Consequences of homeothermic capacity of nestlings on parental care in the European starling

USDA National Wildlife Research Center From the SelectedWorks of Larry Clark 1984 Consequences of homeothermic capacity of nestlings on parental care in the European starling Larry Clark Available at: https://works.bepress.com/larry_clark/115/

Oecologia (Berlin) 65:387-393 Oecologia 9 Springer-Verlag 1984 Consequences of homeothermic capacity of nestlings on parental care in the european starling L. Clark* Department of Biology, University of Pennsylvania, Philadelphia, PA 1914, USA Summary. The homeothermic capacity of chicks varied as a function of brood size, age, and air temperature. Commitment to brooding by parents also varied as a function of brood size, age of the young brooded, and prevailing air temperature. It was experimentally determined that parents altered their brooding commitment in direct response to the achieved mean homeothermic capacity of the brood rather than energy demands of the brood per se. Because larger broods achieved a given level of homeothermic capacity earlier than smaller broods, parents spent less time brooding larger broods. This "freed" time represented an increase in potential foraging time by the parents. However, there was no evidence that parents used this potential increased foraging time to elevate the energy return to the nestlings. Other possible advantages of a facultative brooding response by parents are discussed. Atricial young begin life as ectothermic-poikioltherms then undergo a rapid physiological transition to endothermichomeothermy. The ability of chicks to maintain body temperature (Tb) against a thermal gradient is initially due to thermal inertia, then subsequently to an increased capacity for thermogenesis and increased insulation (King and Farner 1961; Dawson and Hudson 197; Dunn 1975; Marsh 1979, 198). Prior to achieving a thermal independence (endothermic-homeothermy) altricial young are frequently brooded by their parents. Brooding functions to externally supply the heat energy necessary to maintain a high, constant T b for the chicks. This is important since physiological properties of the young, such as metabolism, digestive efficiency, and rapid growth are temperature sensitive (Brody 1945; King and Farner 1961). Hence, brooding behavior is presumably the result of selection pressure to provide a temperature environment which optimizes the rates of physiologic processes at a time when the chicks are incapable of doing so for themselves. Parents decrease their brooding commitment to the young as the chicks grow older and the homeothermic capacity of chicks improves and/or the energy requirements of the chicks increases (Hudec and Folk 1961 ; Morton and Carey 197; Askenmo 1977; Korpimaki 1978). However, workers have been unable to determine precisely the proximate mechanisms responsible for this pattern. Recently, * Present address: Monell Chemical Senses Center, 35 Market Street, Philadelphia, PA 1914, USA more attention has been directed towards the ontogeny of homeothermy and endothermy under ecologically realistic conditions. Chicks exist in the wild within a nest and with broodmates. This may substantially alter the heat flux characteristics of individuals, thereby affecting the onset of homeothermy (O'Connor 1975a, b; Dunn 1976, 1979; Clark and Balda 1981; Clark 1982). For example, in nestling starlings (Sturnus vulgaris) of the same age, chicks within a brood of seven will attain a given level of homeothermy at least four days earlier than chicks within a brood of three when exposed to similar environmental conditions (Clark 1982). Nest placement in the habitat by parents may further influence the heat flux of chicks (sensu Walsberg and King 1978). To the extent that brooding takes time from foraging, a conflict may exist for the allocation of parental behavior (Wittenberger 1982; Johnson and Best 1982). Brooding presumably minimizes the risk of death by exposure for young whose capacity for endogenously regulating T b is poor. But parents must also gather food adequate to support their own maintenance needs as well as those of their chicks. Whether or not these requirements together may exceed the capacity of the parents to fulfill them under certain conditions has not been demonstrated for altricial birds. The focus of this study is to determine to what extent starlings alter the allocation of parental care in response to food demand and homeothermic capacity of chicks. Natural variation in brood size, associated with variation in the onset of homeothermy provides an excellent opportunity to address the question of brooding and feeding commitment, and serves to shed light on mechanisms by which some brood sizes are more productive. The question of whether some conditions alter the limits of parental care or whether the evolution of the development pattern of chicks was affected by such time limitation considerations is to be addressed elsewhere. Materials and methods Laboratory experiments Handling of young. I obtained starling nestlings from two source colonies of 9 nest boxes each. Individually marked chicks of known age were removed from nest boxes ca. 45 rain prior to dusk and transported to a field laboratory at the Stroud Water Research Center, Avondale, PA in 198 and Waterloo Mills Research Station in 1981. Transport to the laboratory took between 2 and 45 rain. I kept

