Behavioral Ecology Vol. 10 No. 2: 149-154
© 1999 International Society for Behavioral Ecology
Female preference for preferred males is reversed under low oxygen conditions in the common goby (Pomatoschistus microps)
School of Biological Sciences, University of East Anglia, Norwich, NR4 7TJ, UK
Address correspondence to J. D. Reynolds. E-mail: Reynolds{at}uea.ac.uk
Received 6 January 1998; revised 29 June 1998; accepted 19 July 1998.
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ABSTRACT |
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Female preference for males that already have eggs in their nest has been reported in many fish species. The presence of eggs may provide a cue for copying the choice of previous females and may indicate that high-quality care will be available. Consistent with a review of 13 studies, we found that female common gobies (Pomatoschistus microps) preferred to spawn with males that had already been chosen by females and whose nests therefore already contained eggs. However, this preference was reversed under conditions of low dissolved oxygen. We would not expect this reversal if the second female were using eggs as a signal of male genetic attractiveness to other females unless the benefits were outweighed by direct selection. The reversal also could not be explained by differences in active courtship by males, as courtship rates did not differ under low oxygen between males with or without eggs. Low oxygen conditions corresponded with a nearly threefold increase in male ventilation of eggs and a reduction in time spent near a selecting female. The reversal is therefore most likely due to females avoiding males that would be unable to meet the demands of care of a second clutch under low oxygen conditions. Thus, an abiotic feature of the environment reveals plasticity of female choice, consistent with hypothesized changes in benefits of mating with preferred males.
Key words: common gobies, female choice, fish spawning, mate copying, oxygenation, Pomatoschistus microps.
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONACKNOWLEDGEMENTSREFERENCES |
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Animals are expected to choose mates according to characteristics that will enhance the fitness of their offspring while minimizing the costs paid for assessment and mating (Andersson, 1994
; Gibson and Langen,
1996; Johnstone,
1995; Reynolds,
1996). These choices may be based on physical and behavioral
traits of members of the opposite sex as well as resources defended. If such
traits reflect mate quality, choosy individuals may receive genetic benefits
for offspring growth or survival (e.g.,
Petrie, 1994;
Reynolds and Gross, 1992).
Depending on the breeding system, direct benefits for offspring such as safe
nest sites, good territorial resources, and highquality parental care could
also be obtained (Alatalo et al.,
1984; Bisazza and Marconato,
1988; Sargent,
1982).
Animals may learn about the quality of potential mates by copying choices
made by others (Gibson and
Höglund, 1992;
Pruett-Jones, 1992).
Furthermore, the prospective mates themselves may differ in quality as a
result of previous matings—for example, by changing the level of care
they provide (Jamieson, 1995;
Rohwer, 1978). Thus, the
second female will see a male which now has a higher quality if he provides
more care as a result of his prior mating success. We can therefore expect
animals to be sensitive to previous mating status of members of the opposite
sex.
In fishes, there are numerous examples of females preferring males that are
already caring for eggs in their nests
(Table 1). Some experiments
have manipulated matings to make males seem "preferred," while
others have allowed the first female a free choice. There is still uncertainty
and controversy as to the benefits received by females when mating with males
that already have eggs in their nests
(Gibson and
Höglund, 1992;
Goldschmidt et al., 1993;
Jamieson and Colgan, 1989;
Kraak, 1996;
Petersen, 1995;
Pruett-Jones, 1992). Several
hypotheses have been proposed. First, if the first female had made a free
choice, the second female's assessment may actually be independent of the male
having been chosen previously (e.g.,
DeMartini, 1987;
Lindström
and Kangas, 1996). These females may simply "agree"
about the same male traits being attractive. Second, egg presence may signal
that the male was attractive to other females. By copying choices of other
females, a female may improve her mate choice if assessment is prone to error
(Gibson and
Höglund, 1992;
Losey et al., 1986). Third,
the female can reduce time, energy, or predation risk associated with making
her own assessment (Dugatkin and
Höglund, 1995;
Gibson and
Höglund, 1992;
Losey et al., 1986;
Pruett-Jones, 1992). Fourth,
egg presence may indicate that males have been successful in caring for broods
(Ridley, 1978;
Sargent, 1988). Fifth, the
higher value to males of large numbers of eggs may increase the males'
parental input (Coleman et al.,
1985; Sargent,
1988). Finally, the risk of predation or cannibalism by the
guarding male may be reduced by the presence of other eggs
(Rohwer, 1978).
