day when females no longer were allowed to compete: The male spent most time before the female that had displayed for longer in the inter-female competitive situation. Indeed, this past information of ornament or competitive displays completely overrode more recently acquired information, and significantly influenced male mate choice. Furthermore, ornament display under competition did not correlate significantly with ornament display in the absence of competition. Consequently, on the day of the male's choice, ornament display contained little or no information regarding female dominance. Thus, male pipefish seem to remember and make use of information regarding partner dominance, presumably according to the reliability of that information. An alternative explanation is that males are conservative and stick to a decision once made. However, `conservatism' as a reason to why males should ignore recent display information and instead prefer older information seems unlikely. Moreover, in nature these fish do not form pair bonds or exhibit territoriality (Vincent et al., 1994
),
further making the "conservatism" explanation unlikely. Note that
the effect of mating competition on the choosing sex is not merely one of
constraining the options for choice (indirect mate choice, see
Wiley and Poston, 1996) but
active mate choice.
We ran a mirror-image experiment in 1996, with females separated the first
day and competing the second (Berglund and
Rosenqvist, 2001). Another difference from the experiment reported
here was that males had full access to females on the second day, such that
copulations were possible and occurred (this could not be allowed in the
present experiment, as males would then get pregnant and lose interest in
females the second day). In the mirror-image experiment, with females
separated during the first day, ornament display day one significantly
predicted ornament display on the second day, when female-female interactions
were allowed. Ornament display on either day also significantly predicted male
mate choice. This makes a possible alternative explanation to our results
unlikely, namely the explanation that time itself, rather than the absence of
female-female competition on day two, caused the results. Both males and
females chose and behaved similarly on both days in the mirror-image
experiment, so time effects, such as experience with the experimental set-up,
are unlikely to have confounded the results presented here. Thus, when females
were separated on the first day, their ornament display was the same on the
second day with competition, but when competition preceded separation this was
no longer true. Does intense competition make females less able, or less
willing, to subsequently display their attractiveness? The finding that
females competing more intensely on day one displayed their ornaments to a
lesser extent on day two (Figure
4) may suggest that intense competition is tiring or otherwise
discourages females from performing the display on the following day. Indeed,
long-term reproductive inhibition has been demonstrated in this species
before: Larger, and presumably dominant, females may decrease reproductive
activity in smaller females (Berglund,
1991). Alternatively, a female having proven her potential during
female-female encounters may not need to display her attractiveness further,
as males will rank such information more highly than pure displays of
attraction. Presently, we cannot tell whether females become dispirited or
arrogant after an episode of intense competition, but the finding that only
chosen, not rejected, females refrained from displaying their attractiveness
on day two suggests arrogance.
Thus, ornament display under female-female competition may be a more reliable and important signal than intersexual ornament display. Males mating with dominant females may gain direct benefits for themselves in terms of reduced risk during courtship, as well as possible direct and/or genetic benefits for their offspring from mating with high quality females. Therefore, male pipefish prefer beautifully ornamented females, but, above all, victorious ones.
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ACKNOWLEDGEMENTS |
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The work was funded by the Swedish Natural Research Council (grant to A.B.) and by the Norwegian Research Council (grant to G.R.). We thank Klubban Biological Station and Kristineberg Marine Research Station for research facilities. Thanks to Arnt Narve Bordal, Maria Sandvik, and Hanna Schiöler-Wasslavik for field assistance and video analysis, and to Ingrid Ahnesjö, Ian Fleming, Elisabet Forsgren, Maria Sandvik, and Staffan Ulfstrand for valuable comments on an earlier draft.
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