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Nest tending increases reproductive success, sometimes: environmental effects on paternal care and mate choice in flagfish
ANIMAL BEHAVIOUR, 2007, 74, 577e588 doi:10.1016/j.anbehav.2006.12.013
Nest tending increases reproductive success, sometimes: environmental effects on paternal care and mate choice in flagfish REB ECC A E. H ALE & COLET TE M. ST M AR Y
Department of Zoology, University of Florida, Gainesville (Received 23 February 2006; initial acceptance 22 April 2006; final acceptance 18 December 2006; published online 20 August 2007; MS. number: A10371)
Parents should adjust parental care if the costs and benefits of that care vary. Traditionally, the benefit of care has been assumed to be increased offspring fitness, yet increasing evidence indicates that care can also increase mating success. We examined male behaviour and reproductive success across environments in flagfish, Jordanella floridae, a pupfish found across a range of salinities in Florida, U.S.A. Care may be more beneficial to offspring in freshwater habitats than in brackish ones. If so, female preferences for care-giving males should be stronger in fresh water. We quantified male behaviour in fresh and brackish water for four populations and examined whether male behaviour influenced the probability of spawning or the number of eggs spawned. A male’s behaviour influenced his reproductive success, but did so differently in fresh and brackish water. In fresh water, the male’s behaviour prior to spawning was a strong predictor of whether or not he would spawn, whereas in brackish water, postspawning behaviour of males predicted additional spawning success. These results suggest that the traits that females use to assess potential mates differ depending on the salinity of the environment. Despite the importance to a male’s spawning success of different activities in different salinities, male behaviour did not differ consistently between salinities. We discuss possible benefits to females of a phenotypically plastic mate choice criterion and examine explanations for why male behaviour does not covary with the strength of sexual selection across environments. The Association for the Study of Animal Behaviour. Published by Elsevier Ltd.
Keywords: behavioural plasticity; courtship; flagfish; Jordanella floridae; mate choice; mating; parental care; parental investment; sexual conflict; sexual selection
The optimal amount of care to provide one’s young reflects a balance between the benefits of care to young and the costs to the parent’s residual reproductive value (e.g. Williams 1966; Sargent & Gross 1993; Webb et al. 2002). Consistent with this model, parents often reduce the care that they provide their offspring when the costs of caring are high (e.g. Brommer et al. 2000; Weimerskirch et al. 2001) and increase care when the benefits are high (Dale et al. 1996; Listøen et al. 2000). These natural selection pressures are not the only factors influencing parental
Correspondence and present address: R. E. Hale, Department of Biological Science, Florida State University, Tallahassee, FL 32306, U.S.A. (email: [email protected]). C. M. St Mary is at the Department of Zoology, University of Florida, Gainesville, FL 32611, U.S.A. 0003e 3472/07/$30.00/0
investment decisions, as an increasing body of work demonstrates that female mating preferences can select for male activity that is likely to improve offspring fitness (Møller & Thornhill 1998; Tallamy 2000; Pampoulie et al. 2004). For example, mating success can be associated with the quality of a potential mate’s nest (Reynolds & Jones 1999), the care that he will provide young (Forsgren ¨ stlund & Ahnesjo¨ 1998; Lindstro¨m et al. 2006) 1997; O and whether he is caring for a current brood (Petersen et al. 2005). Thus, natural and sexual selection can simultaneously influence optimal care. Natural and sexual selection may favour different amounts of care in species in which the choosy sex (e.g. females) is not the care-giving sex (e.g. males) (reviewed in Clutton-Brock 1991), as is the case for many invertebrates, fish and birds (reviews in Andersson 1994; Tallamy 2000).
577 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd.
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ANIMAL BEHAVIOUR, 74, 3
Specifically, imposing sexual selection on paternal care predicts an increase in care above the natural selection optima (Kirkpatrick 1985; Hoelzer 1989; Iwasa & Pomiankowski 1999), which can create conflict between the interests of males and females (reviewed in Arnqvist & Rowe 2005). Females should favour males that provide the greatest fitness benefits to offspring, whereas males should balance benefits to offspring against the costs of providing care (e.g. Trivers 1972; Westneat & Sargent 1996). For species distributed across a range of environmental conditions, the strength of this conflict can vary across environments if environmental conditions influence the benefits of care to offspring (Dale et al. 1996). If the strength of female preferences for parental males is correlated with the expected benefit of care to young, then preferences should be stronger in the environments in which care is most beneficial. Variation in care across environments, then, should reflect the changes in benefits to offspring as well as changes in the strength of mating preferences. We examined variation in parental care both within and between populations of flagfish, Jordanella floridae. Care in flagfish is provided entirely by males, who defend nesting territories and guard, clean and fan eggs from multiple females. Male parental behaviour is variable both within (St Mary et al. 2001; Hale et al. 2003) and between (C. M. St Mary, unpublished data) populations, and a component of this variation can be attributed to variation in salinity (St Mary et al. 2001). The benefits of parental care under various salinities are currently unknown. However, previous work suggests that care may be more beneficial in fresh water. Specifically, an increased rate of fungal infection in fresh water appears to reduce survival of unattended embryos (St Mary et al. 2004). Consequently, egg cleaning may be more beneficial in fresh than in brackish water. Furthermore, if egg cleaning is more beneficial to offspring in fresh water, then the strength of mating preferences for nest-tending males should be stronger in fresh water. We examined the effects of salinity on male activity before and after spawning in four populations of flagfish. Flagfish are native to both freshwater and brackish habitats, so we examined the effect of native habitat type on behavioural responses to salinity by observing males from both coastal and inland habitats. Behaviour may differ between populations native to different habitat types because of genetic drift resulting from reproductive isolation. Alternatively, behaviour may differ consistently between habitat types, suggesting adaptation to local conditions. In flagfish, the amount of gene flow across the salinity gradient is unknown. However, the proximity of freshwater habitats in Florida to coastal salt marsh may facilitate gene flow across the salinity gradient within drainages. An effect of native habitat type on behaviour would indicate that gene flow is restricted and that selection regimes differ between salinities. We also examined female mating preferences by determining whether male pre- and postspawning activity was associated with reproductive success. Male flagfish perform nest-tending activities, such as fanning and nest cleaning, prior to spawning (Bonnevier et al. 2003), and
these activities may serve as signals to potential mates of the quality of care that a male will provide young (Tallamy 2000). In addition, females often mate repeatedly with the same male and a male’s behaviour once he has eggs in his nest may influence whether a female will mate with him again (Tallamy 2000). Therefore, we examined male behaviour both before and after spawning, with respect to his initial and subsequent reproductive success. An effect of salinity on reproductive success would indicate that mating tendencies of males and/or females are plastic in response to salinity. An effect of male behaviour on reproductive success would suggest that females dynamically adjust their spawning activity in response to male behaviour. We expected female preferences based on male activity to vary in strength and direction across salinity treatments and populations, and a male’s preference for a particular female and his interest in mating to be similarly correlated with his activity across all treatments in much the same way that we expect courtship to be similar in all treatments. Indeed, field observations indicate that courtship T-circling (Mertz & Barlow 1966) precedes spawning in both inland and coastal populations (R. Hale, personal observation). As a result, we further expected variation across salinities and populations in the association between male behaviour and reproductive success to indicate variation in female mating preferences.
METHODS
Collection and Transportation Fish were collected from four sites in Florida between May and July of 2003 under Florida Fish and Wildlife Conservation Commission Scientific Collector’s Permit number FNC-03-015 U.S. and Fish and Wildlife Service Special Use Permit numbers 58875 and 03008 for St Marks National Wildlife Refuge and number 03 SUP 59 for Merritt Island National Wildlife Refuge. Seine nets, minnow traps and dip nets were used to collect animals. Otter Creek (OC, Levy County) and Miccosukee (MC, MiamiDade County) are inland and freshwater. St Marks (SM, St Marks National Wildlife Refuge, Wakulla County) and Merritt Island (MI, Merritt Island National Wildlife Refuge, Brevard County) are coastal, with freshwater areas in close proximity to brackish areas. Animals were transported to the Florida State University (FSU) campus in Tallahassee, where the experiments were conducted, in insulated coolers. Fish were transferred to 1-m diameter wading pools at the FSU Mission Road Greenhouse, where they experienced the natural daylight cycle. All animals were returned to their native sites within 4 months of collection.
Acclimation and Experiments Responses to salinity in each of the four populations were examined in a factorial design with two native habitat types (coastal and inland) crossed with two salinity treatments (fresh and brackish). Two populations were nested within each native habitat type. Males and females
HALE & ST MARY: PARENTAL CARE AND MATE CHOICE
from each population were acclimated to either 0.2 ppt (hereafter referred to as 0 ppt) or 15 ppt salinity from their native salinity at a rate of 5 ppt every other day such that all animals reached their target salinity treatment on the same day. Fish were then maintained at these salinities for 2 weeks prior to experimentation. Brackish water (15 ppt) was made by mixing Instant Ocean Aquarium Salt (Aquarium Systems, Inc., Mentor, OH, U.S.A.) with well water, whereas the freshwater treatment (0 ppt) consisted of unaltered well water. The experiment was conducted indoors at 28 1 C on a 14:10 h light:dark cycle. Each male was placed in a 37.5litre aquarium with two artificial plants, a carpeted spawning mat and a filter. We placed one female from the same population as the male and that was acclimated to the same salinity in a transparent plastic box within this aquarium, so that water was shared between the box and the aquarium. The female was maintained in the box for 48 h and then released into the aquarium. Twelve OC, nine MC and 11 SM males were observed in each salinity treatment; 10 and 11 MI males were observed in the fresh and brackish treatments, respectively. Twenty-four hours following the release of the female (day 1), we filmed each pair for 20 min and then we inspected each spawning mat for eggs. Daily from day 2 to day 14, each spawning mat was removed and all eggs were counted. Pairs were filmed for 20 min the first day that eggs were observed. All filming took place between 0800 and 1200 hours. Male behaviour was analysed using The Observer Pro 5.0 (Noldus Information Technology, Wageningen, The Netherlands). Each observation was divided between the time spent at or away from the nest, swimming, fanning, following the female, in courtship (T-circling) or spawning. In addition, we recorded frequencies of bites at and away from the nest, chases and spawning events. See Hale et al. (2003) for definitions of these activities. We also recorded instances in which the male followed rather than chased the female, if he remained no more than approximately three body lengths behind the female and swam at approximately the same speed but did not make contact with the female. We measured reproductive success based on whether a pair spawned (spawning success) and the number of eggs that each male received.
