Behavioral Ecology Vol. 14 No. 1: 97-102
© 2003 International Society for Behavioral Ecology
Do energetic demands constrain incubation scheduling in a biparental species?
aThe Edward Grey Institute, Zoology Department, South Parks Road, Oxford OXI 3PS, UK b34 Acre EndStreet, Eynsham OX8 1PA, UK cInstitute of Biological and Life Sciences, Graham Kerr Building,University of Glasgow, Glasgow G12 8QQ, UK dScottish Natural Heritage, 2/5 Anderson Place, Edinburgh EH6 5NP, UK eDepartment of Clinical Veterinary Medicine, Madingley Road, Cambridge CB3 0ES, UK
Address correspondence to W. Cresswell. E-mail: will.cresswell{at}zoo.ox.ac.uk.
Received 2 July 2001; revised 2 June 2002; accepted 2 June 2002.
 |
ABSTRACT |
|---|
 TOP ABSTRACT INTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
|---|
The high energetic demands of incubation in birds may be an important ecological factor limiting the evolution of life-history traits, such as clutch size. In biparental species, however, the demands of incubation may not be a major constraint because there may always be sufficient feeding time available for the off-duty bird to regain energy used during an incubation bout. We investigated whether the energetic demands of incubation constrain optimum incubation bout length in a biparental incubator by decreasing the energetic demands of incubation. We put an insulated cup around the lining of semipalmated sandpiper nests so that the rate of cooling of eggs was reduced by 21%. Semipalmated sandpipers responded by increasing their mean incubation bout length of around 11.1 h by about 10%. Bout lengths in unmanipulated natural nests became longer as hatch approached (incubation stage), and this was independent of weather. Bout lengths may have decreased with increasing rainfall and were independent of time of day. The results suggest that bout length in semipalmated sandpipers is constrained by their cumulative energetic expenditure during an incubation bout, and this is determined partly by the high costs of steady-state incubation. The results also suggest that the incubating bird determines the bout length rather than the returning bird. Semipalmated sandpipersmay have maximized incubation bout length to minimize changeovers during incubation because these probably increasepredation risk. Selection to minimize the frequency of changeover may then be a factor contributing to the evolution ofbiparental care and life-history traits in semipalmated sandpipers.
Key words: biparental care, incubation, life history, semipalmated sandpiper.
|
INTRODUCTION |
|---|
|
TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
|---|
The energetic demands of reproduction are important inthe evolution of a particular life-history trait inaspecies(Partridge and Harvey, 1988
). In birds, a major cost of reproduction is the energetic demand of incubation (Piersma and Morrison, 1994), and so, for example, clutch size may be limited by these demands (Thomson et al., 1998). However, even if the energetic demands of incubation are high, they may not necessarily constrain an incubating bird because of adaptations to manage these demands. For example, the energetic demands of incubation can be managed by the use of body reserves (Aldrich and Raveling, 1983; Gabrielsen, 1989; Reed et al., 1995) or by a pattern of incubation scheduling in which any energy used during incubation is regained by foraging bouts off the nest (Andreev, 1999; Haftorn, 1988). Arguably, the most important determinant of whether the energy demands of incubation might act on life-history parameters will be the system of parental care. For example, in biparental species, one parent attending only 50% of the time can maintain 100% incubation (Norton, 1972). The energetic demands of incubation might not then be important if parents can simply increase the proportion of time spent feeding (and therefore the amount of reserves available to allocate during incubation) when not incubating. Biparental species also have much reduced or even negligible egg rewarming costs because the nest is rarely left unattended (Biebach, 1986; Vleck, 1981); therefore, the total energetic demands of incubation may be much less than for uniparental species (Williams, 1996).
Although it is clear from two recent experimental studies that the high energy demands of uniparental incubation can be limiting (Bryan and Bryant, 1999), there have been few experimental studies that explore whether biparental species are also affected by the high costs of incubation (see Reid etal., 2002), that is, studies that demonstrate experimentally that biparental species are not incubating in the way that maximizes the fitness of their eggs because of the high energetic demands of incubation. In this study we investigate whether a biparental species changes its pattern of incubationscheduling in response to a decrease in the energetic demands of incubation. If the species is constrained by the energetic demands of incubation, then we would predict a change in incubation pattern; and, therefore, we can conclude that the energetic demands of incubation can be a factor influencing life-history evolution in biparental species.
How incubation scheduling might change in a biparental species as energetic demands decrease will depend on how parents determine their incubation bout lengths. If the level of energy reserves of the sitting parent determines incubation bout length (the "parental energy threshold model;" see Chaurand and Weimerskirch, 1994), then the length of an incubation bout will increase because any given level of reserves will last longer if energy demands are lower. If, however, the ability to gain energy reserves of the off-duty parent determines incubation bout length, then the length of an incubation bout will decrease because an off-duty bird will have a smaller energy deficit to recover. If the energetic demands of steady-state incubation do not constrain incubation scheduling in biparental species, we would predict no change in incubation scheduling. This might arise because incubation scheduling is optimized for factors other than energetic demands, such as avoiding predators or coordinating changeover, where changeovers occur each day at a particulartime or after a fixed time interval.
In this study we determined whether the energetic demands of incubation affect incubation scheduling by measuring the mean incubation bout length in semipalmated sandpiper Calidris pusilla L. nests (in which demands were experimentally decreased for 2 days) compared with control nests. Semipalmated sandpipers nest on the ground in the arctic (Gratto-Trevor, 1992), and heat loss from eggs because of lowair and ground temperatures is likely to be important (Andreev, 1999). We therefore experimentally decreased the energetic demands of incubation by the addition of insulating lining material to the nest. Also, semipalmated sandpipers have near total nest attendance (Ashkenazie and Safriel, 1979; Gratto-Trevor, 1992), so the energetic demands of egg rewarming can be ignored (see Williams, 1996).
First, we tested these two crucial assumptions: that nest attendance was continuous and that the addition of insulating material reduced the energetic demands of steady-state incubation significantly. Second, we then tested whether mean incubation bout length per nest was independent of treatment. We also examined the cumulative effects of the treatment on incubation length to confirm whether the sitting or the returning bird determines bout length. If the sitting bird determines bout length, then the effects of the treatment will be immediate. However, if the off-duty bird determines bout length, then the effects of treatment on bout length will be delayed. This is because the first returning bird will not have experienced the treatment and so will replace the sitting bird as if there was no treatment. Finally, we examined the effects of time of day, season, and weather on incubation bout scheduling in unmanipulated nests. If the energetic demands of incubation are relatively unimportant, we could expect bout lengths to remain constant and for changeovers to occur at the same time each day. If incubation demands are important, we would expect bout length to increase with better weather conditions and later in the season when unfavorable weather conditions are less likely.
|
METHODS |
|---|
|
TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
|---|
Semipalmated sandpiper nests were studied at Barrow, Alaska (71°19' N, 156°42' E) between 10 June and 4 July 2000. Nests were almost all discovered before clutch completion so their exact completion date was known. In a few cases, nests were found after clutch completion, and the date of clutch completion was estimated as date of hatch minus 21 days, the incubation period we recorded for the study site (n = 3 nests followed through to hatching; see also Gratto-Trevor, 1992
; Sandercock, 1998).
Incubation scheduling was studied at eight pairs of nests (n = 16 nests) selected from a sample of 58 nests according towhether both birds had been caught and marked at the nest, whether the nests were approximately matched according to clutch completion date, and whether pairs of nests were in close proximity to each other (between 10 and 150 m apart). Each nest had a complete clutch of four eggs. Both birds at a nest were caught with a walk-in trap, and standard biometrics were taken: maximum wing chord, tarsus and toe, head and bill, bill, and mass (Prater et al., 1977). Each bird was assigned to a particular sex on the basis of within-pair differences in their bill, and head and bill length, with the bird of the pair with the longer measure being considered the female: this method of sexing is reasonably reliable if both birds of a pair are measured (Gratto and Cooke, 1987; Gratto-Trevor, 1991; Sandercock et al., 1999). In all cases except one, there was a difference in these measurements of at least 0.5mm, and in the single case in which the difference was only 0.1 mm, wing length and tarsus and toe were 3 and 2mmlarger, respectively, in the bird with the longer bill.
Both birds at a nest were ringed with a standard metal ringwith a 10-mm-long x 1.1-mm-diameter glass bead PassiveIntegrated Transponder (PIT tag) epoxyed to the outer surface, with the long axis running parallel with the lower tarsus. The tag and ring were then encircled in a thin strip of colored tape so that individual birds could be recognized. No adverse effects were observed on the birds marked in this way when walking or flying, and of those birds observed (n = 7), all resumed incubation within a few minutes of release.
We fitted each experimental nest with a PIT tag detecting antennae loop (Francis Scientific Instruments, Cambridge, UK) attached to a data logger so that the identity and time that a semipalmated sandpiper marked with a PIT tag spent on the nest was recorded. Fitting of a loop took about 5 min; all birds returned to the nest within a few minutes of the loops being fitted, and there were no detectable adverse effects of the loops on any of the 16 nests. Each loop had an internal diameter of 10 cm and so fitted neatly around the nest cup ofasemipalmated sandpiper nest. Loops were camouflage painted and buried in vegetation. Any PIT tag within about 5cm of the loop was recorded every 15 s, and the identity of any tags recorded in a minute period was logged every minute along with the time. For 12 out of the 16 experimental nests, a flexible-end temperature probe connected to a TinyTalk datalogger (Gemini Dataloggers Ltd, Chichester, UK) was placed in the center of the clutch, allowing the temperature of the nest to be recorded every 30 s. This temperature trace allowed us to determine whether a bird was on the nest independently of the PIT tag. Occasionally, semipalmated sandpipers sat on the nest in a position so that their PIT tags were recorded intermittently. If the nest temperature duringthese periods was above 30°C and clearly above a control temperature trace (see Unattended Nest Temperature below) obtained from a non-nest site, then the sandpiper was considered to be sitting continuously, despite the intermittent PIT tag record. The PIT tag recorders for the four nests without temperature probes gave near complete attendance records, suggesting that all minutes in which a bird was sitting were logged successfully.
The insulation quality of each study nest was experimentally improved for 46–48-h periods by the addition of an expanded polystyrene drinking cup cut down to 5 cm and painted dull brown. The eggs and its lining were removed from the nest, and the cup was placed in the bottom of the nest so the lip of the cup just protruded above the level of the ground. The lining and the eggs were then replaced by placing them inside the polystyrene cup. Addition of the experimental cup to the nest took about 3 min, and the incubating bird returned to the nest within 2 min after addition or removal of the cup in all cases.
To quantitatively assess the impact of the manipulation on the rate at which heat was lost from a nest scrape, the rate of heat loss from artificial scrapes was measured before and after the insertion of a polystyrene cup. Artificial scrapes were used for these experiments to avoid disturbance to breeding birds. Artificial scrape dimensions did not differ from those of real nests (maximum diam of 78 mm ± 1 SE and 80 ± 1: t18 = -1.29, p =.21; depths of 31 ± 1 mm and 31 ± 1 mm: t18 = -0.1, p =.93; lining masses of 4.9 ± 0.1 g and 4.8 ± 0.1 g: t18 = 0.25, p =.81 for real and artificial scrapes, respectively). A ball of Fimo modeling clay (Eberhard Faber, Neumarkt, Germany) with a thermocouple embedded in the center was warmed to 30°C by using a battery-operated heating mat (RadioSpares, Glasgow) and placed in a nest scrape. A 5-cm-thick expanded polystyrene block was placed over the top to minimize convective heat loss, simulating the heat loss from eggs in an attended nest. A TinyTalk datalogger was connected to the thermocouple, allowing the temperature of the ball to be recorded every 10 s as it cooled toward an ambient temperature that was recorded simultaneously. Newton's lawof cooling (egg temperature = ambient temperature + Bexp[-C x time], where B and C are positive fitted constants) was fitted to the cooling curve recorded, a model that provided an excellent fit to the data (mean R2 of.99). The best-fit value of the exponential cooling coefficient C reflects the rate at which the ball cooled down and thus represents therate at which heat was lost from the nest scrape. Identicalprotocol and equipment were used to estimate the value of the cooling coefficient C both before and after the insertion of the insulating cup, and values were compared.