388 1.,,, i,,. ~-"-'"S?" Table 1. Least squares regressions for homeothermic capacity vs T, for ages 1-6 and brood sizes 1, 3, 5, and 7. SE is one standard error. Equations are pictured in Fig. 1 '~.6 I- I O l-.2 II I- = 1. E I--.6 a O ~1. "I- o O.2 I.'/" 1 DAY / I ' I I ~ I I / I J".,," i".j.1" / /.., /"./" //I 2 DAYS 1 i.../ 3 DAYS 4 DAYS 1 1 1 1 1 1 l l l l l t.-~-.- -:::....~/f'". 1""...I j--" 5 DAYS" 6 DAYS" I i i I I I i 1'5 2'5 3 5 5 1'5 2'5 3 5 AIR TEMPERATURE (~ ]Fig. 1. The regression lines for the laboratory derived data on homeothermic capacity of nestling starlings. The mean homeothermic capacity of broods is plotted against air temperature outside the nest box. Brood sizes tested were 1, 3, 5, and 7 for the first six days after hatching (day =hatching day). An index value of 1. represents no change in body temperature from the beginning to end of the trial chicks in styrofoam hamburger containers to prevent excessive cooling during their transport to the laboratory. At the laboratory I fed chicks a mixture of canned dog food, whole wheat bread, and cottage cheese until they were replete, after which the chicks were kept under a brooding lamp until used for metabolic trials. For metabolic trials I randomly assigned chicks of the same age to broods of one, three, five, and seven. Individuals always began each metabolic trial with a T b between 38 and 4 ~ C. I recorded initial proventricular T b of chicks to the nearest.5 ~ C using a Yellow Springs Instrument thermistor and recorder in 198 and copperconstantan thermocouple connected to an Omega model 141 mv recorder with cold junction compensator (+_.5 ~ C) in 1981. Both temperature probes were calibrated in a water bath against a mercury thermometer with calibration traceable to the National Bureau of Standards (USA). I placed chicks into natural nests constructed of dried grass and wooden nest boxes. The nest boxes used were identical to those used by starlings at the field sites. The nest boxes were 28.8 x 19.2 x 19.2 cm in dimension, constructed of 1.8 cm exterior grade plywood. Inside edges of the nest box were sealed with ceramic cement, while the lip of the box was lined with silicone and pliable rubber. When sealed the nest box was air tight. Air input through the box was via a.6 cm diameter hole centered 2.4 cm above the nest in the wall opposite the exit port. I placed each box with a brood into an environmental cabinet maintained at a constant T a. Trials lasted 6 min. The air temperature range at which chicks were tested was between 6.5 and 34 ~ C. Individual broods were usually exposed to four trials within a five hour period. After each Age Size Slope SE Int SE R 2 p < 1 1.18.13.7,312.161.196 3.29.7.13.161.526.4 5.35.5 -.18.138.64.1 7.12,4.564.8.439.14 2 1.33.11 --,157.252.68.23 3.19.3.43.67.681.1 5.21.3,393.74.689.1 7.8.4.75.75.48.64 3 1.32.7 --.153.163.671.1 3.2.4.357.95.537.1 5.6.3.828.6.242.63 7.2.2.94.44.117.276 4 1.25,4.197.88.85.1 3.1,1.676.32.662.1 5 --.9,9 1.111.211.78.315 7.1.1.952.16.299.12 5 1.25.5.252.125.653.1 3.7.2.785.36.465.1 5.3.1.912.34.239.4 7,3.2.966.45.27.151 6 1,18.4.461.95.499.1 3.4.1.918.3.234.12 5.3.2.928.34.156.51 7.6.1.944.24.914.11 trial I removed the nest boxes from the cabinet and recorded the positions and T b of the chicks within the nests. At this time I fed the chicks until they were replete. If a chick's T b was below 38~ it was rewarmed under a brooding lamp until its T b was between 38 and 4 ~ C. Broods were then tested at the next lowest T~. The approximate decrease in T, for successive trials was 7 ~ C. Estimation ofhomeothermic capacity. The ability of an individual to maintain T b independent of T, is a measure of homeothermic capacity for that individual. I measured the mean homeothermic capacity of a brood as Hc=T.r-T, To-To where T s was the mean final proventricular temperature (~ of individuals within a brood, To was the mean initial proventricular temperature of individuals within a brood, and T, was the air temperature outside the nest box entrance. An index value of 1. represents a fully achieved level of homeothermic capacity. The relationship between HC and T. for ages 1-6 is summarized in Fig. 1 and Table 1. These data were collected in conjunction with metabolic data and are discussed more fully in Clark (1982). Field observations and experiments Nest attendance. Adult starlings were observed during sampling periods of 1-2 h from dawn to dusk at the Stroud Water Research Center in Avondale, PA. Birds were colormarked for individual recognition either by plastic patagial