Analyses Three composite responses were analysed: number of approaches towards the female (chases plus follows), number of nest-tending activities (bites at the nest plus fanning events) and proportion of time at the nest. We considered male activity to reflect a decision either to perform the activity at a level appropriate to the environment or to not perform the activity at all. Under this assumption, males that did not perform a given activity did so either because they were categorically inactive or because they assessed the environment and decided that ‘no activity’ was optimal. Ideally, we would have evaluated only those males whose activity levels were adjusted to the environment, but this was not possible. As an
alternative, we analysed each composite behavioural response in two ways. First, each response was treated as a binomial response variable with males scored as either showing or not showing the response. The effects of salinity, native habitat type and population on whether or not males showed the response were analysed using logistic regression. Second, the responses were treated as interval data, with the effects of the treatments on the frequency of the responses analysed using log-linear (Poisson) regression. In these analyses, males that did not perform the activity were excluded. Each of these analyses is valuable in our interpretation of male behaviour. The logistic regression evaluates activity as a binomial response and considers whether or not a male performed an activity, regardless of whether he was categorically inactive or he decided that ‘no activity’ was optimal. In contrast, the log-linear regression evaluates the magnitude of activity and considers the male’s energetic investment into the activity. All analyses were conducted using PROC GENMOD in SAS version 8 (SAS Institute, Cary, NC, U.S.A.) using logistic regression for binomial data and log-linear regression for frequency data. For log-linear regressions, a negative binomial error distribution was specified to reduce model deviance. Interaction terms (see below) were removed from full statistical models using backward elimination, if P > 0.10. Main effects of salinity, native habitat type and population (nested within habitat type) were included in all analyses, regardless of the significance of their effect, to consistently remove variance explained by these variables from all analyses. Summary statistics provided in the text and figures are means standard error. We analysed the effects of salinity, native habitat type and population (nested within native habitat type) on male behaviour during a preparental phase and a parental phase. We limited our testing of interaction effects to that between salinity and native habitat type. The preparental phase consisted of day 1 observations of all males that had not spawned in the 24 h since the female was released (73 of 82 males). The parental phase began when eggs were first observed in a nest and parental behaviour was measured from the observation of each male on the first day that eggs were observed (57 of 82 males). We also examined whether a pair’s reproductive success, either the probability of spawning or the number of eggs received, were influenced by male behaviour (either preparental or parental), salinity, native habitat type, population (nested within native habitat type), and all possible two- and three-way interactions between male behaviour, salinity and native habitat type. First, we examined the effect of preparental male behaviour on spawning success and number of eggs received across the entire 14-day trial. Second, we examined the effect of parental male behaviour on spawning success and number of eggs received in the 2 days immediately following the parental observation, because females may continue to spawn with the same male once he has eggs in his nest. In analyses examining the effect of male activity (yes/no) on spawning (yes/no), we included all males for which there were behavioural observations. In analyses examining the
579
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ANIMAL BEHAVIOUR, 74, 3
Table 1. Effects of preparental behaviour and parental behaviour on reproductive success (spawning success and eggs spawned) of flagfish Spawned (yes/no) Model
Predictor
Preparental behaviour 1 Approaches Salinity Habitat type Population (habitat) 2
3
Nest tending Salinity Habitat type Population (habitat) Tending*salinity At nest Salinity Habitat type Population (habitat)
Parental behaviour 1 Approaches Salinity Habitat type Population (habitat) Approaches*salinity Approaches*habitat 2 Nest tending Salinity Habitat type Population (habitat) Tending*habitat 3
At nest Salinity Habitat type Population (habitat) At nest*salinity
Eggs spawned
df
c2
P
N
c2
P
N
1 1 1 2
0.07 1.07 0.65 8.32
0.79 0.30 0.42 0.016
73
0.18 1.47 0.13 0.48
0.67 0.22 0.72 0.79
30
1 1 1 2 1
1.40 7.43 0.50 9.33 10.83
0.24 0.006 0.480 0.009 0.001
73
1.1 1.59 0.18 0.67
0.29 0.21 0.67 0.72
30
1 1 1 2
0.04 1.37 0.65 8.57
0.85 0.24 0.42 0.014
73
2.07 4.96 0.09 1.09
0.15 0.026 0.76 0.58
35
1 1 1 2 1 1
1.93 6.60 4.41 2.62 4.45 4.03
0.16 0.010 0.036 0.27 0.035 0.045
57
0.19 3.93 0.09 2.77 4.08
0.67 0.047 0.77 0.25 0.043
42
1 1 1 2 1
8.84 1.88 0.53 1.51 4.83
0.003 0.17 0.47 0.47 0.028
57
0.97 0.2 0.09 0.32
0.32 0.65 0.77 0.85
37
1 1 1 2 1
4.47 3.84 1.65 1.82 3.21
0.035 0.050 0.20 0.40 0.07
57
1.42 0.01 0.0 0.85
0.23 0.94 0.96 0.65
37
Population is nested within habitat type. Logistic and log-linear regressions were used to examine effects on whether or not males spawned and the number of eggs received, respectively, as a function of preparental and parental behaviour. Tests of interaction effects were limited to the interaction between behaviour and habitat type, and behaviour and salinity. Interaction terms with P > 0.2 were removed from the statistical models. P values of significant tests are highlighted in bold.
effect of the frequency of activity on the number of eggs spawned, we included only those males that spawned and performed the relevant activity. As a result, sample sizes of the latter analyses were smaller than those of the former analyses (Tables 1 and 2). We first present the results for reproductive success, as these generate predictions for how male behaviour should vary with salinity.
RESULTS
Salinity, Native Habitat Type and Population The effects of salinity, native habitat type and population (nested within habitat type) on reproductive success were evaluated in models that also included male behaviour as independent variables. Preparental and parental behaviour were considered in separate models (Table 1). Only population (nested within habitat type) had a consistent effects on initial spawning success across all three
models (preparental behaviour models, Table 1). Initial spawning success was 54% for Otter Creek, 71% for Miccosukee, 50% for Merritt Island and 91% for St Marks. None of these variables had a consistent effect on whether the pair spawned again after the initial spawning event (parental behaviour models, Table 1). Among males that spawned (57 of 82 males), salinity, native habitat type and population (nested within habitat type) did not influence the number of eggs received over 14 days (mean SE ¼ 49.1 8.9 eggs), the latency to spawn (4.2 0.6 days), or the mean clutch size (11.0 1.5 eggs), estimated as the total number of new eggs observed divided by the number of days on which new eggs were observed for a given male. In addition to the 57 pairs that were observed during the preparental phase and that subsequently spawned, nine pairs spawned on the day that the female was released before a preparental observation could be made. These males necessarily had a shorter latency to spawn than the other males used in our analyses, and they received, on average, nearly twice as many eggs (mean SE ¼ 80.4 34.8 eggs), but had similar mean
HALE & ST MARY: PARENTAL CARE AND MATE CHOICE
Table 2. The effects of salinity, native habitat type (inland versus coastal) and population (nested within habitat type) on preparental behaviour and parental behaviour Performed (yes/no) N
c2
P
N
0.002 0.48 0.046 0.017
73
6.69 0.09 1.08
0.01 0.76 0.58
30
1.07 0.17 7.99
0.30 0.68 0.018
73
5.48 0.01 1.80 16.21
0.019 0.92 0.41 <0.001
27
1 1 2
0.33 0.71 2.46
0.56 0.40 0.29
73
2.20 0.08 0.89
0.14 0.78 0.64
35
Salinity Habitat type Population (habitat) Clutch size
1 1 2 1
0.38 0.01 9.01 1.07
0.54 0.91 0.011 0.3
57
0.22 0.09 1.12 0.01
0.64 0.77 0.58 0.94
42
Nest tending activities
Salinity Habitat type Population (habitat) Clutch size
1 1 2 1
0.0 0.3 1.31 11.19
0.95 0.58 0.52 <0.001
57
1.59 5.20 1.18 3.36
0.21 0.023 0.55 0.067
37
Time at nest
Salinity Habitat type Population (habitat) Habitat*salinity Clutch size
1 1 2 1 1
0.44 1.59 0.15 5.18 8.83
0.51 0.21 0.93 0.022 0.003
57
0.18 2.39 0.30 3.10
0.67 0.12 0.86
41
Variable Preparental behaviour Approaches
Nest tending activities
Time at nest
Parental behaviour Approaches
Predictor
df
c2
Salinity Habitat type Population (habitat) Habitat*salinity Salinity Habitat type Population (habitat) Habitat*salinity Salinity Habitat type Population (habitat)
1 1 2 1
9.5 0.49 6.15 5.67
1 1 2 1
Frequency performed
P
0.078
Population is nested within habitat type. Logistic regression was used to examine the proportion of males that performed the activity. Loglinear regression was used to examine the number of activities performed. Tests of interaction effects were limited to the interaction between habitat type and salinity. Interaction terms with P > 0.2 were removed from the statistical models. P values of significant tests are highlighted in bold.
clutch size (13.8 4.7 eggs). Four of these males were from the Miccosukee site, three from Merritt Island and two from St Marks.
Sexual Selection on Male Behaviour A male’s behaviour influenced his reproductive success, although it did so differently in fresh and brackish water. In fresh water, preparental behaviour was important to spawning success, whereas in brackish water, parental behaviour was important. In fresh water, males that tended their nests during the preparental phase were significantly more likely to spawn than males that did not tend their nests (logistic regression, tending: c21 ¼ 10:88, N ¼ 38, P ¼ 0.001; habitat type: c21 ¼ 0:05, P ¼ 0.82; population (habitat): 2 c1 ¼ 10:57, P ¼ 0.005; Table 1, Fig. 1). If the direct benefits of nest tending are greater in fresh than in brackish water, as we suggest they are (St Mary et al. 2004), then females should increase their preference for tending where the benefit of doing so is greater, particularly if a male’s nest tending during the preparental phase indicates his tending once he has eggs.