Experiments in which we added the cup to real semipalmated sandpiper nests were performed on two or three pairs of nests simultaneously (only six PIT tag loggers were available) in three periods of 5 days each. One nest of a pair was manipulated for 48 h while the paired nest acted as a control. After 48 h the insulation was removed, and the nest that had formerly acted as the control was manipulated in turn, with the previously manipulated nest acting as a control.There were therefore two types of control operating: first,each nest acted as its own control (within the same nest: with manipulation followed by no manipulation, or the reverse order), and second, each nest had another nearby acting as a concurrent control (simultaneous nests). The experiment was therefore in a matched-pair design so that order effects and differences between nests (e.g., development stage, calendar date, and weather) should not bias the results in any systematic way. After the 4-day experimental period, all manipulations and equipment were removed, and another set of experimental nests was used.
We calculated the duration of an incubation shift (a bout) for each bird of a pair, the time at which any changeover occurred, and whether or not the nest was being manipulated or not from the minute-by-minute records of the PIT tag nest loggers. Mean bout length was then calculated for each bird for all bouts occurring entirely within an experimental manipulation period or a control period. Bouts that overlapped both experimental and control periods or that were incompletely recorded at the beginning and end of logging were disregarded. On some nests, there were battery or download failures for the loggers, and so, some data were missing (e.g., three males were not sampled properly during the experimental periods). Most analyses in this paper use the mean bout length per nest (n = 16), in which the mean of the mean bout length for the male and the female at the nest was calculated (for the validity of pooling and ignoring sex see Effect of Treatment and Table 1).
|
Weather and temperature data were collected in the following ways. Unattended nest temperature was recorded every 30 s by an unshaded probe held just above the ground (as in the real nests that had temperature probes present). Ground temperature was measured every 4 min using a plasterof paris filled Pectoral Sandpiper Calidris melanotus egg (opportunistically obtained from a deserted nest) with a thermistor at its center placed in an artificial scrape in a typical nest site. The egg was then covered with a 25.5-mm deep cap of expanded polystyrene, covered with foil to minimize the effects of solar radiation. Hourly measures of air temperature, wind speed, solar radiation, and rainfall were obtained from the Point Barrow Observatory for the National Oceanic and Atmospheric Administration. Mean values for all weather variables over the 48-h period of treatment or control were used for analyses. Ground temperature was not collected for the first 4 days of the experiments and was estimated from the closely correlated unattended nest temperature: (ground temperature = 0.47 [unattended nest temperature] - 0.19; F1,21 = 174.9, p <.001, R2 =.89).
Statistical analysis
Data were analyzed by using the SPSS statistical program (Norusis, 1990) and according to the method of Sokal and Rohlf (1981). All probabilities quoted are two-tailed. Means and standard errors are quoted in the form mean ± 1 SE. Daily nest survival rates were calculated according to the method of Mayfield (1961) with confidence limits calculated according to the method of Johnson (1979).
|
RESULTS |
|---|
|
TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
|---|
Tests of assumptions
Overall nest attendance
Nest attendance over the observation period was nearly continuous with a nest being unattended on average for 0.5 ± 0.1% of the time (n = 12 nests with both PIT tag detectors and temperature probes) or about 8 min in 12 h. Periods off the nest (apart from during our scheduled nest visits) were almost all 1–2 min in duration and probably mostly due to our unintentional disturbance as we performed other work on the study site. Changeovers between incubating birds at the nest were mostly instantaneous with 84.6% (n = 162 changeovers) occurring within 1 min (i.e., there was no break in attendance recorded), and there was a mean break in incubation of 0.5 ± 0.1 min (n = 16 nest means) per changeover. No changeovers were coincident with our visits to a nest.
Effect of treatment
The rate at which heat was lost from artificial scrapes before the insertion of a cup was similar to the rate of heat loss from a sample of real semipalmated sandpiper scrapes (mean cooling coefficient values of 0.0055 ± 0.0002 and 0.0055 ± 0.0002 for real and artificial scrapes, respectively; t18 = 0.07, p =.94). Therefore, the artificial scrapes used to measure theeffects of the treatment accurately mimicked the thermal properties of real scrapes. The insertion of an expanded polystyrene cup significantly reduced the rate at which heat was lost from a scrape (mean cooling coefficient in artificial scrape with a cup of 0.0043 ± 0.0002, paired t test t11 = 5.1, p<.001). The treatment reduced the rate at which heat waslost from a scrape by approximately 21% on average.
