The Condor92341-359 8 The CooperOrnithological Society 1990

BREEDING ENERGETICS AND THERMAL ECOLOGY OF THE ACORN IN CENTRAL COASTAL ’

WESLEY W. WEATHERS Department of Avian Sciences,University of California, Davis, CA 95616

WALTER D. KOENIG AND MARK T. STANBACK HastingsNatural History Reservationand Museum of VertebrateZoology, Universityof California, Berkeley, CA 94720

Abstract. We used the doubly labeled water (DLW) technique to measurethe field met- abolic rate (FMR) of adult (n = 4) and nestling (n = 30) Acorn ( formicivorus).Resting metabolic rate (RMR) of adults and nestlingswas calculatedfrom 0, consumption.We constructedthe nestlings’ energybudget from measurementsof the growth rate, FMR, and RMR of different aged nestlings.We measured the body temperature (Tb) of two nestlingsin the field using implanted radiotelemeters,assessed the nestlings’ thermal environment in terms of the air temperature (TA experienced inside and outside of nest cavities, and studied the ontogeny of nestling homeothermy in the laboratory. Adult FMR averaged 195 kJ/day, which is 30% lower than predicted from adult mass (82 g) and 2.7 times the measured basal metabolic rate. Nestling FMR @J/day) increased with mass (m in grams) according to the relation: FMR = -27.1 + 2.4m. Nestling FMR stabilized at about 160 Id/day (82% of the adult level) by 3 weeks of age. Nestlings,which are adult sized when they fledge30-32 daysafter hatching,grow relatively slowly. Their logistic growth rate constant (K = 0.226) is 30% lower than predicted from their massand is equivalent to that of a tropical speciesof their size. Nestlings also develop endothermy much more slowly than expected and are unable to maintain adult 7’, when exposedto 15°C for 30 min until they are 3 weeks old. In the field, nestling T, fluctuated until about 3 weeks of age, apparently due to intermittent brooding by the adults. Nestlings metabolized an average of 3,853 Id/ over the nestling period (age: O-31 days). Of the total, RMR comprised 46.8%, whereas activity, thermoregulation, and the heat increment of feedingcombined accountedfor 40.2%. The energyaccumulated in growth amounted to 50 1 kJ, or 13% of the total. Grossgrowth efficiency(ratio of energyaccumulated in tissue to total metabolized energy) is the lowest reported for any bird. Two factors contribute to low growth efficiency: (1) a slow growth rate, which may result in part from tannins contained in the nestling’s partially acorn diet, and (2) thermostatic costsassociated with a low nest-cavity T,. These unusualphysiological features indicate that energeticcon- straints may play an important role in influencing the costs and benefits of group living in this cooperatively breeding species. Key words: Acorn Woodpecker;doubly labeled water: reproduction;thermoregulation; growth; nestling;body temperature; energy metabolism: Melanerpes formicivorus.

INTRODUCTION viva1 and reproductive successin both California Acorn Woodpeckers (Melanerpes formicivorus) (Koenig and Mumme 1987) and New are unusual for at least two reasons. First, they (Stacey and Koenig 1984) and are an important are cooperativebreeders that live in family groups constraint leading to cooperative breeding in this of up to 15 adults, all of which cooperate in species. Koenig and Mumme (1987) proposed rearing young at a single nest (Koenig and that granary storesconstitute a limited resource Mumme 1987). Second, they depend upon whose importance to survival and reproduction acorns, which they eat as fresh mast in the au- makes nondispersal by offspring virtually oblig- tumn and store, often by the thousands, in spe- atory until such time, if any, that they acquire a cialized storage trees called granaries. Stored breeding position in the population. acornsare critically important to overwinter sur- Although food resourcesmay have thus played a central role in the evolution of cooperative breeding in this species,we lack basic informa- I Received 3 July 1989. Final acceptance3 1 January tion concerningthe energyrequirements of Acorn 1990. Woodpeckers or how they allocate energy to re-