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A separate body of literature has shown that mate choice may change
according to environmental conditions. For example, in the sand goby
(Pomatoschistus minutus), females became less selective in the
presence of a predator (Forsgren,
1992), as did male pipefish (Syngnathus typhle), a
sex-role—reversed species (Berglund,
1993). Similarly, female three-spined sticklebacks
(Gasterosteus aculeatus) became less selective as the energetic costs
of mate assessment increased (Milinski and
Bakker, 1992), and female Trinidadian guppies (Poecilia
reticulata) switched to smaller males under high light conditions, when
these males courted more than larger ones
(Reynolds, 1993).
Here we present the first study to combine questions about previous mating
status of males and flexibility in female choice according to abiotic
conditions. In the common goby (Pomatoschistus microps), males may
care for eggs from more than one female simultaneously. Males ventilate
("fan") the eggs to provide oxygenation and defend their eggs from
predators for 7-12 days until they hatch. Fanning of the eggs is a
nonshareable resource because eggs compete for oxygen
(Coleman and Fischer, 1991;
Torricelli et al., 1985). Male
gobies increase their fanning activity under conditions of low dissolved
oxygen (Jones and Reynolds,
1999a). Such conditions are widespread in estuaries and bays
typical of the habitat of gobies (Diaz and
Rosenberg, 1995) and can occur naturally or as a result of organic
pollution (Breitburg, 1992;
Diaz and Rosenberg, 1995;
Jones JC and Reynolds JD, personal observations). Manipulation of oxygen
therefore provides a convenient tool for understanding flexibility of mate
choice, and, conversely, an understanding of mating behavior may be useful for
understanding sublethal impacts of pollutants
(Jones and Reynolds,
1997).
If females prefer to spawn with the same males chosen by a previous female
for any of the reasons listed above, then under conditions of low dissolved
oxygen we may predict a change in this preference for three possible reasons.
First, the added oxygen demand of a second clutch may exceed the additional
egg ventilation that males are able to provide for their brood. For example,
although a previous study with common gobies found that males compensated for
low oxygen by increasing fanning rates, there was a plateau in fanning over
time, suggesting a possible limit to compensation in low oxygen
(Jones and Reynolds, 1999a).
There were no differences among oxygen treatments in egg cannibalism by the
attending male. If egg survival is reduced by the extra demands of multiple
clutches under low oxygen, then a second female would benefit by avoiding
nests where the male is already providing a large amount of care.
Alternatively, once a male begins caring for eggs, it may not be able to court
new females due to the extra time required for providing extensive parental
care under low oxygen. Indeed, the male may be unwilling to accept additional
clutches if these jeopardize the survival of his eggs. Females may therefore
be selected to search for more receptive partners. Finally, under oxygen
stress parental care is more costly to males, as shown by greater weight loss
(Jones and Reynolds, 1999a).
Therefore, males that are providing costly care of eggs may be in poorer
condition and hence may be more likely to consume their eggs
(Smith and Reay, 1991; cf.
Lindström,
1998) or may be less effective in providing care
(Unger and Sargent, 1988).
The aims of this study were first to test for a preference in common goby females for males that already have eggs in their nests, and second to test for a reversal of this preference under low dissolved oxygen. The results are interpreted in light of general hypotheses for mate choice copying and plasticity.
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METHODS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONACKNOWLEDGEMENTSREFERENCES |
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We studied common gobies from a near-shore site at Canvey Island, in the Thames estuary, Essex, UK, in August 1995 and June 1996. In this region there are periods of low oxygen conditions in the range of 40-50%, with occasional episodes lasting several weeks at 20-30% dissolved oxygen during the summer season when the fish are breeding (Oatley R, personal communication, based on U.K. Environment Agency internal reports on water quality).
The fish were caught with a push-net and brought to an aquarium facility
using natural seawater (34
salinity). They were kept in storage tanks,
separated by sex, and fed a diet of chopped mussels (Mytilus edulis),
frozen artemia, and frozen mysid shrimp ad libitum once a day. Trials were
carried out in glass aquaria (1.2 m x 0.6 m x 0.4 m high), divided
into independently sealed compartments using white inert plastic barriers. All
compartments had a sand substrate of 4 cm depth. Aquaria were split so that in
one half of each tank the compartments were used as low oxygen replicates, and
in the other half they were used as control replicates. Treatment sides were
selected randomly and water quality was maintained by partial exchange of
water twice weekly after the first week. During the experiments males were fed
finely chopped mussels ad libitum daily and excess food was removed every
second day. The light regime was 16 h light : 8 h dark.