The effect of treatment
There was a significant effect of the experimental treatment on the mean incubation bout length at a nest comparing nests on a matched-pair basis, in which birds incubated on average 55.2 ± 20.4 min or 9.6 ± 3.5% longer with an insulated cup than without the cup. The effect of the treatment was analyzed in a matched-pair format within the same 16 nests, with eight nests receiving treatment before control and eight nests vice versa: mean bout length for experimental nests was 12.0 ± 0.2 h, compared with 11.1 ± 0.3 h for control nests (t15 = 2.7, p =.017). The effect of the treatment was alsoanalyzed in a matched-pair format between pairs of adjacent, concurrent nests giving similar results (Figure 1).
|
The first complete bout length directly after the applied treatment was similar to the last complete bout length of the experimental treatment (matched-pairs t test within nests, t15 = -0.9, p =.37). Therefore, the effects of the manipulation did not become significantly greater as the treatment period progressed; the trend was for bout length to increase later in the period. The effects of themanipulationweresimilar for the two sexes (matched-pairs t test within nests, t10 = -0.7, p =.51, comparing the change in male incubation bout length on treatment with the change in female bout length; note the sample size differs from other analyses because of missing data from males at five nests).
The effects of sex, time of day, and weather on incubation bout length
Females tended to incubate more during the night (81% of midpoints of 13 nest means of female bouts were between 1800 and 0600 h, compared to 31% of 16 nest means for male bouts; 
2 = 7.5, p =.006). Male and female semipalmated sandpipers had similar incubation bout durations at unmanipulated nests (matched-pairs t test, t13 = -0.3, p =.81), with overall mean incubation bout duration of 11.1 ± 0.3 h (n = 29 means from 29 birds at 16 nests, with three males notbeing sampled). Consequently, there was no consistent time of day for changeovers. Incubation bout duration in unmanipulated nests was independent of sex (sex, F1,12 = 0.02, p =.89; controlling for nest, F15,12 = 3.7, p =.014).
Mean incubation bout duration in unmanipulated nests was dependent on stage of incubation (days after clutch completion) and rainfall, although the effect of rainfall is entirely dependent on a single outlying point (Table 1 and Figure 2). Incubation bout duration in unmanipulated nests was not dependent on calendar date, solar radiation, wind speed, or air or ground temperature (Table 1).
|
|
DISCUSSION |
|---|
|
TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
|---|
When we experimentally reduced the energetic demands of incubation by reducing the rate of heat loss from the clutch, semipalmated sandpipers increased their bout lengths by 10%, suggesting that the length of their bouts was constrained by their cumulative energetic expenditure during the bout. This was confirmed by the result that the incubating bird, rather than the returning nonincubating bird, probably determined bout length (because the experimental treatment effect did not result in shorter incubation bouts and was immediate in effect). These results are consistent with the idea that semipalmated sandpipers have a finite amount of reserves, and when these are depleted, the bout length ends. There have been many studies that have shown that parents end their incubation bout when their "hunger levels" or body reserves fall below a certain level (Chaurand and Weimerskirch, 1994
; Haftorn, 1978; Reid et al., 1999; Weathers and Sullivan, 1989; Weimerskirch, 1995). An incubating parent's incubation bout length will then depend on both its cumulative energetic expenditure during the bout and the level of reserves it started the bout with. For example, heavier lapwings Vanellus vanellus and black-tailed godwits Limosa limosa, have longer incubation bouts (Hegyi and Sasvári, 1998).
Our observational results are also partly consistent with the hypothesis that incubation bout length in semipalmated sandpipers is constrained by the costs of incubation. First, semipalmated sandpipers increased the length of their incubation bouts as hatching approached, as has also been reported by Ashkenazie and Safriel (1979). This is consistent with the predictions of models that describe how animals should manage their reserves when foraging returns or energy requirements are unpredictable (Houston et al., 1988, 1993). If there is a relatively small, but fixed probability each day that an individual will not be able to meet its energy demands, then a bird must have energy reserves, otherwise it will starve when it encounters a day of poor feeding or high energy demands. The probability of encountering such a poor day will depend on the number of days in which it can occur; over a 3-week incubation period a sandpiper is likely to encounterapoor day, but in the last few days of incubation theprobability of encountering a poor day will be lower. Therefore, a semipalmated sandpiper may be able to afford torun its reserves down more at the end of incubation and have longer incubation bouts as a consequence. If the probability of a poor day decreases, as might be expected as weather conditions ameliorate through the summer, then wewould also expect bout lengths to increase, but weather conditions actually got worse during the incubation period at our study site. All weather variables were such that the energetic demands of incubation must have increased as hatch approached; at the end of the incubation period it was windier (rs =.45, p =.03), rainier (rs =.40, p =.05), and less sunny (rs =.43, p =.04), and the ground temperature was lower (rs =.60, p =.002; all correlations n = 24 daily means of weather variables with date). However, it is still possible that despite the weather, foraging conditions may have improved through the study period, allowing birds to return with larger reserves, or the thermal properties of the ground or the eggs may have changed, so that energetic demands were lower and bout lengths longer.