[3411 342 W. W. WEATHERS, W. D. KOENIG AND M. T. STANBACK production. To fill this gap, we report here the of energy &J/day), it represents total heat pro- results of a study of the breeding energeticsand duction (or loss). FMR equals metabolized en- thermal ecology of the Acorn Woodpecker. This ergy (ME) when there is no net synthesisof body work reveals several highly unusual features of tissue (fat, protein, or carbohydrate), or other the physiological ecology of this species,includ- production (e.g., crop milk, or ova). The sum of ing extremely slow nestling growth and remark- FMR and energy retained as growth or produc- ably low growth efficiency. These characteristics tion constitutestotal metabolized energy (TME). reinforce the impression gained from demo- Resting metabolic rate (RMR) is the rate of heat graphic studies of marked individuals (Koenig production (calculated from 0, consumption in and Mumme 1987) that Acorn Woodpeckers are this study) of a fasted measured at rest adapted to conditions of extreme food or nutrient and in the dark during the active phase of its limitation, which are only partly mitigated by daily cycle. RMR increasesat temperatures be- group living and acorn storage. low the lower critical temperature due to ther- moregulatory costs.Basal metabolic rate (BMR) METHODS, STUDY SITE, AND SPECIES is the rate of heat production of resting, fasted We studied the energetics and thermal ecology measuredin the dark within the thermal of adult and nestling Acorn Woodpeckers during neutral zone during the rest phase of their daily the 1985 and 1986 breeding seasons.To accom- cycle. In the absenceof direct measurements, the plish this we (1) monitored the body mass of BMR of adult can be estimated as 0.75 nestlings growing in the field, (2) measured the times the thermoneutral RMR (Aschoffand Pohl resting oxygen consumption of adults and young 1970). Tissue energy (TE) is the total gain (or in the laboratory, (3) assessedthe birds’ thermal loss) of grossenergy contained in body tissue of environment under field conditions in terms of an animal. Gross energy (E) is the energy released the air temperature (TJ experienced inside and as heat when an organic substanceis completely outside of nest cavities, (4) used the doubly la- oxidized to CO, and water. beled water (DLW) technique to measure total daily energy expenditure and water flux of adults NESTLING GROWTH AND DEVELOPMENT and nestlings, (5) measured the body tempera- Growth rate of nestlings was determined by ture of nestlings in the field using implanted ra- weighingknown-aged nestlingsbetween 1975 and diotelemeters, and (6) quantified the ontogeny of 1988. Nestlings were weighed at irregular inter- nestling endothermy under laboratory condi- vals depending on accessibility of nests. Many tions. nestlingswere weighed at intervals of 2 to 3 days, Our study site was on and adjacent to Hastings whereas others were only weighed two or three Natural History Reservation, a 900-ha reserve times during the entire nestling period. Mea- in the upper Carmel Valley, Monterey County, surements were made from day 0 (hatching day) California, where a color-marked population of to day 29, 1 to 3 days prior to fledging. Sample Acorn Woodpeckers has been under continuous sizes for particular agesvaried, but in all, 3,660 study since 197 1 (Koenig and Mumme 1987). A measurements were made on over 300 different description of the reserve, its plant communities, individuals. Only massesof individuals that sur- and climate are available in MacRoberts and vived to 22 days of age, when birds were per- MacRoberts (1976) and Koenig and Mumme manently banded, were included. We photo- (1987). graphed nestlings at different ages to provide a pictorial record of their development. ENERGY TERMS AND CONCEPTS Efforts to standardize usageof energy terms and RESTING METABOLIC RATE (RMR) concepts(e.g., NRC 198 1, Calder 1982) have not Adults. We determined adult basal and ther- met with universal acceptance,owing in part to moregulatory energy requirements (maintenance differing requirements among subdisciplines. metabolism) by measuring fasting oxygen con- Accordingly, we herein describe the terms and sumption (PO,) of four woodpeckers(mean mass: conceptsused in our study. 73.1 g) that rested in the dark at stable ambient Field metabolic rate (FMR) is the rate of CO, temperatures between 0 and 38°C during the ac- production of free-living animals as measured tive phase of their daily cycle. