Behavioral Ecology Vol. 12 No. 1: 84-92
© 2001 International Society for Behavioral Ecology
The effect of partial brood loss on male desertion in a cichlid fish: an experimental test
a Smithsonian Tropical Research Institute, Unit 0948, APO AA 34002 0948, USA b Department of Statistical Sciences, University of Cape Town, Rondebosch 7701, Cape Town, South Africa
Address correspondence to M. D. Jennions, who is now at Division of Botany and Zoology, Australian National University, Canberra, ACT 0200, Australia. E-mail: jennionm{at}naos.si.edu .
Received 9 January 2000; revised 14 May 2000; accepted 25 June 2000.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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There is little experimental evidence testing whether current brood size and past brood mortality influence mate desertion. In the cichlid Aequidens coeruleopunctatus both parents initially defend offspring. In a field study, all experimental broods, irrespective of initial brood size (222.9 ± 60.4, mean ± SD), were manipulated to a size of 100 fry. Neither the duration nor investment of females in parental care differed between control and brood reduced pairs, even though care seemed costly. On average, females lost 5.1 ± 4.8% of initial weight while guarding a brood until independence. In contrast, males with experimentally reduced broods guarded fry for significantly fewer days before deserting their mate than did males from control pairs with natural-sized broods (20.5 ± 7.5 vs. 14.2 ± 6.2 days). In at least 20% of cases (n = 9/45), the deserting male immediately mated with another female. Males with experimentally reduced broods also spent less time guarding fry before deserting and attacked fewer brood predators than did males with control broods. For broods manipulated to have 100 fry, there was a significant negative relationship between the days until male desertion and the proportion of the initial brood removed. This indicates that male assessment of the future success of the current brood (hence its reproductive value) is based on past mortality and/or that there is variation among males in the expected size of future broods. Both current brood size and brood size relative to initial brood size are therefore predictors of male, but not female, parental behavior and mate desertion. Female care may be unaffected by brood reduction due to limited breeding opportunities and partial compensation for reduced male care.
Key words: brood reduction, brood size, cichlids, mate desertion, parental care, life-history trade-off, mating opportunities.
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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Optimal life-history strategies are based on the trade-off between investment in current and future reproduction (Roff, 1992
). Investment in
the current brood in the form of parental care is beneficial because it
increases off-spring reproductive value
(Clutton-Brock, 1991). Even
so, in species with biparental care where a single parent is also capable of
rearing a brood to independence, albeit with reduced success, mate desertion
often occurs (e.g., insects: Eggert and
Müller, 1997;
Robertson and Roitberg, 1998;
birds: Beissinger and Snyder,
1987; Fujioka,
1989; Hemborg,
1999; Mock and Parker,
1986; Valera et al.,
1997; mammals: Kleiman,
1977). The timing of desertion reflects the trade-off between the
costs and benefits of continuing to care for the current brood versus those
derived from deserting (Grafen and Sibly,
1978; Lazarus,
1990; Maynard Smith,
1977). For example, desertion is more likely when the success of
single-parent care is higher (Beissinger,
1986); offspring are older
(Sargent and Gross, 1986;
Wisenden, 1994); a parent's
future fecundity is higher if it deserts rather than continues to care
(Balshine-Earn, 1995); current
brood size is lower than average (Lazarus,
1990); re-mating opportunities increase
(Balshine-Earn and Earn, 1997);
and future conditions are, on average, more favorable for breeding
(Carlisle, 1982;
Pöysä
et al., 1997). The influence of these factors may, however, vary
among breeding pairs due to differences in intrinsic condition, parental
ability, fecundity, and attractiveness (e.g.,
Erikstad et al., 1997;
Galvani and Coleman, 1998;
Hõrak et
al., 1999; Robertson and
Roitberg, 1998).
Despite a long history of theoretical work on mate desertion following
Maynard Smith's initial use of game theory
(Maynard Smith, 1977; see
reviews by Kokko, 1999;
Webb et al., 1999), few field
experiments have manipulated variables that increase the likelihood of mate
desertion (Eadie and Lyon,
1998;
Székely et
al., 1996). Most examples come from work on birds and involve the
manipulation of brood size (e.g., Armstrong
and Robertson, 1988;
Beissinger, 1990;
Winkler, 1991), offspring
quality (Erikstad et al.,
1997), perceived paternity (see review by
Westneat and Sherman, 1993) or
attractiveness (Johnsen et al.,
1997). In insects, there have also been attempts to manipulate the
opportunity for remating (Robertson and
Roitberg, 1998) and food availability
(Scott and Gladstein, 1993;
Trumbo, 1991). In a few fish,
reducing brood size sometimes leads to total brood cannibalism, which is
equivalent to brood desertion (see reviews by
Okuda and Yanagisawa, 1996;
Sargent, 1997), but otherwise
there is simply a decline in the intensity of parental care (e.g.,
Ridgway, 1989).
Cichlid fish are an ideal group for the experimental study of mate
desertion (2000+ species). There have been a minimum of 21 evolutionary
transitions from biparental to female-only care, and a maximum of 10 in the
reverse direction (Goodwin et al.,
1998); male-only care occurs in only two species
(Balshine-Earn and McAndrew,
1995). Moreover, sporadic male desertion has been confirmed in
eight species of cichlid fish with biparental care (see review by
Balshine-Earn and Earn, 1998).
Determining which factors promote desertion in biparental species with
occasional desertion and female-only care may help explain the evolution of
obligate male desertion, which accounts for at least 68% (21/31 transitions)
of the interspecific variation in patterns of sex-based care. Although a few
laboratory experiments have looked at the effect of remating opportunities
(Keenleyside, 1983,
1985;
Rogers, 1987) and male size
(Balshine-Earn and Earn, 1998)
on mate desertion, there is no experimental evidence that reduced brood size
promotes mate desertion. The best data come from field observations that
convict cichlid broods guarded by females are smaller than those guarded by
both parents (Wisenden, 1994).
Unfortunately, the direction of causation is unknown. Brood size may have been
smaller because males deserted and broods with female-only care suffered
greater predation, or because males more often deserted smaller broods. More
important, these observational data cannot determine whether current brood
size and variation in past brood mortality both affect male desertion.
In the present study we experimentally reduced brood size in the Panamanian
acara, Aequidens coeruleopunctatus. Both biparental and female-only
care have been reported, and male desertion seems to be fairly common
(Barlow, 1974;
Carlisle, 1981;
Townshend, 1984). We asked
three main questions:
- Do males desert smaller broods sooner? Marginal-value theory predicts that
whenever parents have the potential to breed in the future, they will desert
when the instantaneous rate of return from staying is equal to that from
deserting (Grafen and Sibly,
1978). The benefit curve is lower, and hence the rate of return
from caring smaller, for reduced broods. Limited observational and
experimental studies of birds indicate that smaller broods are more often
deserted (Beissinger,
1990).
- Does the past success of the brood influence the timing of mate desertion?
Carlisle (1982) argued that
past mortality sometimes predicts future mortality for the current brood. If
true, then even when current brood size is identical, the reproductive value
of a brood is smaller if it has suffered higher previous mortality. This has
only been confirmed in a single empirical study
(Pöysä
et al., 1997). Alternatively, adults may vary in their future
reproductive potential (repeatable fecundity). The value of a brood of a given
size is lower for a parent with high fecundity relative to that of a parent
with low fecundity because of the former's greater future reproductive
prospects. Because more fecund parents suffer proportionately greater loss
when current brood size is equalized across pairs, the degree of past brood
reduction should predict the value of the current brood
(Galvani and Coleman,
1998).
- Does a reduction in brood size affect male and female parental investment
equally? Reduced benefits from guarding a smaller brood should decrease
parental investment (Clutton-Brock,
1991; Sargent and Gross,
1986,
1993). Indeed, experimentally
reducing brood size in fish providing uniparental care usually results in
lower parental investment (e.g., Carlisle,
1985; Coleman et al.,
1985; Lavery and Keenleyside,
1990;
Lindström
and Sargent, 1997; Mrowka,
1987; Sargent,
1981,
1988;
Ridgway, 1989). Before mate
desertion, brood reduction should have a similar effect on the value of the
current brood to both parents, but the alternatives available to each sex may
differ. For example, if initiating another breeding attempt is easier for
males than for females, then males may engage in extrapair courtship while
seeking a new mate. Females could then be forced to compensate for the
associated reduction in male care to ensure brood survival
(Westneat and Sargent, 1996).
Depending on the exact costs and benefits of single and biparental care,
females may even increase investment in smaller broods in anticipation of
future desertion by their mate. Even after desertion, the sex with the lower
potential reproductive rate may continue to invest heavily in the current
brood (Lazarus, 1990;
Székely et
al., 1999; Yamamura and Tsuji,
1993). Thus, although both parents probably place less value on a
smaller brood, female investment in smaller broods may increase because of
their limited rebreeding opportunities and compensatory parental behavior.
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METHODS |
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Study species and site
We conducted our experiment on Aequidens coeruleopunctatus at Rio Parti, Republic of Panama (9° S, 78°30' W) from January to April 1999. Breeding is mainly confined to the dry season (January-April). In the study area the river was 3-10 m wide and most pools had a maximum depth less than 1 m. Rio Parti drains a mainly deforested area used for cattle ranching for over 15 years (Townshend, 1984
). Females lay eggs on a dead leaf
(Barlow, 1974), and after eggs
hatch both parents orally transfer the yolk-sacked embryos
("wrigglers") to a previously excavated pit. In 3-5 days the yolk
is absorbed, and the 5-6 mm long young school as free-swimming fry. The
parents then guard the fry for another 3-5 weeks. Larger cichlid fry are less
vulnerable to predation and the benefits of parental care decrease with brood
age (Jennions MD, unpublished data;
Wisenden and Keenleyside,
1992). Both parents guard fry and attack approaching fish.
Although both sexes are equally involved in disputes with neighboring pairs,
females stay closer to the fry and more often chase intruding fish (Jennions
et al., in preparation). At least nine genera of fish are potential brood
predators (Kramer and Bryant,
1995), and juvenile cichlids are the most threatening.
Experimental approach
We captured brood-guarding females at night using a submersible torch and
hand-held dip net. We recorded their standard length (±0.1 mm) and mass
(±0.1 g) and marked them with a subcutaneous injection of dilute
acrylic paint. We confirmed the sex of marked parents based on body size,
coloration, and subsequent behavior. Once the parents had moved the embryos to
an excavated pit, they became available for the experiment. A pilot study
showed that brood predators are strongly attracted to sediment disturbance
during the day. We therefore carried out brood manipulations at night. The
yolk-sacked embryos were siphoned into tubing and transferred to a plastic
tray. We then counted out 100 fry and returned them to the pit by pouring them
back down a 2 cm wide plastic tube. Initial brood size was 222.9 ± 60.4
wrigglers (n = 36). In 35 of 36 cases initial brood size was > 100
and fry were removed. In one case it was less than 100 and fry were added. If
we refer to the manipulated pairs as "reduced," we have only used
the 35 pairs where brood size was reduced in the analysis. In control broods
the fry were sucked into the tubing and then released straight back into the
pit. We assigned approximately every fourth brood to the manipulation
treatment, with the caveat that, with one exception, every pool in the stream
contained broods subject to both treatments. There were no significant
differences between control and reduction brood treatment females in standard
length (t = 0.396, p = 0.69; mean ± SD, reduction:
63.1 ± 5.2 mm, n = 35; control: 63.6 ± 6.8 mm,
n = 111), body condition (ANCOVA: F1,131 = 0.20,
p =.654), or breeding date (t = 0.759, p =.45;
reduction: 61 ± 29; control: 57 ± 26; day 1 = January 1). The
power to detect a difference of medium strength (d = 0.5) was 72%
(Cohen, 1988).