Reduction and maintenance of low oxygen conditions
We assigned males to either a low oxygen treatment (35% dissolved oxygen)
or a control treatment (fully saturated water). The level of 35% was selected
because it is encountered by gobies in the wild (see above and
Breitburg, 1992). Indeed,
considerably lower levels of oxygen occur in many coastal areas of Europe and
Scandinavia (Diaz and Rosenberg,
1995). The moderate level used was low enough to influence fanning
activity without causing distress to the fish
(Breitburg, 1992;
Jones and Reynolds, 1999a;
Petersen and Petersen, 1990).
Nitrogen gas was bubbled into the water gradually over a period of 6 h to
achieve the low oxygen condition, and oxygen content was monitored regularly
and maintained (range 30-40%) by bubbling in additional nitrogen or air. Tanks
were sealed with plastic lids to limit oxygen fluctuation, and equal
disturbance was given to both treatments. This work was carried out under a
U.K. Home Office license for animal care.
Experiment 1: test for reversal of preference under low oxygen
In early August 1995 pairs of males matched for length (to the nearest mm)
and wet weight (g) were assigned randomly to one of the two experimental
treatments in 137-1 compartments of glass aquaria. Each compartment was either
a control or a low oxygen replicate. At first, compartments were divided in
half by a removable plastic barrier, which separated pairs of males, allowing
each male time to acclimate. A compartment was separated from the male areas
by mesh screens across the front of the tank, for later placement of a female
(Figure 1). Each male of a pair
was allocated randomly to the left or right male compartment. Pairs of
compartments had the same oxygen level but would differ in the presence of
eggs in the nests of males.
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Males were left for 24 h before we reduced the oxygen concentration in the low oxygen group. A few hours after reduction of the oxygen content was underway, all males were provided with a nest (one half of a 6-cm diam clay flower pot) and left for another 24 h. Fecund females were measured and allocated randomly to the appropriate oxygen treatment in separate nonexperimental tanks 12 h before the experiment began. Then we placed a female, restrained under a mesh cage, into her compartment across the front of the tank (see Figure 1) and removed the two mesh screens restraining the males. After 1 h, the plastic barrier separating the males was removed and the female was released from the cage and allowed to spawn with the male of her choice. Male—male competitive interactions were minimized by this design because during the assessment period the female's cage blocked much of the gap between the males (mean interactions/h = 3, range = 0-10). If no spawning occurred within 24 h, we repeated the procedure once more with a new female. Females were removed after spawning. Thus, pairs of males were established in each oxygen condition in which one male had been chosen by a female and had eggs in his care, and the other did not.
The males were left until day 4 of parental care (the day of spawning was called day 0), which was just less than halfway through the parental cycle. Then we introduced a second fecund female, restrained under a mesh cage, into the choice arena at the same location as the first female and left her for 1 h before being released. This time the female had a choice between a male that had been chosen by a previous female and therefore had eggs in his nest and a male that had not been chosen and therefore lacked eggs. The replicate was observed continuously for 1 h and any new spawning activity was recorded for up to 24 h after female introduction. If no spawning took place within this time, the procedure was repeated once more with a new female.
We ran 20 replicates, and both females spawned in 12 of these (6 control oxygen, 6 low oxygen), yielding a total of 24 spawnings. The mean (±SD) daily water temperature was 14.9°C (±0.58). The mean (±SD) total body length of males and females were 47.8 ± 2.32 mm and 50.5 ± 2.60 mm, respectively. There were no size differences among males that participated in spawnings in the oxygen or eggs/no eggs treatments (two-way ANOVAs: oxygen F1,20 = 0.025, p =.875; presence of eggs F1,20 = 0.019, p =.892, interaction F1,20 = 0.092, p =.765). Similarly, there were no size differences among females that spawned according to oxygen treatment or their order of spawning (first or second) (two-way ANOVAs: oxygen F1,20 = 0.315, p =.581; order of spawning F1,20 = 0.276, p =.605, interaction F1,20 = 3.038, p =.10).