389 tags attached to their wings, or by colored plastic leg bands. The former provided the most reliable method for quick identification. A total of 221 nest-hours of observation were logged for the four years of the study. In each observation period I recorded the number of visits adults made as well as the duration of each visit. Visits were timed to the nearest second using a stop watch. The prevailing shaded air temperature outside the nest box, wind, precipitation, and cloud cover were recorded for each observation. I recorded the sex of adults for 97 h of observation. Adults were considered to be brooding if they remained within the nest box for more than 3 s. Prior to an adult's attendance temperatures of the inner surface of nest cups containing young less than six days of age ranged as low as 2-5~ above air temperatures outside the nest box. Thermocouple probes placed within the inner surface of the nest cup recorded a dramatic increase in cup temperature 3 s after a parent entered the box. Once the adult had been in attendance for more than 3 s, nest cup temperatures ranged between 3-34 ~ C. Similar observations have been reported by Westerterp et al. (1982). I manipulated the size of broods to either one, three, five, or seven nestlings within the first few hours after hatching (day ). This usually required cross-fostering chicks to obtain a uniformly aged brood of initially similar weights. There were no apparent differences in growth and survivorship between foster and native chicks (Clark 1983). Broods comprised of equal aged young simulated conditions used in laboratory studies on the development of endothermy and homeothermy of nestlings (above). My own time constraints precluded me from gathering sufficient behavioral observations on broods of one and seven. Therefore I restricted the bulk of the behavioral analysis to brood sizes of three and five though I report the homeothermic capacity of all brood sizes. Nest boxes. In 198 I compared the percentage of time parents brooded young to the weight gains of nestlings for brood sizes three and five under two conditions (boxes heated and not heated). Heated boxes were maintained at 3-33~ C by use of electrical heating tapes (95 W, Fisher Scientific) and thermostats (Hovabator). Nine boxes were equipped with heaters. One was not used by starlings and two were destroyed by predators. Three boxes each were used for broods of three and five. Five unheated nest boxes for each brood size were used as controls. The maximum difference in the age of chicks among the experimental nest treatments was one day. Thus all chicks experienced the same overall environmental conditions, differing only in brood size, or nest box treatment effects. Analysis. Parametric statistical analyses were performed using the General Linear Model procedures of the Statistical Analysis System (Helwig and Council 1979) or procedures outlined in Sokal and Rohlf (1981). Nonparametric staffstics used were those outlined in Conover (198). Unless otherwise noted, the comparisons of means or regression coefficients were tested and found to be homogeneous. Where no F values are given for tests of regression coefficients, significance was evaluated at the 5 percent experimental error rate using the minimum significance difference estimate of Gabriel (Sokal and Rohlf 1981). uo 1 i -i t AGE t (DAYS) t Fig. 2. The residuals of the percentage of time parents brooded their young for broods of three (open bars) and five (solid bars). Residuals were generated by factoring out air temperature effects on parental brooding behavior. See text for further discussion on interpretation of pattern. Length of bar is _+ 1 standard error of the mean (horizontal bar). For each age, brood sizes were compared using a t-test (see text for explanation). * is P<.5. <** P<.1 Results Brooding as a function of age, air temperature, and brood size. The total time chicks were brooded during the day was significantly correlated with the prevailing air temperature. For broods of three, the proportion of time parents were in attendance of the chicks (PTB) was described by the regression equation, PTB=-.2 [TO]+.59, R 2=.355, P<.1. Parents attending broods of five were less responsive to variation in air temperature than were parents attending broods of three (comparison of slopes, P<.5, Sokal and Rohif 1981). For broods of five, the relationship was, PTB -- -.1 [To] +.255, R 2 =.62, P =.54. I used the residuals derived from the above regression equations for broods of three and five to look for brood size and age effects in PTB while controlling for T o. Brood size and age represent significant unexplained variance in PTB. How this unexplained variance is partitioned is of interest: specifically, after T a is controlled how do parents raising broods of three and five differ in the amount of time they brood chicks as a function of the chicks' age (ca. development and inertial effects)? Analysis of the pattern of residuals derived from the regression of PTB on T, addresses this issue. A multiple regression of the full model or a two-way analysis of variance on the residuals of PTB was deemed inappropriate because the data were highly heteroscedatic with respect to age (P<.1). This was primarily due to decreasing variance about PTB as the parents ceased brooding older chicks. Therefore, each age was analyzed separately and differences in PTB between broods of three and five for each age class were determined using a t-test. There was no difference in the residuals of PTB for broods of three and five at day one (Fig. 2). Parents spent significantly less time attending broods of five for ages two through five (Fig. 2). In general, parents stopped brooding broods of five when chicks were three days of age and ceased brooding broods of three when chicks were six days of age. Brooding as a function of homeothermic capacity. I tested the hypothesis that parents adjusted the percentage of time t

39.8.7 O O,6 GI 9 Ul o o 12,mOrt.5 o o o9 P-='4 o o o I.- 9 o oo z r e o,~ o ~... o o IJJ co 9 o. o,:, o o ~ o o o % o ~.o..1 o @ 9 o o.4.5.6.7.8.9 1. HOMEOTHERMIC CAPACITY Fig. 3. The percentage of time parents brooded young as a function of homeothermic capacity of the young. Open circles represent values for broods of three, Solid circles are for broods of five. The line is the common fitted regression for HC values less than.9. The large open circle represents 19 observations for broods of three. The large solid circle represents 2 observations for broods of five chicks were brooded (PTB) as the mean homeothermic capacity (HC) of the brood improved. PTB was obtained via direct observation (see above). However, I estimated the value of HC of chicks in the field using the relationships found in Table 1 and Fig. 1. For brood sizes of three and five two linear regressions were simultaneously fit to the data to determine the value of HC above which the PTB was independent of HC, and below which there was an inverse relationship between PTB and HC. The models were run iteratively for values of HC until the criterion condition was met. The criterion for best fit of the two regressions was a minimization of the sum of the mean square error terms for the two models. For both brood sizes the PTB was independent of HC when values for HC were above.9 (P>.1). PTB was linearly dependent on homeothermic capacity for laboratory derived values of HC below.9 (PTB = - 1.29[HC] + 1.15, R 2 =.599, P<.1, Fig. 3). PTB did not differ between broods of three and five for HC values less than.9. Analysis of covariance indicated broods of three and five shared a common slope (F~,T1 =.19, P =.66) and had the same elevation (F~,71 =.16, P =.69). Thus, parents altered the proportion of time they brooded young in response to the homeothermic capacity of chicks rather than age or brood size, per se. Parents of larger broods may spend less time brooding their offspring and spend more time foraging to meet the higher energy demands required for growth. To distinguish between the HC and the energetic hypotheses I experimentally controlled for air temperature effects on the brooding behavior of parents. I used electrical heating tapes and thermostats to maintain temperatures within heated nest boxes between 3-33 ~ C. At this range of T, both brood sizes possessed equivalent homeothermic capacities over all ages (Fig. I). If parents were altering brooding behavior in response to factors other than HC, i.e. energy demand of the brood, parents brooding five chicks in heated boxes w a ee. #1 W I- p. ;r ILl o n- Ill 7 5O 1 1 + BROOD SIZE 3 o HEATED 9 NOT HEATED 2 3 4 5 6 7 18 AGE (DAYS) + BROOD SIZE 5 Fig. 4. The percentage of time parents brooded young for heated (n = 3) and unheated boxes (n = 5). The verticle bars are +_ 1 standard error of the mean. Where no bar is shown standard error values were too small to represent '7 IZ "r 2 r 15 l- et) > 1 I J,. m 5 2: i I i,, i j 4' BROOD SIZE 3 i, z, i, 1 2 3 4 5 6 AGE (DAYS) i i i i i BROOD SIZE 5 o _-o'" HEATED 9 NOT HEATED o,,,,,, Fig. 5. The number of visits per hour made by parents for broods from heated and unheated nest boxes would be expected to attend their chicks less than parents attending broods of three in heated boxes. There was no difference between broods sizes for PTB (P>.1). In the heated boxes parents initially spent less than five percent of the time brooding chicks and quickly ceased brooding altogether, This was much less than the initial 8 percent for control nests (Fig. 4). Therefore, the percentage of time chicks were brooded was a function of the homeothermic capacity of the brood and not energy demand associated with differences in brood size or age. Benefits to the young. Since parents adjusted their brooding time as a function of the homeothermic capacity of the young it remained to be determined whether or not the chicks benefitted from the increase in potential foraging time by parents brought about by the early realization of a full homeothermic capacity of the chicks. I tested whether the number of visits made by parents feeding young housed in heated boxes was higher than the number of visits made by parents rearing young in control boxes. No differences existed between the number of visits for heated and unheated boxes for either broods of three or five (Fa,36 =.15, P=.98; F1,36 =.11, P=.98, respectively, Fig. 5). The number of visits is only a crude measure of parental care and is insensitive to variation in the amount of food

o Z P, ;'~ BROOD SIZE 3 I-O ~ NOT HEATED 9 ] '1" 6-~'~o e o. HEATED o [ I LLI BROOD SIZE 5 >.4 1.-. t ~, <.A.3 o " "" m.2 o Ix O. 1 /~..~,~, ~ ~, ~/~ ~, ~, ~,,-,_ ~ -'r--~,'.-,--. o- -ty~l'~ 5 1 15 AGE (DAYS) Fig. 6. The average relative weight gain per day for chicks from heated and unheated nest boxes brought by parents per foraging trip. Parents released from brooding constraints may spend more time foraging for larger food items, thereby increasing the energy return per trip (e.g. Royama 1966, Howe 1979, Wittenberger 1982). Therefore, I tested whether or not the relative daily weight gains of young were higher for young raised in heated nest boxes. No significant differences were found between the heated and control treatments for either brood size (BS 3 P>.1, BS 5 P>.1, Wilcoxon Sign Rank Test, a onetailed test, where the hypothesis was weight gain of chicks in heated boxes was greater than weight gain by chicks in control boxes, Fig. 6). Also, for each brood size, the young within broods raised in heated boxes fledged within the range of weights of the young raised in control boxes (for BS 3 mean weights--77.2, 75.7; BS 5 mean weights= 71.8, 73.2 grams for heated and controls, respectively). Therefore, under the environmental conditions prevailing during this experiment the young did not derive any benefit (in terms of weight gain or number of feeding visits by the parents) from any potential increase in parental foraging time. Discussion The development of homeothermic capacity by chicks can have several consequences for parental care. Young with poorly developed thermoregulatory responses to heat or cold stress rely on the shading or brooding behavior of adults for maintenance of normothermic body temperatures. This period of thermal dependence by chicks on adult behavior is often for only a brief portion of the total nestling period in altricial breeding systems. Parents must allocate their care to conflicting activities, such as attendance of young and foraging. Depending on the prevailing climatic conditions the behavioral option a parent chooses could conceivably influence the growth characteristics of the young, the overall energy balance of the young or parent, and/or the probability of survivorship for the young or parent. Study of the interactions of prevailing environmental conditions during breeding, developmental patterns of chicks, and parental care patterns, contains within it two basic levels of questions: 1) What are the short-term limits to reproduction and to parental care patterns?, and 2) How 391 is the evolution of life history traits influenced? It is the former that provides insight into the mechanisms by which natural selection can favor specific life history characteristics. Homeothermic capacity of young. Development of the mean homeothermic capacity of brood members varied as a function of brood size, age of chicks, and ambient temperature. As chicks grow older their tissues become more capable of producing sufficient heat for temperature regulation via shivering thermogenesis (Dawson and Evans 1957). For isolated individuals of altricial species tested in the laboratory, the ability to endogenously regulate Tb is preceded by a period of one-six days where chicks must rely primarily on 1)thermal inertia, 2)a limited metabolic heat production, and 3) the magnitude of the thermal gradient to maintain a relatively constant T b (Marsh 1979, 198). Insulation from feathers in unimportant at this time since an effective covering does not exist until well after the development of endothermic capabilities (e.g. Dyer 1968; Clark 1978). In starlings, visible shivering thermogenesis does not begin until approximately five-six days post-hatching. Further, isolated individuals do not demonstrate maximum endothermic responses to temperature gradients until 12-14 days post-hatching (Ricklefs and Webb 1984). Full dorsal feather cover is not achieved until eight-ten days post-hatching. The effectiveness by which nestlings in the wild can maintain T b is increased somewhat by the nature of their nesting environment. Heat loss is retarded by being in a insulative nest with broodmates. Also, the huddling behavior of chicks effectively increases their thermal inertia. For example, the homeothermic capacity of brood sizes of five at three days of age is approximately equal to HC of broods of three at five days of age for a given T,. These findings are based on HC values derived from broods where the chicks were of equal age. Asynchrony of the age of chicks within a brood may make comparisons of HC based on brood size more difficult. However, since the homeothermic capacity of chicks is initially due to inertial effects and not thermogenesis, mass can be used as an effective predictor of HC (see Clark 1982). Parental brooding commitment. Parents altered their brooding commitment to young as a function of the mean homeothermic capacity achieved by chicks within broods. This change in parental brooding commitment is in addition to, and independent of, changes in PTB brought about by energy requirements of the broods and maturational effects on thermogenesis by brood members. Three lines of evidence support this interpretation. First, prior to the onset of shivering thermogenesis by individual brood members, the PTB afforded young of broods of three and five differed. Broods of five possessed a larger thermal inertia, and were brooded less for a specified age of chicks and environmental air temperature. A brood of three and five may differ in age and to some extent weight, but if the HC values are similar, values for PTB will also be similar. Second, the PTB for broods of three and five from heated boxes were similar over all ages whereas those from controls differed. Third, when gross differences in energy consumption by broods was controlled by looking at PTB within a brood size for heated and control nest boxes, parents reduced their brooding commitment to chicks within heated boxes.

392 Of what significance are attendance patterns? Differences in the rate of mean weight gain for experimental and control broods may reflect the overall ability of parents to provide food for their young. Further, weights at fledging may be a good indicator determining whether tradeoffs exist, since fledging weight may represent a future survivorship probability of the nestling (Perrins 1965, Fretwell 1969). Within brood sizes, parents freed from brooding commitments (heated boxes) did not use this "extra" time to increase the number of feeding visits to the young or bring more food to the younger per visit (as reflected in absolute and relative weight gains of chicks from heated and control boxes). Nor did chicks from heated boxes fledge at heavier weights than those fledged from controls. While generally unsupportive of the notion that chicks indirectly benefit from potential increased foraging time of parents, these results must be viewed with caution. The prevaihng environmental conditions during the course of these observations in 198 may not have been severe enough to see trends in the directions indicated. Larger sample sizes over a wider range of air temperatures are needed before definitive statements about derived benefits to the young of parental brooding commitments can be made. Any potential increase in foraging time by parents may have been offset by the increased maintenance energy costs for the chicks left unattended. This is unlikely. Young for the developmental ages considered are not effective at endogenously generating heat for temperature regulation. Within the first six days after hatching broods of five have hourly maintenance metabolisms zero to ten percent higher than broods of three, all other environmental factors being equal. Even under the least favorable environmental conditions this additional energetic cost amounts to less than two percent of an individual chick's gross hourly energy intake (based on values