In brackish water, preparental behaviour was not related to spawning success (logistic regression: tending: c21 ¼ 2:29, N ¼ 35, P ¼ 0.13; habitat type: c21 ¼ 1:54, P ¼ 0.21; population (habitat): c21 ¼ 1:37, P ¼ 0.51). However, three activities performed during the parental phase were important to subsequent reproductive success. Males that approached the female during the parental phase were more likely to spawn than males that did not approach the female (Table 1, Fig. 2). However, males that approached the female received fewer eggs on average than males that did not approach (Table 1, Fig. 3). Males that spent time at the nest were also more likely to spawn. In both fresh and brackish water, females preferred males that tended the nest during the parental phase, but only if the pair was from a coastal population (Table 1, Fig. 2). We expected that preferences for activities that increase offspring fitness would be stronger in fresh water than in brackish water. Assuming spawning success indicates, in part, female mating preferences (i.e. single male choice test; Wagner 1998; Shackleton et al. 2005) and that nestassociated activities (nest tending and presence at the nest) increase offspring fitness (Klug et al. 2005), then our data offer mixed support for this prediction. Both preparental-phase and parental-phase nest-associated
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ANIMAL BEHAVIOUR, 74, 3
100 (a)
7
80 60
9
*
*
11
40
11
20 % Spawned
582
0
Inland
Coastal
100
Tended Did not tend
(b) 80 60
12
12 10
8
40 20 0
males, but among males that tended, coastal males tended more. Two activities that did not influence reproductive success were affected by salinity. Among coastal males, preparental nest tending was more frequent in brackish water. In addition, coastal males were more likely than inland males to approach the female during the preparental phase and all males approached the female more often in brackish water (Table 2, Fig. 4a, b). In addition to these treatment effects, male behaviour during the parental phase was influenced by clutch size. The more eggs a male had in his nest during the parental phase, the more likely he was to tend and to spend time at his nest (Table 2, Fig. 6).
Inland
Coastal Native habitat type
Figure 1. Spawning success as a function of preparental behaviour in (a) fresh and (b) brackish water. Numbers above bars indicate the total number of males observed. *P < 0.05.
activities were important to spawning success, but their influences were not always greater in fresh than in brackish water (e.g. males that spent time at the nest during the parental phase were more likely to spawn, but only in brackish water; the opposite of what we expected). Furthermore, in both fresh and brackish water, parentalphase nest tending increased spawning success.
Behavioural Responses to Sexual Selection Based on the effects of male behaviour on spawning success described above, we expected males to be more likely to perform certain activities in the salinities in which those activities increase spawning success. Specifically, we expected nest tending during the preparental phase to be more likely in fresh water, for approaches and presence at the nest during the parental phase to be more likely in brackish water, and for nest tending to be more likely among coastal males. Nearly without exception, these expectations were not met. Preparental nest tending was not more likely in fresh water (Table 2, Fig. 4d) nor were parental-phase approaches and nest tending more likely in brackish water (Table 2, Fig. 5a). Furthermore, males were not more likely to spend time at the nest during the parental phase when in fresh water than when in brackish water (salinity habitat type interaction; Table 2, Fig. 5e). Finally, coastal males were not more likely to tend the nest during the parental phase than were the inland
Association between Preparental and Parental Behaviour The decision to spawn with a male based on his nest tending before spawning may offer a female direct benefits if such nest tending directly increases success of offspring subsequently spawned and reared in the nest, or if the male’s activity towards an empty nest indicates his care of a future brood. We used log-linear and logistic regressions to determine whether the frequency or probability, respectively, of male preparental behaviour is a good indicator of male parental behaviour. In the analyses of the probability of performing a particular activity, we included all males that spawned, and we examined the effects of all two- and three-way interactions between salinity, native habitat type and day 1 male behaviour (preparental behaviour) on male behaviour on the first day that the male had eggs (parental behaviour). In the analyses of the frequency of activities, we included only males that performed the activity during the preparental phase and then subsequently spawned. This greatly reduced sample sizes, precluding the testing of all possible interactions. Therefore, we pooled all males regardless of salinity treatment, native habitat type or population. In general, male activity before spawning did not predict postspawning behaviour (Table 3). Males that spent time at the nest during the preparental phase were equally likely to do so once they had eggs as were males that did not spend time at the nest during the preparental phase. Furthermore, whether or not a male approached the female during the preparental phase did not predict whether he did so once he had eggs. Similarly, whether a male tended the nest during the preparental phase did not predict whether he did so once he had eggs. The number of approaches towards the female, the frequency of nest tending and the time spent at the nest during the preparental phase also did not predict the male’s performance of these activities once he had eggs.
DISCUSSION
Female Mating Preferences We found no evidence that the tendency to spawn is plastic in response to salinity, as there was no main effect
HALE & ST MARY: PARENTAL CARE AND MATE CHOICE
100
Fresh water (a)
10
2
8
80
5
40
20
20
100
Inland
80
100
9 7
*
40
20
20
80
Inland
100 1
Inland
Coastal
(f)
At nest
40
40
20
20
Coastal Native habitat type
0
11
*
Not at nest 12
60
Inland
*
11
6
80 6
60
0
Tended Did not tend
4
0
Coastal 11
7
(d)
11
40
(e)
*
12
Coastal
80 60
100
3 Inland
3
6
60
0
*
5
0
Coastal
(c)
12
Approached Did not approach
60
40
0
Brackish water (b)
80
60
% Spawned
100
*
3 6
Inland
Coastal Native habitat type
Figure 2. Spawning success as a function of parental behaviour of flagfish in fresh and brackish water, respectively: (a, b) approach female, (c, d) tend nest and (e, f) spend time at nest. Numbers above bars indicate the total number of males observed. *P < 0.05.
of salinity, native habitat type, or their interaction on reproductive success. However, we found evidence that sexual selection on male behaviour varies across salinities and that selection on preparental behaviour differs from selection on parental behaviour, indicating that females use male parental care behaviour to assess mates and that they adjust their mating activity in response to salinity and the presence of eggs in a male’s nest. In fresh water, where the benefits of care are expected to be greater (St Mary et al. 2004), males that tended nests during the preparental phase had higher spawning success than males that did not tend nests. In brackish water, activity during the parental phase influenced reproductive success; males that approached the female and that spent time at the nest were more likely to spawn. In both salinities,
coastal males were more likely to spawn if they tended the nest during the parental phase. If spawning success reflects female mating preferences (Wagner 1998; Shackleton et al. 2005), as we suggest it does, then these results indicate that preferences are plastic in response to salinity and that they vary geographically. Females often choose mates based on the quality of their nest sites (Kodric-Brown 1983; Reynolds & Jones 1999) or the care that they will provide young (e.g. Forsgren 1997; ¨ stlund & Ahnesjo¨ 1998), and preferences for these direct O benefits may change as factors defining quality change. For example, Reynolds & Jones (1999) found that, in gobies, Pomatoschistus microps, female preference for males with small, more cryptic nest entrances disappeared under low oxygen conditions, where the importance of water flow
583
ANIMAL BEHAVIOUR, 74, 3
25 20 Eggs received
584
Fresh Brackish 7
15 10 5 0
8 18
24
Approached
Did not approach Male activity
Figure 3. Mean SE number of eggs that a male received as a function of whether the male approached the female and was in fresh or brackish water. Inland and coastal populations were pooled. Sample sizes are given above bars.
and egg fanning to offspring survival may outweigh the benefit of reduced nest predation. Nest tending in flagfish appears to reduce predation (Klug et al. 2005) and may reduce fungal infection (via the removal of infected egg or detritus from the nest). We found that females were more likely to spawn with males that tended nests before spawning, but only in fresh water. The relative importance of removing detritus may be low in brackish water, where the rates of fungal infection are lower (St Mary et al. 2004), such that preparental tending is a less reliable indicator of offspring survival in this environment. If preparental nest tending is an indicator to females of direct benefits for offspring, then we might expect preparental nest tending to be correlated with nest tending after spawning, but this was not the case. An alternative adaptive explanation is that preparental nest tending may have immediate effects on the nest itself that influence survival of eggs once they are laid such that preparental nest tending indicates hatching success. Indeed, removal of detritus from the nest prior to spawning may reduce fungal infection throughout embryo development (Cote & Gross 1993), because the spores of at least some oomycetes (e.g. Saprolegnia) are attracted to dead material (Smith et al. 1985). Females may also choose mates based on the amount they are courted. For example, female green swordtails, Xiphophorus helleri, are more likely to respond to males that perform courtship displays than they are to males performing other activities (Rosenthal et al. 1996), and similar preferences for courtship displays have been demonstrated in insects and birds (reviewed in Andersson 1994). In flagfish, males that approached the female in brackish water were more likely to spawn than males that did not approach the female. Rates of fungal infection are low in brackish water, so females may shift their choice criterion from male activity that may improve offspring fitness to activity that indicates a male’s eagerness to spawn, such as whether or not a male approaches. We have argued that females may be more likely to spawn with males that show nest tending before spawning because of the direct benefits that nest tending offers.
An alternative explanation is that females do not choose mates based on the direct benefits of parental care but on the indirect, genetic benefits to their offspring (reviewed in Andersson 1994). Females can improve the fitness of their offspring by selecting males of higher genetic quality (e.g. Parker 2003), and in flagfish, male behaviour may indicate male quality. If the energetic costs of activity vary with salinity, so might the reliability of male behaviour as an indicator of quality. In fresh water, where the energetic costs of nest tending may be higher (Evans 1993, see below), male nest tending before spawning may be a better indicator of male quality than it is in brackish water, where all males, regardless of condition or genetic quality, may be able to tend nests. However, while this explanation holds for the pattern in fresh water, it cannot explain the advantage of postspawning nest tending in brackish water. Regardless of the type of benefit that females gain from their decisions, our results suggest that female reproductive decisions are plastic not only in the magnitude, and possibly the direction, of preference but also in the traits used to select mates. In addition, female preferences changed after spawning. These changes may reflect that females make different decisions when assessing males with versus without eggs, when assessing a male for the first time versus reassessing him after already spawning with him, or when assessing a male after a period of not spawning versus after having recently spawned. These three possibilities were confounded in our experiment but potentially reflect different mate choice decisions.
Male Behaviour Our results clearly indicate a sexual selection advantage of preparental nest tending in fresh water, whereas this advantage was not present in brackish water. Given this, and our understanding of how salinity influences embryo hatching success and adult metabolism, we would expect male nest tending to vary with salinity. However, males were not more likely to tend nests in fresh water, and coastal males actually tended nests more in brackish water. Coastal males may have tended nests less in fresh than in brackish water as a result of negative effects of a novel environment, yet this is not entirely consistent with our results. If a novel salinity environment were to elicit such a response, we would expect to see effects of salinity on female fecundity, a measure that we expect to be tightly linked with energy expenditure and metabolic rate. However, there were no effects of salinity or native habitat type on clutch size, total eggs laid, or latency to spawn. Our results also indicate an advantage of approaching the female during the parental phase for inland males in brackish water. However, males were not more likely to approach and did not approach more in brackish water, suggesting that relatively strong sexual selection in brackish water does not entirely explain plasticity in approach activity. Similarly, both coastal and inland males were favoured if they tended the nest in brackish water, but
HALE & ST MARY: PARENTAL CARE AND MATE CHOICE
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Figure 4. Preparental behaviour of male flagfish (i.e. observed on day 1). (a) Proportion of males that made advances towards the female. (b) Number of approaches towards the female, excluding males that did not approach. (c) Proportion of males that tended nests. (d) Number of nest-tending activities performed by males, excluding males that did not tend. (e) Proportion of males that spent time at the nest. (f) Percentage of time that males spent at the nest, excluding males that spent no time at the nest. Means and SEs were calculated from lntransformed values and backtransformed for the figures. In (a), (c) and (e), the numbers above the bars are the total number of males observed. In (b), (d) and (f), the numbers indicate sample sizes and equal the number of males observed in (a), (c) and (e) that performed the activity. *P < 0.05.
they were not more likely to tend the nest in brackish water, despite the mating advantage. There are at least two possible explanations for why plasticity in male behaviour did not mirror plasticity in female mating preferences: (1) responses to salinity are the direct consequence of metabolic processes or (2) male behaviour reflects a balance of the fitness consequences across environments. We reject the first hypothesis because there were no consistent effects of salinity on behaviour either before or after spawning; although preparental males approached the female more in brackish water, no other male activities showed the same pattern. Our results are consistent with the second
hypothesis. This hypothesis requires that the increased offspring fitness and sexual selection benefits in fresh water be balanced by the increased energetic or opportunity costs of care in fresh water, and thus, that the optimum level of male care remains constant across environments. Energetic costs of care may, indeed, be higher in fresh water than in brackish water. Metabolic costs often vary with salinity as a result of the effect of salinity on osmoregulatory demands. For example, in euryhaline fish, those that tolerate a broad range of salinities, metabolic rate often increases as a function of the gradient between environmental and plasma ion concentrations
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Figure 5. Parental behaviour of male flagfish (i.e. observed on the first day of eggs). (a) Proportion of males that made advances towards the female. (b) Number of approaches towards the female, excluding males that did not approach. (c) Proportion of males that tended nests. (d) Number of nest-tending activities performed by males, excluding those that did not tend. (e) Proportion of males that spent time at the nest. (f) Percentage of time that males spent at the nest, excluding males that spent no time at the nest. Means and SEs were calculated from ln-transformed values and backtransformed for the figures. In (a), (c) and (e), the numbers above the bars are the total of males observed. In (b), (d) and (f), the numbers indicate sample sizes and equal the number of males observed in (a), (c) and (e) that performed the activity. *P < 0.05.
(Nordlie 1978; Evans 1993). In flagfish, plasma ion concentrations correspond to approximately 10e15 ppt (Nordlie & Walsh 1989), suggesting that osmoregulatory costs may be higher in fresh water than in brackish water. These osmoregulatory costs may translate into different costs of parental care through two mechanisms. First, care may be more costly in fresh water because of direct physiological costs or constraints. If the costs of osmoregulation are higher in fresh water, then the costs of sustaining parental care activity may also be higher. Furthermore, fish already sustaining high metabolic rates for osmoregulation may not be able to increase their metabolic rates sufficiently
to provide care (i.e. narrower metabolic scope). Second, higher energetic demands of osmoregulation may make it more costly to forgo foraging to provide care. Whether such costs vary with salinity in flagfish has yet to be measured, but data from other species suggest that the effect of salinity on metabolic rate varies widely (e.g. Brocksen & Cole 1972; Muir & Niimi 1972; Moser & Hettler 1989; Claireaux & Lagardere 1999). We expect sexual selection benefits to covary with the direct benefits of care to offspring, whereas the costs of care may vary independently. In this system, the parental costs, direct benefits and the sexual selection benefits of
HALE & ST MARY: PARENTAL CARE AND MATE CHOICE
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across salinities, being stronger in fresh water, where costs and benefits are both high. To our knowledge, variation in the strength of sexual conflict across populations has not been measured (Arnqvist & Rowe 2005), but we suggest that a system in which the benefits of care vary across environments offers a good opportunity to describe such variation because the direct benefits of choosing a good parent as a mate should also vary.
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We thank Joe Travis, Jane Brockmann, Craig Osenberg, Alice Winn, Shirley Baker and the laboratories of C. St Mary, C. Osenberg and B. Bolker for discussion of the data and comments on the manuscript. Sheryl Soucy-Lubell, Becky Fuller, Margaret Gunzburger and Jessica Draughton helped with collection of animals and data. In addition, the judges of the 2005 ABS Allee Symposium provided useful criticisms of the manuscript. Animal care and use procedures were approved by both the University of Florida IACUC and Florida State University ACUC. This work was supported by a National Science Foundation Doctoral Dissertation Improvement Grant.
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References
Number of eggs in nest Figure 6. The percentage of males that (a) tended their nests and (b) spent time at their nests as a function of the number of eggs in the nest. Bin size ranges for egg number are not constant. Numbers above bars indicate the number of males in that bin.
care may all positively covary such that environments with relatively high benefits also have relatively high costs. A consequence of this covariance may be that the strength of sexual conflict over paternal care is variable Table 3. The relationships between preparental and parental male activity Performed (yes/no)
Frequency performed
Predictor
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c2
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1 1 1 2
0.61 2.95 0.07 0.05
0.43 47 0.22 0.96 21 0.09 0.79 0.09
Nest tending Salinity Habitat type Population (habitat)
1 1 1 2
2.29 0.70 0.28 0.08
0.13 47 0.04 0.84 20 0.40 0.60 0.96
At nest Salinity Habitat type Population (habitat)
1 1 1 2
3.07 0.04 63.00 0.13
0.08 47 0.17 0.68 23 0.83 0.43 0.94
P
N
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N
Population is nested within habitat type. Logistic regression was used to examine the proportion of males that performed the activity. Loglinear regression was used to examine the number of activities performed, with males pooled across treatments.
Andersson, M. 1994. Sexual Selection. Princeton, New Jersey: Princeton University Press. Arnqvist, G. & Rowe, L. 2005. Sexual Conflict. Princeton, New Jersey: Princeton University Press. Bonnevier, K., Lindstrom, K. & St Mary, C. M. 2003. Parental care and mate attraction in the Florida flagfish, Jordanella floridae. Behavioral Ecology and Sociobiology, 53, 358e363. Brocksen, R. W. & Cole, R. E. 1972. Physiological responses of three species of fishes to various salinities. Journal of the Fisheries Research Board of Canada, 29, 399e405. Brommer, J., Kokko, H. & Pietiainen, H. 2000. Reproductive effort and reproductive values in periodic environments. American Naturalist, 155, 454e472. Claireaux, G. & Lagardere, J. P. 1999. Influence of temperature, oxygen and salinity on the metabolism of the European sea bass. Journal of Sea Research, 42, 157e168. Clutton-Brock, T. H. 1991. The Evolution of Parental Care. Princeton, New Jersey: Princeton University Press. Cote, I. M. & Gross, M. R. 1993. Reduced disease in offspring: a benefit of coloniality in sunfish. Behavioral Ecology and Sociobiology, 33, 269e274. Dale, S., Gustavsen, R. & Slagsvold, T. 1996. Risk taking during parental care: a test of three hypotheses applied to the pied flycatcher. Behavioral Ecology and Sociobiology, 39, 31e42. Evans, D. H. 1993. Osmotic and ionic regulation. In: The Physiology of Fishes (Ed. by D. H. Evans), pp. 315e341. Boca Raton, Florida: CRC Press. Forsgren, E. 1997. Female sand gobies prefer good fathers over dominant males. Proceedings of the Royal Society of London, Series B, 264, 1283e1286. Hale, R. E., St Mary, C. M. & Lindstrom, K. 2003. Parental responses to changes in costs and benefits along an environmental gradient. Environmental Biology of Fishes, 67, 107e116. Hoelzer, G. A. 1989. The good parent process of sexual selection. Animal Behaviour, 38, 1067e1078.