Experiment 2: test for male behavioral trade-offs
In June 1996 we investigated whether oxygen treatment influenced the time a
male spent fanning his eggs or courting a new female. The experimental design
was the same as for experiment 1, but this time we did not allow the second
female to spawn and focused instead on male behavior, which we recorded for a
20-min period 30 min after the second female was restrained under a cage in
front of the males' compartments. This experiment yielded the following data
for 16 replicates for each of the four treatments: time spent fanning in the
nest, time spent beside the female, and courtship toward the female. Courtship
included: (1) approach to the female, (2) courtship fanning, which occurs in
or near the nest but is not associated with egg ventilation, (3) male display
posture (i.e., pushing up on pelvic disc and erecting fins), (4) small, jerky
movements near to the female, and (5) attempts to lead the female to the nest.
A courtship index was used as in Forsgren et al.
(1996) and Jones and Reynolds
(1999b), whereby each bout of
courtship fanning, jerking movement, approach to female, and male display
scored 1, but each leading display, the most prominent courtship activity,
scored 2. Seven replicates (male pairs) were excluded from analyses; two due
to lack of spawning and five (two control and three low oxygen) because the
male had eaten his entire clutch of eggs.
The mean (±SD) daily water temperature was 16.9°C (±0.4). The mean (±SD) total body lengths of males (n = 50) and females (n = 50) that participated in courtship were 46.0 ± 2.3 mm and 47.4 ± 2.8 mm, respectively, and neither length differed among treatments (two-way ANOVA, males: oxygen F1,46 = 0.279, p =.599, egg presence F1,46 = 0.097, p =.756, interaction F1,46 = 0.032, p =.858; females: oxygen F1,46 = 0.052, p =.820, egg presence F1,46 = 0.503, p =.480, interaction F1,46 = 0.004, p =.952).
Statistical analyses
The test for reversal of female choice is one-tailed, on the basis of
predictions in the Introduction. The rest of the statistical tests are
two-tailed, and statistical significance was accepted at p <.05.
We performed parametric tests when data met the standard assumptions. Male
behavior was compared among all groups using nonparametric Kruskal-Wallis
tests. To determine where differences between groups lay, we used a
nonparametric multiple comparisons test for nonequal groups with tied ranks
(Zar, 1996).
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RESULTS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONACKNOWLEDGEMENTSREFERENCES |
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Experiment 1: test for reversal of preference under low oxygen
In the control treatment, five females spawned with the male that already had eggs under his care, and one spawned with the male without eggs. In the low oxygen treatment, the reverse occurred; one female spawned with the male with eggs, and five spawned with the male without eggs. Therefore, as predicted, female preference for males with eggs in their nests was reversed under conditions of low oxygen (one-tailed Fisher's Exact p =.04).
Experiment 2: test for male behavioral trade-offs
The oxygen treatments and presence or absence of eggs had strong effects on
the time males spent fanning in the presence of a second female
(Figure 2a; Kruskal-Wallis
H = 37.59, n = 50, p <.001). Nonparametric
multiple comparisons tests revealed that low-oxygen males with eggs spent more
time fanning than males in the other three treatments (Dunn Q values
4.3-9.9, all p <.05). Males with eggs in the control treatment
also spent more time fanning than control males lacking eggs (Q =
5.22, p <.001) or than low-oxygen males lacking eggs (Q =
5.41, p <.001).
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The large amount of time spent fanning by low-oxygen males caring for eggs corresponded with a small percentage of time spent near females (Figure 2b). This was significantly lower than for the other treatments (Dunn Q values 3.6-7.0, all p <.05). We also found that low-oxygen males without eggs spent more time near the female than control males without eggs (Q = 3.24, p <.01). The overall effects of oxygen treatment and presence of eggs shown in Figure 2 is highly significant (Kruskal-Wallis H = 12.05, n = 50, p =.007).
There was a trend toward oxygen treatment and presence of eggs affecting male courtship intensity (Figure 2c; Kruskal-Wallis H = 6.71, n = 50, p =.08). The data suggest that this trend was caused by oxygen level rather than egg presence (Figure 2c). There was no effect of oxygen treatment or egg presence on male weight loss over the 4 days of parental care (ANOVA, oxygen effect: F1,46 = 0.08, p =.78; egg effect F1,46 = 1.26, p =.27; oxygenxegg interaction: F1,46 = 0.02, p =.89).
There was no difference among oxygen treatments in egg cannibalism by parental males (comparison of slopes of regressions between initial and final egg numbers; t2,23 = 1.694, p >.1).