obtained in Clark 1983). Further, the larger total energy requirements of broods of five (in terms of growth) may have offset any potential gains provided by parents via extra foraging commitment. However, even when brood size was controlled and the achieved level of HC was artificially manipulated there was still no benefit to young in terms of food return or achieved weight gain. The question remains as to whether or not the observed parental attendance patterns have any other potential advantages to reproduction or survival. Parents brooding larger brood sizes may use increases in potential foraging time to forage for themselves in an effort to offset the higher energetic costs of reproduction associated with raising larger broods. By feeding larger broods more frequently, adults must spend more time and energy in transit to and from foraging sites. This direct cost to the parents, of time and energy, may affect the parents' probability of survivorship and/or future fecundity. Weight loss by parents during breeding has been cited as evidence of a cost to reproduction (Howe 1979; Hails and Bryant 1979; however, see Freed 1981). Time budgets obtained for marked adults rearing young in heated boxes indicated that adults used the "freed" time to increase time spent in foraging activity and transit. The increased foraging effort by parents did not yield direct energy benefits to their young. The increase in transit time to foraging areas allowed parents to exploit sites further away from their nests. These distant sites were often frequented by nonbreeding birds but only occasionally by breeding birds. I was unable to gather sufficient data for within brood size comparisons of adult weights for heated and control boxes. Therefore I have no direct measure of the cost of reproduction of adults. Patterns of parental attendance of the young may directly influence the probability of survivorship of the nestlings. Yarbrough (197) suggested that birds nesting in environments where cold stress is a significant factor in nestling mortality might be selectively favored to possess a minimum brood size. Yarbrough cited evidence that broods of fewer than three gray-crowned rosy finches (Leucosticte tephrocotis griseonucha) were seldom known to survive. Clark and Gabaldon (1979) reported similar findings for the pinyon jay (Gymnorhinus cyanocephalus). These findings suggest that broods must possess a minimum degree of thermal inertia to enhance the chicks' probability of survival when they are left unattended for long periods of time in cold or cool weather. The potential for conflict in the allocation of parental care (whether a parent should brood or forage) is dependent on prevailing weather and foraging conditions as well as the intrinsic energy and brooding requirements of young among different brood sizes. The critical period just after hatching is often brief, being less than five days for starlings which have a nestling period totaling 19-22 days. The first five days post-hatching are indeed critical. For passerines in general over one-half of the total mortality of nestlings occurs before 5% of the nestling period has transpired (Ricklefs 1969; Askenmo 1977; Korpimaki 1978). In starlings, 8-9% of the total mortality occurs by this time, 6-7% occurs by five days post-hatching, and 5% by three days post-hatching (Ricklefs and Peters 1979, Clark 1983). In his four year study, Clark (1983) found that about equal proportions of mortality were due to hypothermia, starvation, and predation. However, all but one death due to hypothermia occurred prior to five days post-hatching. Starvation and predation were more evenly distributed throughout the nestling period. These observations are consistent with the notion that selection acts strongly upon parents to accurately assess the tradeoffs between feeding and brooding young if they are to optimize their reproductive output. The interaction of parental care, brood size, and mortality patterns is an important issue that will lead to clearer understanding of the evolution of clutch size. Acknowledgements. K. Baker, K. Derrikson, T. Dickenson, A.N. Gilbert, D. Miles, W. Moise, and R.E. Ricklefs provided valuable comments on an earlier draft of this paper. I thank R. Vannote and the staff of the Philadelphia Academy of Natural Sciences at the Stroud Water Research Center for permission to use their facilities. This research was supported in part by grants from the Frank M. Chapman Fund of the American Museum of Natural History and the Harris Foundation. This work represents research done in partial fulfillment of a doctoral dissertation in Biology at the University of Pennsylvania. References Askenmo C (1977) Effects of addition and removal of nestlings on nestling weight, nestling survival, and female weight loss in the Pied Flycatcher, Fidedula hypoeua (Pallus). Ornis Scand 8:1-8 Brody S (1945) Bioenergetics and Growth. Hafner Press, New York Clark L (1978) Bioenergetics of nestling Pifion Jays. Masters Thesis. Northern Arizona University, Flagstaff Clark L (1982) The development of effective homeothermy and