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Iwasa, Y. & Pomiankowski, A. 1999. Good parent and good genes models of handicap evolution. Journal of Theoretical Biology, 200, 97e109. Kirkpatrick, M. 1985. Evolution of female choice and male parental investment in polygynous species: the demise of the sexy son. American Naturalist, 125, 788e810. Klug, H., Chin, A. & St Mary, C. M. 2005. The net effects of guarding on egg survivorship in the flagfish, Jordanella floridae. Animal Behaviour, 69, 661e668. Kodric-Brown, A. 1983. Determinants of male reproductive success in pupfish (Cyprinodon pecosensis). Animal Behavior, 31, 128e137. ¨ m, K., St Mary, C. M. & Pampoulie, C. 2006. Sexual selecLindstro tion for male parental care in the sand goby, Pomatoschistus minutus. Behavioral Ecology and Sociobiology, 60, 46e51. Listøen, C., Karlsen, R. F. & Slagsvold, T. 2000. Risk taking during parental care: a test of the harm-to-offspring hypothesis. Behavioral Ecology, 11, 40e43. Mertz, J. C. & Barlow, G. W. 1966. On the reproductive behavior of Jordanella floridae (Pisces: Cyprinodontidae) with special reference to a quantitative analysis of parental fanning. Zeitschrift fu¨r Tierpsychologie, 23, 537e554. Møller, A. P. & Thornhill, R. 1998. Male parental care, differential parental investment by females and sexual selection. Animal Behaviour, 55, 1507e1515. Moser, M. L. & Hettler, W. F. 1989. Routine metabolism of juvenile spot, Leiostomus xanthurus (Lacepede), as a function of temperature, salinity and weight. Journal of Fish Biology, 35, 703e707. Muir, B. S. & Niimi, A. J. 1972. Oxygen consumption of euryhaline fish aholehole (Kuhlia sandvicensis) with reference to salinity, swimming, and food consumption. Journal of the Fisheries Research Board of Canada, 29, 67e77. Nordlie, F. G. 1978. Influence of environmental salinity on respiratory oxygen demands in euryhaline teleost, Ambassis interrupta Bleeker. Comparative Biochemistry and Physiology A, 59, 271e274. Nordlie, F. G. & Walsh, S. J. 1989. Adaptive radiation in osmotic regulatory patterns among 3 species of cyprinodontids (Teleostei, Atherinomorpha). Physiological Zoology, 62, 1203e1218. ¨ stlund, S. & Ahnesjo ¨ , I. 1998. Female fifteen-spined sticklebacks O prefer better fathers. Animal Behaviour, 56, 1177e1183. Pampoulie, C., Lindstrom, K. & St Mary, C. M. 2004. Have your cake and eat it too: male sand gobies show more parental care in the presence of female partners. Behavioral Ecology, 15, 199e204. Parker, T. H. 2003. Genetic benefits of mate choice separated from differential maternal investment in red junglefowl (Gallus gallus). Evolution, 57, 2157e2165. Petersen, C. W., Mazzoldi, C., Zarrella, K. A. & Hale, R. E. 2005. Fertilization mode, sperm characteristics, mate choice and
parental care patterns in Artedius spp. (Cottidae). Journal of Fish Biology, 67, 239e254. Reynolds, J. D. & Jones, J. C. 1999. Female preference for preferred males is reversed under low oxygen conditions in the common goby (Pomatoschistus microps). Behavioral Ecology, 10, 149e154. Rosenthal, G. G., Evans, C. S. & Miller, W. L. 1996. Female preference for dynamic traits in the green swordtail, Xiphophorus helleri. Animal Behaviour, 51, 811e820. ¨ m, K. 2001. EnvironSt Mary, C. M., Noureddine, C. & Lindstro mental effects on male reproductive success and parental care in the Florida flagfish (Jordanella floridae). Ethology, 107, 1035e1052. St Mary, C. M., Gordon, E. & Hale, R. E. 2004. Environmental effects on egg development and hatching success in Jordanella floridae, a species with parental care. Journal of Fish Biology, 65, 760e768. Sargent, R. C. & Gross, M. R. 1993. Williams’ principle: an explanation of parental care in teleost fishes. In: The Behavior of Teleost Fishes (Ed. by T. J. Pitcher), pp. 275e293. London: Chapman & Hall. Shackleton, M. A., Jennions, M. D. & Hunt, J. 2005. Fighting success and attractiveness as predictors of male mating success in the black field cricket, Teleogryllus commodus: the effectiveness of no-choice tests. Behavioral Ecology and Sociobiology, 58, 1e8. Smith, S. N., Armstrong, R. A., Springate, J. & Barker, G. 1985. Infection and colonization of trout eggs by Saprolegniaceae. Transactions of the British Mycological Society, 85, 719e723. Tallamy, D. W. 2000. Sexual selection and the evolution of exclusive paternal care in arthropods. Animal Behaviour, 60, 559e567. Trivers, R. L. 1972. Parental investment and sexual selection. In: Sexual Selection and the Descent of Man (Ed. by B. Campbell), pp. 136e179. London: Heinemann. Wagner, W. E. 1998. Measuring female mating preferences. Animal Behaviour, 55, 1029e1042. Webb, J. N., Szekely, T., Houston, A. I. & McNamara, J. M. 2002. A theoretical analysis of the energetic costs and consequences of parental care decisions. Philosophical Transactions of the Royal Society of London, Series B, 357, 331e340. Weimerskirch, H., Zimmermann, L. & Prince, P. A. 2001. Influence of environmental variability on breeding effort in a longlived seabird, the yellow-nosed albatross. Behavioral Ecology, 12, 22e30. Westneat, D. F. & Sargent, R. C. 1996. Sex and parenting: the effects of sexual conflict and parentage on parental strategies. Trends in Ecology & Evolution, 11, A87eA91. Williams, G. C. 1966. Natural selection costs of reproduction and a refinement of Lack’s principle. American Naturalist, 100, 687e690.
Nest tending increases reproductive success, sometimes: environmental effects on paternal care and mate choice in flagfish REB ECC A E. H ALE & COLET TE M. ST M AR Y
Department of Zoology, University of Florida, Gainesville (Received 23 February 2006; initial acceptance 22 April 2006; final acceptance 18 December 2006; published online 20 August 2007; MS. number: A10371)
Parents should adjust parental care if the costs and benefits of that care vary. Traditionally, the benefit of care has been assumed to be increased offspring fitness, yet increasing evidence indicates that care can also increase mating success. We examined male behaviour and reproductive success across environments in flagfish, Jordanella floridae, a pupfish found across a range of salinities in Florida, U.S.A. Care may be more beneficial to offspring in freshwater habitats than in brackish ones. If so, female preferences for care-giving males should be stronger in fresh water. We quantified male behaviour in fresh and brackish water for four populations and examined whether male behaviour influenced the probability of spawning or the number of eggs spawned. A male’s behaviour influenced his reproductive success, but did so differently in fresh and brackish water. In fresh water, the male’s behaviour prior to spawning was a strong predictor of whether or not he would spawn, whereas in brackish water, postspawning behaviour of males predicted additional spawning success. These results suggest that the traits that females use to assess potential mates differ depending on the salinity of the environment. Despite the importance to a male’s spawning success of different activities in different salinities, male behaviour did not differ consistently between salinities. We discuss possible benefits to females of a phenotypically plastic mate choice criterion and examine explanations for why male behaviour does not covary with the strength of sexual selection across environments. The Association for the Study of Animal Behaviour. Published by Elsevier Ltd.
Keywords: behavioural plasticity; courtship; flagfish; Jordanella floridae; mate choice; mating; parental care; parental investment; sexual conflict; sexual selection
The optimal amount of care to provide one’s young reflects a balance between the benefits of care to young and the costs to the parent’s residual reproductive value (e.g. Williams 1966; Sargent & Gross 1993; Webb et al. 2002). Consistent with this model, parents often reduce the care that they provide their offspring when the costs of caring are high (e.g. Brommer et al. 2000; Weimerskirch et al. 2001) and increase care when the benefits are high (Dale et al. 1996; Listøen et al. 2000). These natural selection pressures are not the only factors influencing parental
Correspondence and present address: R. E. Hale, Department of Biological Science, Florida State University, Tallahassee, FL 32306, U.S.A. (email: [email protected]). C. M. St Mary is at the Department of Zoology, University of Florida, Gainesville, FL 32611, U.S.A. 0003e 3472/07/$30.00/0
investment decisions, as an increasing body of work demonstrates that female mating preferences can select for male activity that is likely to improve offspring fitness (Møller & Thornhill 1998; Tallamy 2000; Pampoulie et al. 2004). For example, mating success can be associated with the quality of a potential mate’s nest (Reynolds & Jones 1999), the care that he will provide young (Forsgren ¨ stlund & Ahnesjo¨ 1998; Lindstro¨m et al. 2006) 1997; O and whether he is caring for a current brood (Petersen et al. 2005). Thus, natural and sexual selection can simultaneously influence optimal care. Natural and sexual selection may favour different amounts of care in species in which the choosy sex (e.g. females) is not the care-giving sex (e.g. males) (reviewed in Clutton-Brock 1991), as is the case for many invertebrates, fish and birds (reviews in Andersson 1994; Tallamy 2000).
577 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd.
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Specifically, imposing sexual selection on paternal care predicts an increase in care above the natural selection optima (Kirkpatrick 1985; Hoelzer 1989; Iwasa & Pomiankowski 1999), which can create conflict between the interests of males and females (reviewed in Arnqvist & Rowe 2005). Females should favour males that provide the greatest fitness benefits to offspring, whereas males should balance benefits to offspring against the costs of providing care (e.g. Trivers 1972; Westneat & Sargent 1996). For species distributed across a range of environmental conditions, the strength of this conflict can vary across environments if environmental conditions influence the benefits of care to offspring (Dale et al. 1996). If the strength of female preferences for parental males is correlated with the expected benefit of care to young, then preferences should be stronger in the environments in which care is most beneficial. Variation in care across environments, then, should reflect the changes in benefits to offspring as well as changes in the strength of mating preferences. We examined variation in parental care both within and between populations of flagfish, Jordanella floridae. Care in flagfish is provided entirely by males, who defend nesting territories and guard, clean and fan eggs from multiple females. Male parental behaviour is variable both within (St Mary et al. 2001; Hale et al. 2003) and between (C. M. St Mary, unpublished data) populations, and a component of this variation can be attributed to variation in salinity (St Mary et al. 2001). The benefits of parental care under various salinities are currently unknown. However, previous work suggests that care may be more beneficial in fresh water. Specifically, an increased rate of fungal infection in fresh water appears to reduce survival of unattended embryos (St Mary et al. 2004). Consequently, egg cleaning may be more beneficial in fresh than in brackish water. Furthermore, if egg cleaning is more beneficial to offspring in fresh water, then the strength of mating preferences for nest-tending males should be stronger in fresh water. We examined the effects of salinity on male activity before and after spawning in four populations of flagfish. Flagfish are native to both freshwater and brackish habitats, so we examined the effect of native habitat type on behavioural responses to salinity by observing males from both coastal and inland habitats. Behaviour may differ between populations native to different habitat types because of genetic drift resulting from reproductive isolation. Alternatively, behaviour may differ consistently between habitat types, suggesting adaptation to local conditions. In flagfish, the amount of gene flow across the salinity gradient is unknown. However, the proximity of freshwater habitats in Florida to coastal salt marsh may facilitate gene flow across the salinity gradient within drainages. An effect of native habitat type on behaviour would indicate that gene flow is restricted and that selection regimes differ between salinities. We also examined female mating preferences by determining whether male pre- and postspawning activity was associated with reproductive success. Male flagfish perform nest-tending activities, such as fanning and nest cleaning, prior to spawning (Bonnevier et al. 2003), and
these activities may serve as signals to potential mates of the quality of care that a male will provide young (Tallamy 2000). In addition, females often mate repeatedly with the same male and a male’s behaviour once he has eggs in his nest may influence whether a female will mate with him again (Tallamy 2000). Therefore, we examined male behaviour both before and after spawning, with respect to his initial and subsequent reproductive success. An effect of salinity on reproductive success would indicate that mating tendencies of males and/or females are plastic in response to salinity. An effect of male behaviour on reproductive success would suggest that females dynamically adjust their spawning activity in response to male behaviour. We expected female preferences based on male activity to vary in strength and direction across salinity treatments and populations, and a male’s preference for a particular female and his interest in mating to be similarly correlated with his activity across all treatments in much the same way that we expect courtship to be similar in all treatments. Indeed, field observations indicate that courtship T-circling (Mertz & Barlow 1966) precedes spawning in both inland and coastal populations (R. Hale, personal observation). As a result, we further expected variation across salinities and populations in the association between male behaviour and reproductive success to indicate variation in female mating preferences.