Second, we found that as rainfall increased, so incubation bouts decreased. Semipalmated sandpipers incubate in open grassy nest sites, and so the nest environment and the sitting bird are likely to get wet when it is raining, increasing the energetic demands of steady-state incubation and possibly thermoregulation for the bird. Rain might also reduce the foraging efficiency of off-duty birds so they commence incubation shifts with smaller reserves that are depleted morequickly, resulting in shorter shifts. In any case, the significant effect of rainfall is owing to the effect of a single outlier, although there is no biological reason to exclude this outlier from the analysis (see Figure 1B). Also, we did not finda statistically significant effect of air temperature, wind, or solar radiation on bout length. It seems unlikely that weather does not have an effect on the energetic demands ofincubation, but power is limited in our analysis and a type IIerror is likely. Our results with respect to the effects of weather should probably be treated with caution.
Semipalmated sandpipers seemed to be increasing incubation bout length when it was energetically possible to do so. Longer incubation bouts are likely to be advantageous in semipalmated sandpipers for antipredation reasons. Clutch predation is a major cause of breeding failure in semipalmated sandpipers (Gratto-Trevor, 1992; Norton, 1973), and this was also the case in our study: of 43 nests visited morethan once, there was a daily survival rate of 0.99 (95% CL, 0.99–1.0) and a nest survival probability over the 21-day incubation period of 0.91. Semipalmated sandpiper nests are extremely well camouflaged, and unattended clutches survive better than attended clutches (Ashkenazie and Safriel, 1979; Safriel, 1980). The implication is, therefore, that parental behavior in semipalmated sandpipers attracts predators. Sitting birds, however, weave grass above them so that they are very inconspicuous (Ashkenazie and Safriel, 1979). This suggests that changeovers between incubating birds are the time of greatest risk of a predator discovering a nest. Minimizing the frequency of changeovers by increasing bout length may reduce the probability of a predator finding the nest. Our experimentally induced increase in bout length would reduce the number of changeovers throughout the incubation period by about 9%. This difference, although small, seems sufficient for selection to act on semipalmated sandpipers to increase incubation bout length when possible. This study suggests that evolution of a larger clutch in semipalmated sandpipers may be partly limited by predation selection against the short incubation bouts that arise if the energetic demands of incubation increase.
We found that variation in the energetic demands of steady-state incubation influenced the duration of a parent's incubation bout. This suggests that steady-state incubation is a significant energetic cost and therefore may also be an important influence on parental care and mating systems (Ligon, 1999). The evolution of different mating and parental care systems is constrained by both the phylogeny and the ecology of a species (Owens and Bennett, 1997). Determining the ecological constraints that affect a species' parental care should therefore allow us to understand why one species in a family has, for example, uniparental care and a polygamous mating system rather than another with biparental care and a monogamous mating system (Székely and Reynolds, 1995). The question of how a particular parental care system has evolved in one species in a family and not another may then depend on how the energetic demands of incubation vary with respect to the system of parental care. A key part of this question is whether biparental species are actually constrained by the energetic demands of incubation. If the energetic cost of incubation is sufficiently low, a single parent might be able to incubate for enough time to ensure an adequate thermal environment for the development of its embryos, emancipating its partner to seek new mates. Although the evolution of polygamous mating systems may depend mostly on the ability of the emancipated sex to find and successfully breed with additional mates (Emlen and Oring, 1977; Székely and Cuthill, 2000; Székely and Williams, 1995), other ecological constraints, such as the energetic cost of incubation, may determine the viability of uniparental care and, therefore, whether or not uniparental care and mate desertion may evolve from biparental care. In the specific case of semipalmated sandpipers, it may be that predation risk selecting for long incubation bouts may be a factor contributing to the evolution of biparental care in the species.