393 endothermy by nestling starlings. Comp Biochem Physiol 73A: 253-26 Clark L (I983) Constraints on reproduction and parental care in the European Starling, Sturnus vulgaris. Ph. D. dissertation, University of Pennsylvania, Philadelphia Clark L, Gabaldon DJ (1979) Nest desertion by the Pifion Jay. Auk 96: 796-798 Clark L, Balda RP (1981) The development of effective homeothermy and endothermy by nestling Pifion Jays. Auk 98:615-619 Conover WJ (198) Practical Nonparametrical Statistics. Wiley and Sons, Inc., New York Dawson WR, Evans FC (1957) Relation of growth and development to temperature regulation in nestling field and chipping sparrows. Physiol Zool 3: 313-327 Dawson WR, Hudson JW (197) Birds. In G.C. Whittow (ed), Comparative Physiology of Thermoregulation, vol. 1:223-31. Academic Press, New York Dunn EH (1975) The timing of endothermy in the development of altricial birds. Condor 77: 288-293 Dunn EH (1976) The relationship between brood size and age of effective homeothermy in nestling House Wrens. Wilson Bull 88 : 478-482 Dunn EH (1979) Age of effective homeothermy in nestling Tree Swallows according to brood size. Wilson Bull 91 : 455~456 Dyer MI (1968) Respiratory metabolism studies on red-wing blackbird nestlings. Can J Zool 46:223-233 Freed LA (1981) Loss of mass in breeding wrens: stress or adaptation? Ecology 62: I t 79-1186 Fretwell SD (1969) Dominance behavior and winter habitat distribution in juncos (Junco hyemaiis). Bird Banding 4:1-25 Hails C J, Bryant BM (1979) Reproductive energetics of a free living bird. J Animal Ecol 48:471-482 Helwig J, Council KA (1979) Statistical Analysis Systems User's Guide. Raleigh, NC Howe HS (1979) Evolutionary aspects of parental care in the Common Grackle, Quisalus quiseula. Evolution 33:41-51 Hudec K, Folk C (1961) Postnatal development in the Starling (Sturnus vulgaris) under natural conditions. Folia Zool 1: 35-33 Johnson ET, Best LB (1982) Factors affecting feeding and brooding of Gray Catbird nestlings. Auk 99:148-156 King JR, Farner DS (1961) Energy metabolism, thermoregulation, and body temperature. In: Marshall AJ (ed) Biology and Comparative Physiology of Birds. vol II. Academic Press, New York, pp 215-288 Korpimaki E (1978) Breeding biology of the Starling (Sturnus vulgaris) in western Finland. Ornis Fenn 55:93-14 Marsh RL (1979) Development of endothermy in nestling Bank Swallows (Riparia riparia). Physiol Zool 52:34-353 Marsh RL (198) Development of temperature regulation in nestling Tree Swallows. Condor 82:461-463 Morton ML, Carey C (197) Growth and the development of endothermy in the Mountain White-crowned Sparrow (Zonotrichia leucophrys oriantha). Physiol Zool 44:/77-189 O'Connor RJ (1975a) Growth and metabolism in nesting passerines. In: Peaker M (ed) Advances in Avian Physiology. Symp Zool Soc Lond 35:277-36 O'Connor RJ (/975b) The influence of brood size upon metabolic rate and body temperature in nestling Blue Tits (Parus caeruleus) and House Sparrows (Passer domesticus). J Zool Lond 175 : 391-43 Perrins CM (1965) Population fluctuations and clutch size in the great tit, Parus major L. J Anita Ecol 34:61-647 Ricklefs RE (1969) An analysis of nesting mortality in birds. Smithsonian Contrib Zool 9 : 1-48 Ricklefs RE, Peters S (1979) Intraspecific variation in the growth rates of nestling European Starlings. Bird Banding 5:338-348 Ricklefs RE, Webb T (1984) Metabolism and development in the European Starling. (in review) Royama T (1966) Factors governing feeding rate, food requirements, and brood size of nestling Great Tits, Parus major. Ibis 18:313-347 Sokal RR, Rohlf FJ (198/) Biometry. Freeman and Co., San Francisco Walsberg GE (1978) Brood size and the use of time and energy by the phainopepla. Ecology 59:147-153 Walsberg GE, King JR (1978) The heat budget of incubating Mountain White-crowned Sparrows (Zonotrichia leucophrys oriantha) in Oregon. Physiol Zool 51:92-/3 Westerterp K, Gortmaker W, Wijngaarden H (1982) An energetic optimum in brood-raising in the starling Sturnus vulgaris: an experimental study. Ardea 7:/53-162 Wittenberger JF (1982) Factors affecting how male and female Bobolinks apportion parental investments. Condor 84:22-39 Yarbrough GC (197) The development of endothermy in nestling Gray-crowned Rosy Finches (Leucosticte tephrocotis griseonucha). Comp Biochem Physiol 34A: 917-925 Received September 24, 1984