Behavioral observations
We walked along the bank until we located a brood and then waited 5 min to
ensure that the parents were undisturbed by our presence. Using binoculars we
then recorded parental behavior for 15 min. The summary variables we report
are (1) the time spent within 4 body lengths (± 25 cm) of the brood,
excluding time away if the parent left to chase another fish and then returned
without feeding; (2) the number of bites at the substrate (feeding); (3) the
number of attacks directed at potential brood predators. We did not
distinguish between short, open-mouthed lunges and prolonged chases. Attacks
were clearly recognizable because the intruding fish reoriented and moved away
from the attacker. We made focal observations on each pair approximately every
6 days.
Timing of male desertion
We alternated 4 days at the study site with 1- or 2-day intervals of
absence. Each day we noted which marked females were guarding fry and whether
their mate was present. If the male was initially absent, we continued to
watch until he arrived or 15 minutes had elapsed. We defined the date of
desertion as the last day on which the male was absent for 15 min and
subsequently was not seen guarding the brood. We defined the timing of male
desertion as the number of days the male guarded free-swimming fry before this
date. Female desertion did not occur. Using this definition of desertion we
could not obtain data for all pairs. First, we were sometimes unable to
conduct censuses due to poor water visibility and could not accurately
determine the date of desertion. Second, if the pair disappeared
simultaneously, we could not distinguish desertion by both parents from brood
failure or fry independence.
Statistical analysis
For variables measured once per pair, we compared brood-reduced and control
pairs using two-sample t tests or G tests with Williams'
correction to compare frequencies. The timing of male desertion was first
compared using a two-sample t test. This analysis does not, however,
take into account pairs where both parents disappeared at the same time (our
strictest definition of desertion required that the male leave before the
female). We therefore also compared the number of days males guarded using
survival analysis (Systat,
1998). The number was treated as an "exact failure" if
the male deserted before the female. It was "right censored" if
the pair disappeared simultaneously or if we were unable to continue
monitoring the pair. We excluded from the analysis censored cases where
parents guarded for fewer than 5 days. These were almost certainly instances
of brood failure because the earliest confirmed case of male desertion was on
day 5. We also excluded two cases (one per treatment) where the male was never
seen guarding fry because he could have deserted before the manipulation.
(Inclusion of these cases did not change the results.)
The behavioral data involved repeated measurements from 129 pairs
(n = 471 samples). Both fry size and the number of samples varied
among pairs. We therefore analyzed the data using linear mixed-effects models
for unbalanced group data (Laird and Ware,
1982), formulated and executed in S-PLUS version 4.5
(Mathsoft, 1998) using the lme
algorithm (Pinheiro and Bates,
1999). This allowed us to treat pair identity as a random effect
nested within experimental treatment type. Treatment type is a fixed effect,
while fry size is a continuous variable that can be considered a surrogate
measure of time. Fry size should influence parental behavior because larger
fry are less vulnerable to predators. We used a restricted maximum-likelihood
approach (REML; Patterson and Thompson,
1971) because the response variables were sampled from a bounded
window of continuous time (i.e., fry size). REML is preferable to ordinary
maximum-likelihood procedures when estimation of variance components is
required from an unbalanced design (see review by
McCullagh and Nelder,
1991).
We built separate models for four response variables: the total number of times the male attacked brood predators; the time the male spent guarding fry; the total number of times the female attacked brood predators; and the number of times the female fed. For male variables we only used samples before male desertion. For females we carried out two sets of analyses. First, we only used samples before male desertion. Second, we included samples taken after male desertion because we were interested in the net effect of brood reduction on total female parental investment. To determine whether any difference in male attack rate between treatments was primarily due to males spending less time near the brood, we built models with and without male time with fry as a covariate.
The model with the smallest Akaike Information Criterion, AIC =
-2(log-likelihood) + 2(number of fitted parameters)
(Sakamoto et al., 1986), was
considered the most parsimonious. This approach often performs better than
restricting the final model to those variables with statistically significant
effects in the full model (Burnham et al.,
1995). Interaction terms were nonsignificant in the full model,
and examination of the AIC showed that interactions did not increase the fit
of our models. Thus, the final models presented exclude the interaction terms
between treatment and fry size or male time with fry. The significance of each
predictor variable in the final models was tested using the REML parameter
estimates to calculate t statistics. Finally, we used
likelihood-ratio tests to determine whether a model including the experimental
treatment effect provided a significantly better fit than the nested
alternative model that excluded it
(Kendall and Stuart, 1979). We
used maximum-likelihood procedures to obtain log-likelihood values for each
model and then tested for a significant difference in deviance (=
-2*Difference in log-likelihoods), which is approximately
2 distributed. If there was no difference in deviance, the AIC
indicates the most parsimonious model.
Repeated-measures analyses assume multivariate normality within each
repeated measure of any response variable
(Lindsey, 1993). Where
necessary we therefore transformed response variables to approximate
multivariate normality [log(x+1) and 
x]. We also
carried out diagnostic investigations to ensure linear model suitability.
Proportions were arcsine transformed. For power analysis we made the a priori
assumption of a medium strength effect (i.e., r =.30, d =
0.5) against a null hypothesis of no difference between treatments or
relationship between variables. The reported power is the probability of
detecting an effect of this magnitude when 
(two-tailed) = 0.05
(Cohen, 1988). When outliers
were identified and removed, their residuals are given in standard deviations
(Systat, 1998). Effect sizes
are calculated following Cooper and Hedges
(1994) and expressed as
Pearson's r. Unless otherwise stated, summary data are presented as
mean ± SD and tests are two tailed.
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RESULTS |
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Experimental brood reduction
During the manipulation we reduced brood size by 53.3 ± 12.8% (range 21.3-68.8%, n = 35). There was no significant difference in the frequency with which reduced and control broods failed before becoming free-swimming (G test with Williams correction, G = 0.026, p =.87; reduced: 20.0%; control: 21.3%, n = 35, 108; power
94%). Thus experimental brood reduction did not disrupt parenting and
lead to brood failure during the sedentary stage of caring. Brood size at the
egg/wriggler stage was only weakly related to female size (ANCOVA using data
from 2 years: size: F1, 55 = 2.70, p =.053,
one-tailed; year: F1,55 = 0.10, p =.76;
interaction: F1,55 = 1.47, p =.231; two outliers
removed, residuals 3.9 and 3.3 SD). There was no exponential increase or
decrease in fecundity with size (t test of log-log regression
coefficient, t57 = 0.89, p =.38; H0 =
ß = 1, power >90%).