|
ACKNOWLEDGEMENTS |
|---|
We thank Dave Norton, Dave Ramey, and the Barrow Arctic Science Consortium for invaluable help during fieldwork; Dan Endres of the Point Barrow Observatory for the National Oceanic and Atmospheric Administration; and Thomas Mefford and Ed Dutton of the Climate Monitoring & Diagnostics Laboratory for weather data. We thank Brett Sandercock for helpful comments on an earlier draft. This work was funded by NERC grant GR9/04607 to W.C.
|
REFERENCES |
|---|
|
TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
|---|
Aldrich TW, Raveling DG, 1983. Effects of experience and body weight on incubation behaviour of Canada Geese. Auk 100:670-679.[Web of Science]
Andreev AV, 1999. Energetics and survival of birds in extreme environments. Ostrich 70:13-22.[Web of Science]
Ashkenazie S, Safriel UN, 1979. Breeding cycle and behaviour of the semipalmated sandpiper at Barrow, Alaska. Auk 96:56-67.[Web of Science]
Biebach H, 1986. Energetics of rewarming a clutch in starlings (Sturnus vulgaris). Physiol Zool 59:69-75.
Bryan S, Bryant DM, 1999. Heating nest boxes reveals an energetic constraint on incubation behaviour in great tits, Parus major. Proc RSoc Lond B 266:157-162.
Chaurand T, Weimerskirch H, 1994. Incubation routine, body-mass regulation and egg neglect in the Blue Petrel Halobaena caerulea. Ibis 136:285-290.[CrossRef][Web of Science]
Emlen ST, Oring LW, 1977. Ecology, sexual selection, and the evolution of mating systems. Science 197:215-223.
Gabrielsen GW, 1989. Energy saving in incubating birds. In: Physiology of cold adaptation in birds (Bech C, Reinertsen RE, eds). New York: Plenum Press; 325–328.
Gratto CL, Cooke F, 1987. Geographic variation in the breeding biology of the semipalmated sandpiper. Ornis Scand 18:233-235.[CrossRef]
Gratto-Trevor CL, 1991. Parental care in semipalmated sandpipers Calidris pulsatilla: brood desertion by females. Ibis 133:394-399.[CrossRef][Web of Science]
Gratto-Trevor CL, 1992. The semipalmated sandpiper. In: The birds ofNorth America, No. 6 (Poole A, Stettenheim P, Gill F, eds). Philadelphia: The Academy of Natural Sciences; Washington, D.C.: The American Ornithologists Union.
Haftorn S, 1978. Egg-laying and regulation of egg temperature duringincubation in the goldcrest, Regulus regulus. Ornis Scand 9:2-21.[CrossRef]
Haftorn S, 1988. Incubating female passerines do not let the egg temperature fall below the "physiological zero temperature" during their absences from the nest. Ornis Scand 19:97-110.
Hegyi Z, Sasvári L, 1998. Parental condition and breeding effort in waders. J Anim Ecol 67:41-53.
Houston AI, Clark CW, McNamara JM, Mangel MS, 1988. Dynamic models in behavioural and evolutionary ecology. Nature 332:29-34.[CrossRef]
Houston AI, McNamara JM, Hutchinson JMC, 1993. General results concerning the trade-off between gaining energy and avoiding predation. Phil Trans R Soc Lond Ser B 341:375-397.
Johnson DH, 1979. Estimating nest success: the Mayfield method andan alternative. Auk 96:651-661.[Web of Science]
Ligon JD, 1999. The evolution of avian breeding systems. Oxford: Oxford University Press.
Mayfield H, 1961. Nesting success calculated from exposure. Wilson Bull 73:255-261.
Norton DW, 1972. Incubation schedules of four species of Calidrine sandpipers at Barrow,. Alaska. Condor 74:164-176.
Norton DW, 1973. Ecological energetics of Calidrine sandpipers breeding in northern Alaska (PhD dissertation). Fairbanks, Alaska: University of Alaska.
Norusis MJ, 1990. SPSS/PC+ Advanced statistics, ed. 4.0. Gorinchem: SPSS Ltd.
Owens IPF, Bennett PM, 1997. Variation in mating system among birds: ecological basis revealed by hierarchical comparative analysis of mate desertion. Proc R Soc Lond B 264:1103-1110.