METHODS
Collection and Transportation Fish were collected from four sites in Florida between May and July of 2003 under Florida Fish and Wildlife Conservation Commission Scientific Collector’s Permit number FNC-03-015 U.S. and Fish and Wildlife Service Special Use Permit numbers 58875 and 03008 for St Marks National Wildlife Refuge and number 03 SUP 59 for Merritt Island National Wildlife Refuge. Seine nets, minnow traps and dip nets were used to collect animals. Otter Creek (OC, Levy County) and Miccosukee (MC, MiamiDade County) are inland and freshwater. St Marks (SM, St Marks National Wildlife Refuge, Wakulla County) and Merritt Island (MI, Merritt Island National Wildlife Refuge, Brevard County) are coastal, with freshwater areas in close proximity to brackish areas. Animals were transported to the Florida State University (FSU) campus in Tallahassee, where the experiments were conducted, in insulated coolers. Fish were transferred to 1-m diameter wading pools at the FSU Mission Road Greenhouse, where they experienced the natural daylight cycle. All animals were returned to their native sites within 4 months of collection.
Acclimation and Experiments Responses to salinity in each of the four populations were examined in a factorial design with two native habitat types (coastal and inland) crossed with two salinity treatments (fresh and brackish). Two populations were nested within each native habitat type. Males and females
HALE & ST MARY: PARENTAL CARE AND MATE CHOICE
from each population were acclimated to either 0.2 ppt (hereafter referred to as 0 ppt) or 15 ppt salinity from their native salinity at a rate of 5 ppt every other day such that all animals reached their target salinity treatment on the same day. Fish were then maintained at these salinities for 2 weeks prior to experimentation. Brackish water (15 ppt) was made by mixing Instant Ocean Aquarium Salt (Aquarium Systems, Inc., Mentor, OH, U.S.A.) with well water, whereas the freshwater treatment (0 ppt) consisted of unaltered well water. The experiment was conducted indoors at 28 1 C on a 14:10 h light:dark cycle. Each male was placed in a 37.5litre aquarium with two artificial plants, a carpeted spawning mat and a filter. We placed one female from the same population as the male and that was acclimated to the same salinity in a transparent plastic box within this aquarium, so that water was shared between the box and the aquarium. The female was maintained in the box for 48 h and then released into the aquarium. Twelve OC, nine MC and 11 SM males were observed in each salinity treatment; 10 and 11 MI males were observed in the fresh and brackish treatments, respectively. Twenty-four hours following the release of the female (day 1), we filmed each pair for 20 min and then we inspected each spawning mat for eggs. Daily from day 2 to day 14, each spawning mat was removed and all eggs were counted. Pairs were filmed for 20 min the first day that eggs were observed. All filming took place between 0800 and 1200 hours. Male behaviour was analysed using The Observer Pro 5.0 (Noldus Information Technology, Wageningen, The Netherlands). Each observation was divided between the time spent at or away from the nest, swimming, fanning, following the female, in courtship (T-circling) or spawning. In addition, we recorded frequencies of bites at and away from the nest, chases and spawning events. See Hale et al. (2003) for definitions of these activities. We also recorded instances in which the male followed rather than chased the female, if he remained no more than approximately three body lengths behind the female and swam at approximately the same speed but did not make contact with the female. We measured reproductive success based on whether a pair spawned (spawning success) and the number of eggs that each male received.
Analyses Three composite responses were analysed: number of approaches towards the female (chases plus follows), number of nest-tending activities (bites at the nest plus fanning events) and proportion of time at the nest. We considered male activity to reflect a decision either to perform the activity at a level appropriate to the environment or to not perform the activity at all. Under this assumption, males that did not perform a given activity did so either because they were categorically inactive or because they assessed the environment and decided that ‘no activity’ was optimal. Ideally, we would have evaluated only those males whose activity levels were adjusted to the environment, but this was not possible. As an
alternative, we analysed each composite behavioural response in two ways. First, each response was treated as a binomial response variable with males scored as either showing or not showing the response. The effects of salinity, native habitat type and population on whether or not males showed the response were analysed using logistic regression. Second, the responses were treated as interval data, with the effects of the treatments on the frequency of the responses analysed using log-linear (Poisson) regression. In these analyses, males that did not perform the activity were excluded. Each of these analyses is valuable in our interpretation of male behaviour. The logistic regression evaluates activity as a binomial response and considers whether or not a male performed an activity, regardless of whether he was categorically inactive or he decided that ‘no activity’ was optimal. In contrast, the log-linear regression evaluates the magnitude of activity and considers the male’s energetic investment into the activity. All analyses were conducted using PROC GENMOD in SAS version 8 (SAS Institute, Cary, NC, U.S.A.) using logistic regression for binomial data and log-linear regression for frequency data. For log-linear regressions, a negative binomial error distribution was specified to reduce model deviance. Interaction terms (see below) were removed from full statistical models using backward elimination, if P > 0.10. Main effects of salinity, native habitat type and population (nested within habitat type) were included in all analyses, regardless of the significance of their effect, to consistently remove variance explained by these variables from all analyses. Summary statistics provided in the text and figures are means standard error. We analysed the effects of salinity, native habitat type and population (nested within native habitat type) on male behaviour during a preparental phase and a parental phase. We limited our testing of interaction effects to that between salinity and native habitat type. The preparental phase consisted of day 1 observations of all males that had not spawned in the 24 h since the female was released (73 of 82 males). The parental phase began when eggs were first observed in a nest and parental behaviour was measured from the observation of each male on the first day that eggs were observed (57 of 82 males). We also examined whether a pair’s reproductive success, either the probability of spawning or the number of eggs received, were influenced by male behaviour (either preparental or parental), salinity, native habitat type, population (nested within native habitat type), and all possible two- and three-way interactions between male behaviour, salinity and native habitat type. First, we examined the effect of preparental male behaviour on spawning success and number of eggs received across the entire 14-day trial. Second, we examined the effect of parental male behaviour on spawning success and number of eggs received in the 2 days immediately following the parental observation, because females may continue to spawn with the same male once he has eggs in his nest. In analyses examining the effect of male activity (yes/no) on spawning (yes/no), we included all males for which there were behavioural observations. In analyses examining the
579
580
ANIMAL BEHAVIOUR, 74, 3
Table 1. Effects of preparental behaviour and parental behaviour on reproductive success (spawning success and eggs spawned) of flagfish Spawned (yes/no) Model
Predictor
Preparental behaviour 1 Approaches Salinity Habitat type Population (habitat) 2
3
Nest tending Salinity Habitat type Population (habitat) Tending*salinity At nest Salinity Habitat type Population (habitat)
Parental behaviour 1 Approaches Salinity Habitat type Population (habitat) Approaches*salinity Approaches*habitat 2 Nest tending Salinity Habitat type Population (habitat) Tending*habitat 3
At nest Salinity Habitat type Population (habitat) At nest*salinity
Eggs spawned
df
c2
P
N
c2
P
N
1 1 1 2
0.07 1.07 0.65 8.32
0.79 0.30 0.42 0.016
73
0.18 1.47 0.13 0.48
0.67 0.22 0.72 0.79
30
1 1 1 2 1
1.40 7.43 0.50 9.33 10.83
0.24 0.006 0.480 0.009 0.001
73
1.1 1.59 0.18 0.67
0.29 0.21 0.67 0.72
30
1 1 1 2
0.04 1.37 0.65 8.57
0.85 0.24 0.42 0.014
73
2.07 4.96 0.09 1.09
0.15 0.026 0.76 0.58
35
1 1 1 2 1 1
1.93 6.60 4.41 2.62 4.45 4.03
0.16 0.010 0.036 0.27 0.035 0.045
57
0.19 3.93 0.09 2.77 4.08
0.67 0.047 0.77 0.25 0.043
42
1 1 1 2 1
8.84 1.88 0.53 1.51 4.83
0.003 0.17 0.47 0.47 0.028
57
0.97 0.2 0.09 0.32
0.32 0.65 0.77 0.85
37
1 1 1 2 1
4.47 3.84 1.65 1.82 3.21
0.035 0.050 0.20 0.40 0.07
57
1.42 0.01 0.0 0.85
0.23 0.94 0.96 0.65
37
Population is nested within habitat type. Logistic and log-linear regressions were used to examine effects on whether or not males spawned and the number of eggs received, respectively, as a function of preparental and parental behaviour. Tests of interaction effects were limited to the interaction between behaviour and habitat type, and behaviour and salinity. Interaction terms with P > 0.2 were removed from the statistical models. P values of significant tests are highlighted in bold.
effect of the frequency of activity on the number of eggs spawned, we included only those males that spawned and performed the relevant activity. As a result, sample sizes of the latter analyses were smaller than those of the former analyses (Tables 1 and 2). We first present the results for reproductive success, as these generate predictions for how male behaviour should vary with salinity.
RESULTS
Salinity, Native Habitat Type and Population The effects of salinity, native habitat type and population (nested within habitat type) on reproductive success were evaluated in models that also included male behaviour as independent variables. Preparental and parental behaviour were considered in separate models (Table 1). Only population (nested within habitat type) had a consistent effects on initial spawning success across all three
models (preparental behaviour models, Table 1). Initial spawning success was 54% for Otter Creek, 71% for Miccosukee, 50% for Merritt Island and 91% for St Marks. None of these variables had a consistent effect on whether the pair spawned again after the initial spawning event (parental behaviour models, Table 1). Among males that spawned (57 of 82 males), salinity, native habitat type and population (nested within habitat type) did not influence the number of eggs received over 14 days (mean SE ¼ 49.1 8.9 eggs), the latency to spawn (4.2 0.6 days), or the mean clutch size (11.0 1.5 eggs), estimated as the total number of new eggs observed divided by the number of days on which new eggs were observed for a given male. In addition to the 57 pairs that were observed during the preparental phase and that subsequently spawned, nine pairs spawned on the day that the female was released before a preparental observation could be made. These males necessarily had a shorter latency to spawn than the other males used in our analyses, and they received, on average, nearly twice as many eggs (mean SE ¼ 80.4 34.8 eggs), but had similar mean
HALE & ST MARY: PARENTAL CARE AND MATE CHOICE
Table 2. The effects of salinity, native habitat type (inland versus coastal) and population (nested within habitat type) on preparental behaviour and parental behaviour Performed (yes/no) N
c2
P
N
0.002 0.48 0.046 0.017
73
6.69 0.09 1.08
0.01 0.76 0.58
30
1.07 0.17 7.99
0.30 0.68 0.018
73
5.48 0.01 1.80 16.21
0.019 0.92 0.41 <0.001
27
1 1 2
0.33 0.71 2.46
0.56 0.40 0.29
73
2.20 0.08 0.89
0.14 0.78 0.64
35
Salinity Habitat type Population (habitat) Clutch size
1 1 2 1
0.38 0.01 9.01 1.07
0.54 0.91 0.011 0.3
57
0.22 0.09 1.12 0.01
0.64 0.77 0.58 0.94
42
Nest tending activities
Salinity Habitat type Population (habitat) Clutch size
1 1 2 1
0.0 0.3 1.31 11.19
0.95 0.58 0.52 <0.001
57
1.59 5.20 1.18 3.36
0.21 0.023 0.55 0.067
37
Time at nest
Salinity Habitat type Population (habitat) Habitat*salinity Clutch size
1 1 2 1 1
0.44 1.59 0.15 5.18 8.83
0.51 0.21 0.93 0.022 0.003
57
0.18 2.39 0.30 3.10
0.67 0.12 0.86
41
Variable Preparental behaviour Approaches
Nest tending activities
Time at nest
Parental behaviour Approaches
Predictor
df
c2
Salinity Habitat type Population (habitat) Habitat*salinity Salinity Habitat type Population (habitat) Habitat*salinity Salinity Habitat type Population (habitat)
1 1 2 1
9.5 0.49 6.15 5.67
1 1 2 1
Frequency performed
P
0.078
Population is nested within habitat type. Logistic regression was used to examine the proportion of males that performed the activity. Loglinear regression was used to examine the number of activities performed. Tests of interaction effects were limited to the interaction between habitat type and salinity. Interaction terms with P > 0.2 were removed from the statistical models. P values of significant tests are highlighted in bold.
clutch size (13.8 4.7 eggs). Four of these males were from the Miccosukee site, three from Merritt Island and two from St Marks.