Does brood reduction promote earlier brood desertion by males?
When the male deserted before the female, he guarded fry for significantly
fewer days in brood-reduced than control pairs (t = 3.016, df = 43,
p =.004; Figure 1).
The frequency at which the male deserted before the female was also greater
for brood-reduced pairs (G = 19.25, df = 1, p <.001;
reduced = 21/27, control = 24/81). To include data from pairs where both
parents disappeared simultaneously, we performed survival analyses. Males from
brood-reduced pairs spent fewer days guarding fry than males from control
pairs (stratified Kaplan-Meier estimation of mean survival time: reduced =
16.38 days, control = 27.03 days; Mantel-Haenszel test of treatment effect,
2 = 25.23, df = 1, p <.001;
Figure 2). Using only pairs
where males deserted before females there was no effect of female size on the
number of days males guarded fry (ANCOVA with female size as covariate: female
size: F1,42 = 0.096, p =.758; treatment:
F1,42 = 8.66, p =.005, power 37%), and there was
no interaction between female size and treatment (F1,41 =
0.15, p =. 70, power 36%). Survival analysis confirmed that female
size is not a significant covariate (stratified Cox Regression: t =
0.443, p =.66, n = 104).
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Does the change in brood size affect the timing of male
desertion?
We controlled for the effect of current brood size by only examining pairs
whose brood size was manipulated to 100 fry.
We then looked at the correlation between the number of days males guarded
fry until deserting and the proportion of the brood removed. For 21 pairs,
male desertion date was known exactly because the male deserted before the
female. In addition, we treated three pairs where the parents disappeared
together after 28 or more days of guarding as cases of male desertion. Twenty
eight days is a conservative measure of the time until brood independence (by
then mean fry length is >15 mm). Simultaneous disappearance of both parents
when fry are this size is almost certainly due to both parents deserting the
brood rather than brood failure. There was a significant relationship between
the number of days the male guarded fry and the proportion of the brood
removed (r = -.473, p =.012, one tailed, n = 23,
outlier removed, residual = 3.0 SD; Figure
3). In one experimental pair brood size was increased because the
premanipulation brood size was less than 100. This pair had a strong leverage
effect (leverage = 0.87; Systat,
1998), but even when we removed it from the analysis, the
relationship remained significant (r =.367, p =.047, one
tailed, n = 22). Finally, we performed a survival analysis in which
the number of days males guarded was treated as an exact failure if the male
deserted before the female and as right censored if the pair disappeared
simultaneously (see Methods). The change in brood size was a marginally
significant predictor of the duration of male care (Cox proportional hazards
estimation: t = 1.73, p =.045, one tailed, n = 27;
outlier removed).
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What happens to deserting males?
Of the 45 males who deserted before their mate, at least nine (20%) formed
a pair bond with another female before deserting. It was difficult to detect
pair formation by focal males because they were unmarked. In these nine cases,
we saw the male repeatedly engage in extrapair courtship and, more important,
move between his original mate and the new female while she selected a leaf
for egg laying. We infer that mating occurred because shortly after male
desertion a new brood appeared near the site where the second female was
courted. These nine males deserted after guarding fry for 18.7 ± 6.2
days (range = 11-27 days).
Does the effect of brood reduction on parental care before desertion
differ between the sexes?
The time males spent guarding fry decreased with increasing fry size for
both control and brood reduced pairs (Table
1). Controlling for fry size, males from brood-reduced pairs spent
significantly less time guarding than males from control pairs (p
=.002, n = 124 pairs; Tables
1 and
2). The number of attacks on
brood predators by males was also significantly lower for brood-reduced pairs
(p =.014, n = 118 pairs). Once male guarding time was
included in the model, however, there was no significant effect of brood
reduction on attack rate (Tables
1 and
2). Thus, the decrease in
attack rate is mainly due to brood-reduced males spending less time with fry
before deserting.
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There was no significant difference between treatments in the number of
attacks by females on brood predators or in female feeding rate. This was true
whether we only looked at samples before male desertion or at all available
samples (Tables 1 and
2). Female feeding rate
increased with fry size, but attack rate did not
(Table 1). Survival analysis
showed that the brood reduction treatment did not affect the number of days
females spent guarding fry (stratified Kaplan-Meier estimation of mean
survival time: reduced = 23.15 days, control = 23.74 days; Mantel-Haenszel
test, 2 = 0.83, df = 1, p =.36;
Figure 4). There was no
significant difference between treatments in the proportion of exact failure
and right censored pairs (G = 0.929, p =.34, reduced =
18/28, control = 60/81). At least 4.8% of females (8 of 168 marked) initiated
a second brood.
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The cost of female parental care
Females lost weight while defending broods. The interval between weighing
sessions was 19.9 ± 4.8 days (range = 15-32 days), and initial mass was
10.5 ± 2.9 g (n = 23). We estimated weight loss over 36 days
to represent the average time between egg laying and fry independence (8 days
as eggs and embryos and 28 as fry). The percentage reduction in mass relative
to initial mass was 5.1 ± 4.8% (range = gain 7.6% to lose 12.3%).
Twenty of 23 females lost weight (binomial test, p <.001). There
was a positive relationship between female size and percentage weight loss
(r =.496, p =.016, n = 23). Larger females lost
relatively more weight. Female weight loss is probably costly because it is
associated with reduced future fecundity in another cichlid
(Balshine-Earn, 1995).