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONACKNOWLEDGEMENTSREFERENCES |
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This study shows that under saturated oxygen conditions, female common gobies preferred to spawn with males that had already been chosen by females and whose nests therefore contained eggs. This preference was reversed under low dissolved oxygen conditions. Males in the low oxygen treatment that had eggs in their nests exhibited significantly higher levels of fanning activity, and correspondingly reduced the time they spent close to the female, though they courted with the same intensity as low-oxygen males that lacked eggs.
Why was female mate preference reversed under low oxygen conditions? Three
possible reasons can be considered in conjunction with general issues about
why females should prefer to mate with males that already have eggs. First,
males with eggs under low oxygen conditions may have been unable to spend time
attracting new spawnings due to the increased requirements of their current
brood or due to costs of lengthened periods of brood care
(Jamieson and Colgan, 1989;
Kvarnemo, 1996;
Van Iersel, 1953). Although
males that had eggs under low oxygen spent less time near the female
(Figure 2b), their courtship
intensity was similar to males that lacked eggs
(Figure 2c). Therefore, low
oxygen suppresses courtship regardless of presence or absence of eggs, and
although we cannot rule out a role for male behavior, courtship alone probably
cannot explain the switch in female preference.
Alternatively, females could avoid males with eggs under low oxygen if
higher fanning rates and greater weight loss over the full parental cycle
(Jones and Reynolds, 1999a)
increase the likelihood that males may recoup lost energy by cannibalizing
eggs (Smith and Reay, 1991; cf
Lindström,
1998). We found no effect of egg presence on weight loss over the
first 4 days for low oxygen males, though this was only half of a parental
cycle, and males could disguise poor condition by retaining water
(FitzGerald et al., 1989;
Unger, 1983). Neither was an
increase in egg cannibalism observed for males breeding under low oxygen
conditions in a previous study (Jones and
Reynolds, 1999a), though abandonment of clutches occurred more
often.
Finally, a second clutch of eggs may require more ventilation than males
can provide. Competition for oxygen increases with clutch size
(Belles-Isles et al., 1990;
Reebs et al., 1984;
Rohwer, 1978), and this may be
particularly acute in low oxygen environments, where males of this species are
known to fan eggs at a higher rate (Jones
and Reynolds, 1999a). Other studies of fishes have shown females
reducing their preference when the number of eggs in the nest exceeds a
critical number (Belles-Isles et al.,
1990; Constantz,
1985; Goldschmidt et al.,
1993; Kraak and Videler,
1991). Thus nonshareable care in the form of nest ventilation puts
a ceiling on the benefits expected under the hypothesis that larger broods
will be more valuable to the male and hence should receive better care
(Coleman and Fischer, 1991;
Lindström
and Wennström, 1994;
Sargent, 1988).
The reversal in female choice for males with eggs under low oxygen
conditions offers some insight into the general benefits of female mate-choice
copying (Jamieson, 1995;
Losey et al., 1986;
Pruett-Jones, 1992). If
females in the control oxygen treatment had copied the choice of a previous
female to improve their choice of partner or to minimize the costs of mate
assessment, it is unlikely that this decision would change as such costs are
probably higher under oxygen stress (Fry,
1957; Kramer,
1987). Note that under control conditions the second female may
have copied the first female's choice or she may have chosen the same male
based on a trait other than eggs, as the first female had free choice (see
also DeMartini, 1987;
Hoelzer, 1990;
Lindström
and Kangas, 1996). If a trait signaling genetic benefits through
attractiveness or viability of offspring had been involved, the second female
should not have reversed her choice unless the benefits of such a decision
were outweighed by other factors such as oxygen limitation for the eggs.
In conclusion, female preference for males that had already been chosen by other females and therefore had eggs in their nests was reversed under conditions of low dissolved oxygen. This reversal against "preferred" males shows plasticity of female choice according to abiotic conditions, which is consistent with hypothesized changes in benefits of care provided by males.
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ACKNOWLEDGEMENTS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONACKNOWLEDGEMENTSREFERENCES |
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We thank Bruce Burgoyne, Paul Cooke, Bob Turner, and Neville Burt for their technical support during this research. We also thank Isabelle Côté and Don Kramer for advice, Ian Jamieson for comments on the manuscript, and Robert Poulin and Colin Townsend for their hospitality at the University of Otago where this paper was written. Funding for this research was provided by the School of Biological Sciences of the University of East Anglia and Centre for Environment, Fisheries and Aquaculture Science (Lowestoft). A research grant from the Fisheries Society of the British Isles also contributed toward this study.
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