Partridge L, Harvey PH, 1988. The ecological context of life history evolution. Science 24:1449-1455.
Piersma T, Morrison RIG, 1994. Energy expenditure and water turnover of incubating Ruddy Turnstones: high costs under high Arctic conditions. Auk 111:366-376.[Web of Science]
Prater AJ, Marchant JH, Vourinen J, 1977. Guide to the identification and ageing of holarctic waders. Tring, UK: British Trust for Ornithology.
Reed A, Hughes RJ, Gauthier G, 1995. Incubation behaviour and body mass in greater snow geese. Condor 97:993-1001.[CrossRef][Web of Science]
Reid J, Monaghan P, Ruxton GD, 1999. Effect of clutch cooling rate on Starling incubation strategy. Anim Behav 58:1161-1167.[CrossRef][Web of Science][Medline]
Reid JM, Monaghan P, Ruxton GD, 2002. Males matter: the occurrence and consequences of male incubation in starlings (Sturnus vulgaris). Behav Ecol Sociobiol 51:255-261.[CrossRef][Web of Science]
Safriel UN, 1980. The semipalmated sandpiper: reproductive strategies and tactics. Ibis 122:425.
Sandercock BK, 1998. Chronology of nesting events in western and semipalmated sandpipers breeding near the arctic circle. J Field Ornith 69:235-243.
Sandercock BK, Lank DB, Cooke F, 1999. Seasonal declines in the fecundity of arctic-breeding sandpipers: different tactics in two species with an invariant clutch size. J Avian Biol 30:460-468.
Sokal RR, Rohlf FJ, 1981. Biometry. New York: W. H. Freeman and Company.
Székely T, Cuthill IC, 2000. Trade-off between mating opportunities and parental care: brood desertion by female Kentish plovers. Proc R Soc Lond B 267:2087-2092.[Medline]
Székely T, Reynolds JD, 1995. Evolutionary transitions in parental care in shorebirds. Proc R Soc Lond B 262:57-64.
Székely T, Williams TD, 1995. Costs and benefits of brood desertion in female Kentish plovers, Charadrius alexandrinus. Behav Ecol Sociobiol 37:155-161.
Thomson DL, Monaghan P, Furness RW, 1998. The demands of incubation and avian clutch size. Biol Rev 73:293-304.[CrossRef]
Vleck CM, 1981. Energetic cost of incubation in the zebra finch. Condor 83:229-237.[CrossRef][Web of Science]
Weathers WW, Sullivan KA, 1989. Nest attentiveness and egg temperature in the yellow-eyed junco. Condor 91:628-633.[CrossRef][Web of Science]
Weimerskirch H, 1995. Regulation of foraging trips and incubationroutine in male and female wandering albatrosses. Oecologia 102:37-43.[CrossRef][Web of Science]
Williams JB, 1996. Energetics of avian incubation. In: Avian energetics and nutritional ecology (Carey C, ed). New York: Chapman & Hall; 375–415.
CiteULike 
Connotea 
Del.icio.us What's this?
This article has been cited by other articles:
|
|
 |
|
  J. H Perez, D. R Ardia, E. K Chad, and E. D Clotfelter Experimental heating reveals nest temperature affects nestling condition in tree swallows (Tachycineta bicolor) Biol Lett, October 23, 2008; 4(5): 468 - 471. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 M. E. de Heij, A. J. van der Graaf, D. Hafner, and J. M. Tinbergen Metabolic rate of nocturnal incubation in female great tits, Parus major, in relation to clutch size measured in a natural environment J. Exp. Biol., June 1, 2007; 210(11): 2006 - 2012. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 D. R. Ardia and E. D. Clotfelter Individual quality and age affect responses to an energetic constraint in a cavity-nesting bird Behav. Ecol., January 1, 2007; 18(1): 259 - 266. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
W. Cresswell, S. Holt, J. M. Reid, D. P. Whitfield, R. J. Mellanby, D. Norton, and S. Waldron The energetic costs of egg heating constrain incubation attendance but do not determine daily energy expenditure in the pectoral sandpiper Behav. Ecol., May 1, 2004; 15(3): 498 - 507. [Abstract] [Full Text] [PDF]
|
|
| ||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||