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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We experimentally manipulated broods of Aequidens coeruleopunctatus that initially varied in size to a uniform 100 fry. This yielded three main findings. First, males deserted smaller broods sooner. Experimental brood reduction explained 17% of the variation in the number of days males guarded before deserting a female (effect size: r =.42). Second, the initial size of the brood influenced the timing of mate desertion. The percentage reduction in brood size was negatively related to the number of days males guarded fry before deserting (effect size: r =.32-.47). Third, the reduction in brood size affected male and female parental investment differently. Unlike males, brood reduction did not influence the number of days females guarded fry (effect size: r =.09). Brood reduction did not significantly alter female attack or feeding rates (effect size: r =.037-.096), while males spent significantly less time guarding fry and attacking brood predators before deserting (effect size: r =.23-.29).
Current brood size, past brood mortality, and variation in a male's
future prospects
Our finding that smaller brood size is associated with earlier male
desertion is in agreement with experimental studies of mate desertion in birds
(Beissinger, 1990), as well as
studies of brood desertion involving either a single (e.g.,
Eadie and Lyon, 1998) or both
parents (e.g., Winkler, 1991).
The simplest and most widely cited explanation for this result is that there
is a lower rate of return on investment in a smaller brood (brood size
hypothesis; Grafen and Sibly,
1978). There is, however, an additional possibility: a reduced
brood may be worth less because past mortality predicts the future mortality
of a brood (brood success hypothesis;
Carlisle, 1982). The degree of
partial brood loss could be a cue as to the proportion of the remaining brood
that will survive to independence. Only one study has directly distinguished
between these hypotheses
(Pöysä
et al., 1997). The main problem is that, given similar initial
brood sizes, brood size at the time of desertion and past brood mortality are
highly correlated, making it difficult to distinguish between the hypotheses
(e.g., Bessinger, 1990;
Winkler, 1991). In our study,
however, initial brood size varied considerably.
We found that the percentage reduction in brood size was negatively related
to the number of days male A. coeruleopunctatus guarded fry before
deserting. Our result is therefore consistent with the brood success
hypothesis. Armstrong and Robertson
(1988) presented a similar
finding for two species of waterfowl, but they reduced brood size to either
four or seven eggs and did not present separate analyses for each. In common
goldeneyes (Bucephala clangula) maternal effort is also modified
according to the past mortality of the brood, and past and future brood
mortality are positively correlated
(Pöysä
et al., 1997). In some fish, females use "test egg"
survival to assess male parental ability
(Kraak and van den Berghe,
1992). Similarly, partial brood loss in A.
coeruleopunctatus may act as a cue that males can use to assess a
female's parental abilities or the suitability of a breeding site. The extent
to which past brood mortality predicts future brood success in A.
coeruleopunctatus is currently unknown but is obviously a crucial
prediction of the brood success hypothesis.
To complicate matters, there is yet another explanation for the observed
relationship between the duration of male care and the change in brood size.
If males vary in a predictable manner in their future reproductive prospects,
the value of a current brood of any given size will vary among males (relative
value hypothesis; Galvani and Coleman,
1998; Montgomerie and
Weatherhead, 1988). The relative value of the current brood
depends on the expected size of future broods. For example, in a laboratory
study of convict cichlids (Cichlosoma nigrofasciatum), female size
and fecundity were closely correlated. When brood size was reduced to 100 fry,
larger females invested less in parental care
(Galvani and Coleman, 1998). A
brood of 100 fry is worth less to a large female because her next brood is
likely to be considerably larger. At sites where we can measure males, mating
in A. coeruleopunctatus is strongly size-assortative (r 
0.72; Jennions et al., in preparation). Male body size will therefore covary
with future reproductive prospects if female size is correlated with
fecundity. It is surprising that female size was only weakly related to
fecundity at Rio Parti. As such, male body size and future brood size are
unlikely to be closely correlated. This conclusion is strengthened by the
absence of any relationship for experimental pairs between the number of days
the male guarded fry and female size. The relative value of a given brood size
is therefore unlikely to be closely related to male size. The relative value
hypothesis may still apply, however, if other factors, such as among-male
variation in access to more fecund females assessed using cues other than body
size, results in repeatability of brood size among male A.
coeruleopunctatus.
In general, researchers need to more carefully distinguish between the
three hypotheses that account for a correlation between earlier desertion (or
any other decrease in parental investment) and current brood size. The brood
size hypothesis may offer an incomplete explanation. Experiments that follow
the design we used (see also
Pöysä
et al., 1997), rather than simply removing a fixed percentage of
each brood, provide one test of the brood success' hypothesis of Carlisle
(1982). Where possible, the
assumption that past and future brood mortality are correlated should be
directly tested. Finally, the comparative importance of predictable brood
mortality sensu Carlisle
(1982) and variation among
parents in expected future brood size (the repeatability of brood size) is
usually unknown. The lack of attention to these alternatives may reflect a
bias generated by the predominance of work on parental investment in birds.
Limited variation in and low repeatability of clutch size may be common in
many birds, but this is not true for most invertebrates and ectothermic
vertebrates. In these taxa facultative adjustments in parental investment
related to brood size occur, and all three hypotheses may apply in a single
species. Determining their relative importance is a future challenge.
Does a reduction in brood size affect male and female parental
investment equally?
Before desertion, brood reduction decreased male guarding time. This
decline was partly attributable to males temporarily leaving the brood to
engage in extrapair courtship. A similar decline in male parental care after
brood reduction occurs in several other fish
(Coleman et al., 1985;
Lavery and Keenleyside, 1990;
Ridgway, 1989; Sargent,
1981,
1988; but see
Lavery, 1995), but in none of
these species does brood reduction promote male desertion. A decrease in the
reproductive value of a brood will only lead to mate desertion if the
deserting sex thereby gains some benefit. In birds the potential benefits of
desertion include an earlier onset of moulting
(Ezaki, 1988), arriving sooner
to breeding grounds the next breeding season
(Urano, 1992), reduced
energetic costs of providing care
(Erikstad et al., 1997;
Hõrak et
al., 1999), and increased survivorship (but see
Székely
and Williams, 1995). The most likely benefit of desertion,
however, is the opportunity to remate in the same breeding season
(Beissinger and Snyder, 1987;
Mock and Parker, 1986;
Székely et
al., 1999; Tait,
1980). We showed that at least 20% of the 45 A.
coeruleopunctatus males that deserted their mate bred again almost
immediately. Unfortunately, we could not determine the exact time until
remating because males were unmarked. However, a recent study at another site
using marked males showed that a minimum of 50% of males that deserted remated
(Jennions MD, unpublished data).
In contrast, there was no significant effect of brood reduction on female
care, either before male desertion or over the entire sampling period. Reduced
female care after experimental brood reduction occurs in laboratory studies of
other cichlids (Galvani and Coleman,
1998; Lavery and Keenleyside,
1990; Mrowka,
1987), so why didn't female A. coeruleopunctatus decrease
investment in smaller broods? The energetic costs of female parental care may
be considerable. On average, females lost 5.1% of their initial weight during
one breeding bout. Weight loss has been reported in several species (e.g.,
Sabat, 1994), and probably
arises due to the trade-off between brood defense and foraging
(Rangeley and Godin, 1992) as
well as the energetic cost of chasing predators. Balshine-Earn
(1995) found that female St.
Peter's cichlids, Sarotheredon galilaeus, lose about 11.8% of body
mass during a breeding cycle, which significantly reduces their future
fecundity.
Female care may have remained unchanged despite brood reduction for two
reasons. First, females appear to have limited breeding opportunities. Only
4.8% of females were seen to initiate a second brood at Parti. This is
probably an under-estimate, but work at a second site where females were
permanently marked and frequently censused revealed that only 11.5% of females
(n = 113) initiated a second brood (Jennions et al., in preparation).
Caring for the current brood may therefore be the only option available to
most females. Second, females may have compensated for reduced male care by
increasing their own parental investment
(Coleman, 1993). Female
compensation may start before male desertion because males spend less time
guarding the fry before deserting. We found that naturally deserted females
attack predators significantly more often than paired females at Parti
(Jennions et al., in preparation). Female compensation may therefore
complicate our interpretation of the value of different-sized broods.
Observed female care may reflect a balance between decreased investment due
to lower brood value and greater investment to compensate for lower male
investment. To remove male effects, Carlisle
(1985) manipulated the brood
size of already deserted female A. coeruleopunctatus. The return time
of females who had been chased away from their brood depended on brood size.
This suggests that females do adjust their parental investment according to
brood size. Our own data show, however, that females rarely leave the brood
unattended. The average time with fry was 889 s of a 900-s observation period
(n = 309 females), and 62 of 62 deserted females spent 100% of each
15-min sample with the fry (Jennions et al., in preparation). The only time we
have seen females leave the brood unattended is in response to human
intervention. Even large predatory fish capable of killing adults (e.g.,
C. turjense and Hoplias sp.) are attacked. Female return
time is therefore an unnatural measure of parental investment.
Finally, even though males gain from desertion because they remate,
desertion probably comes at a cost. Female cichlids are usually less
successful at rearing a full brood to independence on their own
(Balshine-Earn, 1997;
Keenleyside and Bietz, 1981;
Nagoshi, 1987). In this
regard, it is interesting that we hastened male desertion at Rio Parti. In an
earlier study here, Townshend and Wootton
(1985) reported almost no
desertion in the cichlid Cichlasoma panamenses, but frequent male
desertion at a forested site. They attributed this site-based difference in
desertion to the higher density of brood predators at Parti (this density
difference still exists; Jennions MD, unpublished data). They argued that the
greater risk of brood predation at Parti selects for prolonged biparental
care. It would therefore be instructive to test whether brood reduction has an
even greater effect on desertion by A. coeruleopunctatus at the
forested site and whether experimental brood reduction will fail to promote
desertion by male C. panamenses at Parti.
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ACKNOWLEDGEMENTS |
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We thank the Smithsonian Tropical Research Unit and all the support staff for their assistance and Autoridad Nacional del Ambiente for issuing research permits. We especially thank P. Backwell, M. Velez, and S. Telford for their help at all stages of this project. J.H. Christy, M. Petrie, D. Pope, J.D. Reynolds, D.F. Westneat, and two anonymous reviewers provided valuable comments or encouragement.
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REFERENCES |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
|---|
Armstrong T, Robertson RJ, 1988. Parental investment based on clutch value: nest desertion in response to partial clutch loss in dabbling ducks. Anim Behav 36: 941-943.
Balshine-Earn S, 1995. The costs of parental care in Galilee St Peter's fish, Sarotherodon galilaeus. Anim Behav 50: 1-7.
Balshine-Earn S, 1997. The benefits of uniparental versus biparental mouth brooding in Galilee St. Peter's fish. J Fish Biol 50: 371-381.
Balshine-Earn S, Earn DJD, 1997. An evolutionary model of parental care in St. Peter's fish. J Theor Biol 184: 423-431.
Balshine-Earn S, Earn DJD, 1998. On the evolutionary
pathway of parental care in mouth-brooding cichlid fish. Proc R Soc Ser
B 265:
2217-2222.
Balshine-Earn S, McAndrew BJ, 1995. Sex-role reversal in the black-chinned tilapia, Sarotherodon melanotheron (Rüppel) (Cichlidae). Behaviour 132: 861-874.[Web of Science]
Barlow GW, 1974. Contrasts in social behaviour between Central American cichlid fishes and coral-reef surgeon fishes. Am Zool 14: 9-34.
Beissinger SR, 1986. Demography, environmental uncertainty, and the evolution of mate desertion in the snail kite. Ecology 67: 1445-1459.[Web of Science]
Beissinger SR, 1990. Experimental brood manipulations and the monoparental threshold in snail kites. Am Nat 136: 20-38.[Web of Science]
Beissinger SR, Snyder NFR, 1987. Mate desertion in the snail kite. Anim Behav 35: 477-487.
Burnham KP, White GC, Anderson DR, 1995. Model selection strategy in the analysis of capture-recapture data. Biometrics 51: 88-898.