Sexual Selection on Male Behaviour A male’s behaviour influenced his reproductive success, although it did so differently in fresh and brackish water. In fresh water, preparental behaviour was important to spawning success, whereas in brackish water, parental behaviour was important. In fresh water, males that tended their nests during the preparental phase were significantly more likely to spawn than males that did not tend their nests (logistic regression, tending: c21 ¼ 10:88, N ¼ 38, P ¼ 0.001; habitat type: c21 ¼ 0:05, P ¼ 0.82; population (habitat): 2 c1 ¼ 10:57, P ¼ 0.005; Table 1, Fig. 1). If the direct benefits of nest tending are greater in fresh than in brackish water, as we suggest they are (St Mary et al. 2004), then females should increase their preference for tending where the benefit of doing so is greater, particularly if a male’s nest tending during the preparental phase indicates his tending once he has eggs.
In brackish water, preparental behaviour was not related to spawning success (logistic regression: tending: c21 ¼ 2:29, N ¼ 35, P ¼ 0.13; habitat type: c21 ¼ 1:54, P ¼ 0.21; population (habitat): c21 ¼ 1:37, P ¼ 0.51). However, three activities performed during the parental phase were important to subsequent reproductive success. Males that approached the female during the parental phase were more likely to spawn than males that did not approach the female (Table 1, Fig. 2). However, males that approached the female received fewer eggs on average than males that did not approach (Table 1, Fig. 3). Males that spent time at the nest were also more likely to spawn. In both fresh and brackish water, females preferred males that tended the nest during the parental phase, but only if the pair was from a coastal population (Table 1, Fig. 2). We expected that preferences for activities that increase offspring fitness would be stronger in fresh water than in brackish water. Assuming spawning success indicates, in part, female mating preferences (i.e. single male choice test; Wagner 1998; Shackleton et al. 2005) and that nestassociated activities (nest tending and presence at the nest) increase offspring fitness (Klug et al. 2005), then our data offer mixed support for this prediction. Both preparental-phase and parental-phase nest-associated
581
ANIMAL BEHAVIOUR, 74, 3
100 (a)
7
80 60
9
*
*
11
40
11
20 % Spawned
582
0
Inland
Coastal
100
Tended Did not tend
(b) 80 60
12
12 10
8
40 20 0
males, but among males that tended, coastal males tended more. Two activities that did not influence reproductive success were affected by salinity. Among coastal males, preparental nest tending was more frequent in brackish water. In addition, coastal males were more likely than inland males to approach the female during the preparental phase and all males approached the female more often in brackish water (Table 2, Fig. 4a, b). In addition to these treatment effects, male behaviour during the parental phase was influenced by clutch size. The more eggs a male had in his nest during the parental phase, the more likely he was to tend and to spend time at his nest (Table 2, Fig. 6).
Inland
Coastal Native habitat type
Figure 1. Spawning success as a function of preparental behaviour in (a) fresh and (b) brackish water. Numbers above bars indicate the total number of males observed. *P < 0.05.
activities were important to spawning success, but their influences were not always greater in fresh than in brackish water (e.g. males that spent time at the nest during the parental phase were more likely to spawn, but only in brackish water; the opposite of what we expected). Furthermore, in both fresh and brackish water, parentalphase nest tending increased spawning success.
Behavioural Responses to Sexual Selection Based on the effects of male behaviour on spawning success described above, we expected males to be more likely to perform certain activities in the salinities in which those activities increase spawning success. Specifically, we expected nest tending during the preparental phase to be more likely in fresh water, for approaches and presence at the nest during the parental phase to be more likely in brackish water, and for nest tending to be more likely among coastal males. Nearly without exception, these expectations were not met. Preparental nest tending was not more likely in fresh water (Table 2, Fig. 4d) nor were parental-phase approaches and nest tending more likely in brackish water (Table 2, Fig. 5a). Furthermore, males were not more likely to spend time at the nest during the parental phase when in fresh water than when in brackish water (salinity habitat type interaction; Table 2, Fig. 5e). Finally, coastal males were not more likely to tend the nest during the parental phase than were the inland
Association between Preparental and Parental Behaviour The decision to spawn with a male based on his nest tending before spawning may offer a female direct benefits if such nest tending directly increases success of offspring subsequently spawned and reared in the nest, or if the male’s activity towards an empty nest indicates his care of a future brood. We used log-linear and logistic regressions to determine whether the frequency or probability, respectively, of male preparental behaviour is a good indicator of male parental behaviour. In the analyses of the probability of performing a particular activity, we included all males that spawned, and we examined the effects of all two- and three-way interactions between salinity, native habitat type and day 1 male behaviour (preparental behaviour) on male behaviour on the first day that the male had eggs (parental behaviour). In the analyses of the frequency of activities, we included only males that performed the activity during the preparental phase and then subsequently spawned. This greatly reduced sample sizes, precluding the testing of all possible interactions. Therefore, we pooled all males regardless of salinity treatment, native habitat type or population. In general, male activity before spawning did not predict postspawning behaviour (Table 3). Males that spent time at the nest during the preparental phase were equally likely to do so once they had eggs as were males that did not spend time at the nest during the preparental phase. Furthermore, whether or not a male approached the female during the preparental phase did not predict whether he did so once he had eggs. Similarly, whether a male tended the nest during the preparental phase did not predict whether he did so once he had eggs. The number of approaches towards the female, the frequency of nest tending and the time spent at the nest during the preparental phase also did not predict the male’s performance of these activities once he had eggs.
DISCUSSION
Female Mating Preferences We found no evidence that the tendency to spawn is plastic in response to salinity, as there was no main effect
HALE & ST MARY: PARENTAL CARE AND MATE CHOICE
100
Fresh water (a)
10
2
8
80
5
40
20
20
100
Inland
80
100
9 7
*
40
20
20
80
Inland
100 1
Inland
Coastal
(f)
At nest
40
40
20
20
Coastal Native habitat type
0
11
*
Not at nest 12
60
Inland
*
11
6
80 6
60
0
Tended Did not tend
4
0
Coastal 11
7
(d)
11
40
(e)
*
12
Coastal
80 60
100
3 Inland
3
6
60
0
*
5
0
Coastal
(c)
12
Approached Did not approach
60
40
0
Brackish water (b)
80
60
% Spawned
100
*
3 6
Inland
Coastal Native habitat type
Figure 2. Spawning success as a function of parental behaviour of flagfish in fresh and brackish water, respectively: (a, b) approach female, (c, d) tend nest and (e, f) spend time at nest. Numbers above bars indicate the total number of males observed. *P < 0.05.
of salinity, native habitat type, or their interaction on reproductive success. However, we found evidence that sexual selection on male behaviour varies across salinities and that selection on preparental behaviour differs from selection on parental behaviour, indicating that females use male parental care behaviour to assess mates and that they adjust their mating activity in response to salinity and the presence of eggs in a male’s nest. In fresh water, where the benefits of care are expected to be greater (St Mary et al. 2004), males that tended nests during the preparental phase had higher spawning success than males that did not tend nests. In brackish water, activity during the parental phase influenced reproductive success; males that approached the female and that spent time at the nest were more likely to spawn. In both salinities,
coastal males were more likely to spawn if they tended the nest during the parental phase. If spawning success reflects female mating preferences (Wagner 1998; Shackleton et al. 2005), as we suggest it does, then these results indicate that preferences are plastic in response to salinity and that they vary geographically. Females often choose mates based on the quality of their nest sites (Kodric-Brown 1983; Reynolds & Jones 1999) or the care that they will provide young (e.g. Forsgren 1997; ¨ stlund & Ahnesjo¨ 1998), and preferences for these direct O benefits may change as factors defining quality change. For example, Reynolds & Jones (1999) found that, in gobies, Pomatoschistus microps, female preference for males with small, more cryptic nest entrances disappeared under low oxygen conditions, where the importance of water flow
583
ANIMAL BEHAVIOUR, 74, 3
25 20 Eggs received
584
Fresh Brackish 7
15 10 5 0
8 18
24
Approached
Did not approach Male activity
Figure 3. Mean SE number of eggs that a male received as a function of whether the male approached the female and was in fresh or brackish water. Inland and coastal populations were pooled. Sample sizes are given above bars.
and egg fanning to offspring survival may outweigh the benefit of reduced nest predation. Nest tending in flagfish appears to reduce predation (Klug et al. 2005) and may reduce fungal infection (via the removal of infected egg or detritus from the nest). We found that females were more likely to spawn with males that tended nests before spawning, but only in fresh water. The relative importance of removing detritus may be low in brackish water, where the rates of fungal infection are lower (St Mary et al. 2004), such that preparental tending is a less reliable indicator of offspring survival in this environment. If preparental nest tending is an indicator to females of direct benefits for offspring, then we might expect preparental nest tending to be correlated with nest tending after spawning, but this was not the case. An alternative adaptive explanation is that preparental nest tending may have immediate effects on the nest itself that influence survival of eggs once they are laid such that preparental nest tending indicates hatching success. Indeed, removal of detritus from the nest prior to spawning may reduce fungal infection throughout embryo development (Cote & Gross 1993), because the spores of at least some oomycetes (e.g. Saprolegnia) are attracted to dead material (Smith et al. 1985). Females may also choose mates based on the amount they are courted. For example, female green swordtails, Xiphophorus helleri, are more likely to respond to males that perform courtship displays than they are to males performing other activities (Rosenthal et al. 1996), and similar preferences for courtship displays have been demonstrated in insects and birds (reviewed in Andersson 1994). In flagfish, males that approached the female in brackish water were more likely to spawn than males that did not approach the female. Rates of fungal infection are low in brackish water, so females may shift their choice criterion from male activity that may improve offspring fitness to activity that indicates a male’s eagerness to spawn, such as whether or not a male approaches. We have argued that females may be more likely to spawn with males that show nest tending before spawning because of the direct benefits that nest tending offers.
An alternative explanation is that females do not choose mates based on the direct benefits of parental care but on the indirect, genetic benefits to their offspring (reviewed in Andersson 1994). Females can improve the fitness of their offspring by selecting males of higher genetic quality (e.g. Parker 2003), and in flagfish, male behaviour may indicate male quality. If the energetic costs of activity vary with salinity, so might the reliability of male behaviour as an indicator of quality. In fresh water, where the energetic costs of nest tending may be higher (Evans 1993, see below), male nest tending before spawning may be a better indicator of male quality than it is in brackish water, where all males, regardless of condition or genetic quality, may be able to tend nests. However, while this explanation holds for the pattern in fresh water, it cannot explain the advantage of postspawning nest tending in brackish water. Regardless of the type of benefit that females gain from their decisions, our results suggest that female reproductive decisions are plastic not only in the magnitude, and possibly the direction, of preference but also in the traits used to select mates. In addition, female preferences changed after spawning. These changes may reflect that females make different decisions when assessing males with versus without eggs, when assessing a male for the first time versus reassessing him after already spawning with him, or when assessing a male after a period of not spawning versus after having recently spawned. These three possibilities were confounded in our experiment but potentially reflect different mate choice decisions.
Male Behaviour Our results clearly indicate a sexual selection advantage of preparental nest tending in fresh water, whereas this advantage was not present in brackish water. Given this, and our understanding of how salinity influences embryo hatching success and adult metabolism, we would expect male nest tending to vary with salinity. However, males were not more likely to tend nests in fresh water, and coastal males actually tended nests more in brackish water. Coastal males may have tended nests less in fresh than in brackish water as a result of negative effects of a novel environment, yet this is not entirely consistent with our results. If a novel salinity environment were to elicit such a response, we would expect to see effects of salinity on female fecundity, a measure that we expect to be tightly linked with energy expenditure and metabolic rate. However, there were no effects of salinity or native habitat type on clutch size, total eggs laid, or latency to spawn. Our results also indicate an advantage of approaching the female during the parental phase for inland males in brackish water. However, males were not more likely to approach and did not approach more in brackish water, suggesting that relatively strong sexual selection in brackish water does not entirely explain plasticity in approach activity. Similarly, both coastal and inland males were favoured if they tended the nest in brackish water, but
HALE & ST MARY: PARENTAL CARE AND MATE CHOICE
Fresh Brackish
% Males
80
* 17
60
18 20
40 20
19
0 100
Inland
% Males
60 17
18 19
20
20
100
Inland
9
8
*
8 6
2
4
11
2
40
Inland
Coastal
(d)
35 30
*
25
8
20 6
15 10
7
6
5 Inland
Coastal
(f)
12
17 18
19
20
20
% Time at nest
% Males
*
10
14
(e)
60
0
12
0
Coastal
80
40
(b)
14
45
80
0
16
0
Coastal
(c)
40
Number of approaches
18
(a)
Number of tending activities
100
10
9
8 9 6
9
8
4 2
Inland
Coastal
Native habitat type
0
Inland
Coastal
Native habitat type
Figure 4. Preparental behaviour of male flagfish (i.e. observed on day 1). (a) Proportion of males that made advances towards the female. (b) Number of approaches towards the female, excluding males that did not approach. (c) Proportion of males that tended nests. (d) Number of nest-tending activities performed by males, excluding males that did not tend. (e) Proportion of males that spent time at the nest. (f) Percentage of time that males spent at the nest, excluding males that spent no time at the nest. Means and SEs were calculated from lntransformed values and backtransformed for the figures. In (a), (c) and (e), the numbers above the bars are the total number of males observed. In (b), (d) and (f), the numbers indicate sample sizes and equal the number of males observed in (a), (c) and (e) that performed the activity. *P < 0.05.
they were not more likely to tend the nest in brackish water, despite the mating advantage. There are at least two possible explanations for why plasticity in male behaviour did not mirror plasticity in female mating preferences: (1) responses to salinity are the direct consequence of metabolic processes or (2) male behaviour reflects a balance of the fitness consequences across environments. We reject the first hypothesis because there were no consistent effects of salinity on behaviour either before or after spawning; although preparental males approached the female more in brackish water, no other male activities showed the same pattern. Our results are consistent with the second
hypothesis. This hypothesis requires that the increased offspring fitness and sexual selection benefits in fresh water be balanced by the increased energetic or opportunity costs of care in fresh water, and thus, that the optimum level of male care remains constant across environments. Energetic costs of care may, indeed, be higher in fresh water than in brackish water. Metabolic costs often vary with salinity as a result of the effect of salinity on osmoregulatory demands. For example, in euryhaline fish, those that tolerate a broad range of salinities, metabolic rate often increases as a function of the gradient between environmental and plasma ion concentrations
585
ANIMAL BEHAVIOUR, 74, 3
15
17 13
60 40 20 0
100
Inland
80
15
12
% Males
17 60
13
40 20 0 100
Inland
8
13
40 20
10
12
10 5
Inland
Coastal
(d)
* Habitat
150
11 120 90 60 7
30
9
11
Inland
Coastal
(f)
Fresh Brackish
60
12 17
0
15
70
* 15
12
0
Coastal
(e)
80 60
20
180
(c)
(b)
0
Coastal
Number of tending activities
% Males
80
12
Number of approaches
25
(a)
% Time at nest
100
% Males
586
11
50 40 30 20
12
7
11
10 Inland
Coastal
Native habitat type
0
Inland
Coastal
Native habitat type
Figure 5. Parental behaviour of male flagfish (i.e. observed on the first day of eggs). (a) Proportion of males that made advances towards the female. (b) Number of approaches towards the female, excluding males that did not approach. (c) Proportion of males that tended nests. (d) Number of nest-tending activities performed by males, excluding those that did not tend. (e) Proportion of males that spent time at the nest. (f) Percentage of time that males spent at the nest, excluding males that spent no time at the nest. Means and SEs were calculated from ln-transformed values and backtransformed for the figures. In (a), (c) and (e), the numbers above the bars are the total of males observed. In (b), (d) and (f), the numbers indicate sample sizes and equal the number of males observed in (a), (c) and (e) that performed the activity. *P < 0.05.
(Nordlie 1978; Evans 1993). In flagfish, plasma ion concentrations correspond to approximately 10e15 ppt (Nordlie & Walsh 1989), suggesting that osmoregulatory costs may be higher in fresh water than in brackish water. These osmoregulatory costs may translate into different costs of parental care through two mechanisms. First, care may be more costly in fresh water because of direct physiological costs or constraints. If the costs of osmoregulation are higher in fresh water, then the costs of sustaining parental care activity may also be higher. Furthermore, fish already sustaining high metabolic rates for osmoregulation may not be able to increase their metabolic rates sufficiently
to provide care (i.e. narrower metabolic scope). Second, higher energetic demands of osmoregulation may make it more costly to forgo foraging to provide care. Whether such costs vary with salinity in flagfish has yet to be measured, but data from other species suggest that the effect of salinity on metabolic rate varies widely (e.g. Brocksen & Cole 1972; Muir & Niimi 1972; Moser & Hettler 1989; Claireaux & Lagardere 1999). We expect sexual selection benefits to covary with the direct benefits of care to offspring, whereas the costs of care may vary independently. In this system, the parental costs, direct benefits and the sexual selection benefits of
HALE & ST MARY: PARENTAL CARE AND MATE CHOICE
% Males nest tending
(a) 100 80
across salinities, being stronger in fresh water, where costs and benefits are both high. To our knowledge, variation in the strength of sexual conflict across populations has not been measured (Arnqvist & Rowe 2005), but we suggest that a system in which the benefits of care vary across environments offers a good opportunity to describe such variation because the direct benefits of choosing a good parent as a mate should also vary.
4
4
7 42
60 40 20
Acknowledgments 0
1–10
11–20
21–40
41–60
4
4
21–40
41–60
(b)
% Males at nest
100 80
We thank Joe Travis, Jane Brockmann, Craig Osenberg, Alice Winn, Shirley Baker and the laboratories of C. St Mary, C. Osenberg and B. Bolker for discussion of the data and comments on the manuscript. Sheryl Soucy-Lubell, Becky Fuller, Margaret Gunzburger and Jessica Draughton helped with collection of animals and data. In addition, the judges of the 2005 ABS Allee Symposium provided useful criticisms of the manuscript. Animal care and use procedures were approved by both the University of Florida IACUC and Florida State University ACUC. This work was supported by a National Science Foundation Doctoral Dissertation Improvement Grant.
7
42
60 40 20 0
1–10
11–20
References
Number of eggs in nest Figure 6. The percentage of males that (a) tended their nests and (b) spent time at their nests as a function of the number of eggs in the nest. Bin size ranges for egg number are not constant. Numbers above bars indicate the number of males in that bin.
care may all positively covary such that environments with relatively high benefits also have relatively high costs. A consequence of this covariance may be that the strength of sexual conflict over paternal care is variable Table 3. The relationships between preparental and parental male activity Performed (yes/no)
Frequency performed
Predictor
df
c2
Approaches Salinity Habitat type Population (habitat)
1 1 1 2
0.61 2.95 0.07 0.05
0.43 47 0.22 0.96 21 0.09 0.79 0.09
Nest tending Salinity Habitat type Population (habitat)
1 1 1 2
2.29 0.70 0.28 0.08
0.13 47 0.04 0.84 20 0.40 0.60 0.96
At nest Salinity Habitat type Population (habitat)
1 1 1 2
3.07 0.04 63.00 0.13
0.08 47 0.17 0.68 23 0.83 0.43 0.94
P
N
c2
P
N
Population is nested within habitat type. Logistic regression was used to examine the proportion of males that performed the activity. Loglinear regression was used to examine the number of activities performed, with males pooled across treatments.
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