Carlisle TR, 1981. The evolution of parental care patterns: a synthesis and a study of the breeding ecology of a cichlid fish, Aequidens coeruleopunctatus (PhD dissertation). Santa Barbara: University of California.
Carlisle TR, 1982. Brood success in variable environments: implications for parental care allocation. Anim Behav 30: 824-836.
Carlisle TR, 1985. Parental response to brood size in a cichlid fish. Anim Behav 33: 234-238.
Clutton-Brock TH, 1991. The evolution of parental care. Princeton: Princeton University Press.
Cohen J, 1988. Statistical power analysis for the behavioural sciences, 3rd ed. Hillsdale, New Jersey: Lawrence Erlbaum.
Coleman RM, 1993. The evolution of parental investment in fishes (PhD dissertation). Toronto: University of Toronto.
Coleman RM, Gross MR, Sargent RC. 1985. Parental investment decision rules, a test with bluegill sunfish. Behav Ecol Sociobiol 18: 59-66.
Cooper H, Hedges LV, eds, 1994. The handbook of research synthesis. New York: Russell Sage Foundation.
Eadie JM, Lyon BE, 1998. Cooperation, conflict, and crèching behavior in Goldeneye ducks. Am Nat 151: 397-408.[Web of Science][Medline]
Eggert A, Müller JK, 1997. Biparental care and social evolution in burying beetles: lessons from the larder. In: Social behaviour in insects and arachnids (Choe JC, Crespi BJ, eds). Cambridge: Cambridge University Press; 216-236.
Erikstad KE, Asheim M, Fauchald P, Dahlhaug L, Tveraa T, 1997. Adjustment of parental effort in the puffin; the roles of adult body condition and chick size. Behav Ecol Sociobiol 40: 95-100.
Ezaki Y, 1988. Mate desertion by male great reed warblers Acrocephalus arundinaceus at the end of the breeding season. Ibis 130: 427-437.[Web of Science]
Fujioka M, 1989. Mate and nest desertion in colonial little egrets. Auk 106: 292-302.[Web of Science]
Galvani AP, Coleman RM, 1998. Do parental convict cichlids of different sizes value the same brood number equally? Anim Behav 56: 541-546.[Web of Science][Medline]
Goodwin N, Balshine-Earn S, Reynolds JD, 1998.
Evolutionary transitions in parental care in cichlid fish. Proc R Soc
Ser B 265:
2265-2272.
Grafen A, Sibly R, 1978. A model of mate desertion. Anim Behav 26: 645-652.[Web of Science]
Hemborg C, 1999. Sexual differences in moult-breeding overlap and female reproductive costs in pied flycatchers, Ficedula hypoleuca. J Anim Ecol 68: 429-436.
Hõrak P, Jenni-Eiermann S, Ots I, 1999. Do great tits (Parus major) starve to reproduce? Oecologia 119: 293-299.[Web of Science]
Johnsen A, Lifjeld JT, Rohde PA, 1997. Coloured leg bands affect male mate guarding behaviour in the bluethroat. Anim Behav 54: 121-130.[Web of Science][Medline]
Keenleyside MHA, 1983. Male desertion in relation to adult sex ratio in the biparental cichlid fish, Herotilapia multispinosa. Anim Behav 31: 683-688.
Keenleyside MHA, 1985. Bigamy and mate choice in the biparental cichlid fish Cichlasoma nigrofasciatum. Behaviour 15: 138-160.
Keenleyside MHA, Bietz BF, 1981. The reproductive behaviour of Aequidens vittatus in Surinam, S. America. Environ Biol Fish 6: 87-94.
Kendall M, Stuart A, 1979. The advanced theory of statistics. vol 2. inference and relationship, 4th ed. New York: Macmillan.
Kleiman DG, 1977. Monogamy in mammals. Q Rev Biol 52: 39-69.[Medline]
Kokko H, 1999. Cuckoldry and the stability of biparental care. Ecol Lett 2: 247-255.[Web of Science]
Kraak SBM, van den Berghe EP, 1992. Do female fish assess paternity quality by means of test eggs? Anim Behav 43: 865-867.
Kramer DL, Bryant MJ, 1995. Intestine length in the fishes of a tropical stream: 2. Relationships to diet—the long and short of a convoluted issue. Environ Biol Fish 42: 129-141.
Laird NM, Ware JH, 1982. Random-effects models for longitudinal data. Biometrics 38: 963-974.[Web of Science][Medline]
Lavery RJ, 1995. Past reproductive effort affects parental behaviour in a cichlid fish, Cichlasoma nigrofasciatum: a comparison of inexperienced and experienced breeders with normal and experimentally reduced broods. Behav Ecol Sociobiol 36: 193-199.[Web of Science]
Lavery RJ, Keenleyside MHA, 1990. Parental investment of a biparental cichlid fish, Cichlasoma nigrofasciatum, in relation to brood size and past investment. Anim Behav 40: 1128-1137.
Lazarus J, 1990. The logic of mate desertion. Anim Behav 39: 672-684.
Lindsey JK, 1993. Models for repeated measurements. Oxford statistical science series 10. Oxford: Oxford Science Publications.
Lindström K, Sargent RC, 1997. Food access, brood size and filial cannibalism in the fantail darter, Etheostoma flabellare. Behav Ecol Sociobiol 40: 107-110.
Mathsoft, 1998. S-Plus guide to statistics. Seattle, Washington: Mathsoft.
Maynard Smith J, 1977. Parental investment: a prospective analysis. Anim Behav 25: 1-9.[Web of Science]
McCullagh P, Nelder JA, 1991. Generalized linear models, 2nd ed. London: Chapman and Hall.
Mock DW, Parker GA, 1986. Advantages and disadvantages of egret and heron brood reduction. Evolution 40: 459-470.[Web of Science]
Montgomerie RD, Weatherhead PJ, 1988. Risks and rewards of nest defence by parental birds. Q Rev Biol 63: 167-187.[Web of Science]
Mrowka W, 1987. Filial cannibalism and reproductive success in the maternal mouthbrooding cichlid fish Pseudocrenilabrus multicolor. Behav Ecol Sociobiol 21: 257-265.[Web of Science]
Nagoshi M, 1987. Survival of broods under parental care and parental roles of the cichlid fish, Lamprologus toae, in Lake Tanganyika. Jpn J Icthyol 34: 71-75.
Okuda N, Yanagisawa Y, 1996. Filial cannibalism in a paternal mouthbrooding fish in relation to mate availability. Anim Behav 52: 307-314.[Web of Science]
Patterson HD, Thompson R, 1971. Recovery of inter-block information when block sizes are unequal. Biometrica 58: 545-554.
Pinheiro JC, Bates DM, 1999. lme and nlme: mixed-effects methods and classes for S and S-PLUS. Madison: Bell Labs, Lucent Technologies and University of Wisconsin.
Pöysä H, Virtanen J, Milonoff M, 1997. Common goldeneyes adjust maternal effort in relation to prior brood success and not current brood size. Behav Ecol Sociobiol 40: 101-106.
Rangeley RW, Godin, J-GJ, 1992. The effect of a trade-off between foraging and brood defence on parental behaviour in the convict cichlid fish, Cichlasoma nigrofasciatum. Behaviour 120: 123-138.[Web of Science]
Ridgway MS, 1989. The parental response to brood size manipulation in smallmouth bass (Micropterus dolomieui). Ethology 80: 47-54.[Web of Science]
Robertson IC, Roitberg BD, 1998. Duration of parental care in pine engraver beetles: why do large males care less? Behav Ecol Sociobiol 43: 379-386.[Web of Science]
Roff DA, 1992. The evolution of life histories: theory and analysis. New York: Chapman and Hall.
Rogers W, 1987. Sex ratio, monogamy and breeding success in the Midas cichlid (Cichlasoma citrinellum). Behav Ecol Sociobiol 21: 47-51.[Web of Science]
Sabat AM, 1994. Costs and benefits of parental effort
in a brood-guarding fish (Ambloplites rupestris Centrarchidae).
Behav Ecol 5:
195-201.
Sakamoto Y, Ishiguro M, Kitagawa G, 1986. Akaike information criterion statistics. Amsterdam: D. Reidel Publishing Company.
Sargent RC, 1981. Sexual selection and reproductive effort in the threespine stickleback Gasterosteus aculeatus (PhD dissertation). Stony Brook: State University of New York.
Sargent RC, 1988. Parental care and egg survival both increase with clutch size in the fathead minnow, Pimephales promelas. Behav Ecol Sociobiol 23: 33-38.[Web of Science]
Sargent RC, 1997. Parental Care. In: Behavioural Ecology of Teleost Fishes (Godin J-GJ, ed). Oxford: Oxford University Press; 292-315.
Sargent RC, Gross MR, 1986. Williams' principle: an explanation of parental care in teleost fishes. In: Behaviour of teleost fishes (Pitcher TJ, ed). London: Croom Helm; 275-293.
Sargent RC, Gross MR, 1993. Williams' principle: an explanation of parental care in teleost fishes. In: Behaviour of teleost fishes, 2nd ed. (Pitcher TJ, ed). New York: Chapman & Hall; 333-361.
Scott MP, Gladstein DS, 1993. Calculating males? An empirical and theoretical examination of the duration of parental care in burying beetles. Evol Ecol 7: 362-378.
Systat, 1998. Systat 8.0. Statistics. Chicago: SPSS Inc.
Székely T, Cuthill IC, Kis J,
1999. Brood desertion in Kentish plover: sex differences in
remating opportunities. Behav Ecol 10:
185-190.
Székely T, Webb JN, Houston AI, McNamara JM, 1996. An evolutionary approach to offspring desertion in birds. Curr Ornithol 13: 271-330.
Székely T, Williams TD, 1995. Costs and benefits of brood desertion in female kentish plovers, Charadrius alexandrinus. Behav Ecol Sociobiol 37: 155-161.
Tait DEN, 1980. Abandonment as a reproductive tactic—the example of grizzly bears. Am Nat 115: 800-808.[Web of Science]
Townshend TJ, 1984. Effects of food availability on reproduction in Central American cichlid fishes (PhD dissertation). Aberystwyth: University of Wales.
Townshend TJ, Wootton RJ, 1985. Variation in the mating system of a biparental cichlid fish, Cichlasoma panamense. Behaviour 95: 181-197.[Web of Science]
Trumbo S, 1991. Reproductive benefits and the duration of paternal care in a biparental burying beetle, Necrophorus orbicollis. Behaviour 117: 82-105.[Web of Science]
Urano K, 1992. Early settling the following season: a long-term benefit of mate desertion by male great reed warblers Acrocephalus arundinaceus. Ibis 134: 83-86.
Valera F, Hoi H, Schleicher B, 1997. Egg burial in
penduline tits, Remiz pendulinus: its role in mate desertion and
female polyandry. Behav Ecol 8:
20-27.
Webb JN, Houston AI, McNamara JM, Szekely T, 1999. Multiple patterns of parental care. Anim Behav 58: 983-993.[Web of Science][Medline]
Westneat DF, Sargent RC, 1996. Sex and parenting: the effect of sexual conflict and parentage on parental strategies. Trends Ecol Evol 11: 87-91
Westneat DF, Sherman PW, 1993. Parentage and the
evolution of parental behavior. Behav Ecol
4: 66-77.
Winkler DW, 1991. Parental investment decision rules
in tree swallows: parental defense, abandonment, and the so-called Concorde
fallacy. Behav Ecol 2:
133-142.
Wisenden BD, 1994. Factors affecting mate desertion by
males in free-ranging convict cichlids (Cichlasoma nigrofasciatum).
Behav Ecol 5:
439-447.
Wisenden BD, Keenleyside MHA, 1992. Intraspecific brood adoption in convict cichlids: a mutual benefit. Behav Ecol Sociobiol 31: 263-269.[Web of Science]
Yamamura N, Tsuji N. 1993. Parental care as a game. J Evol Biol 6: 103-127.[Web of Science]
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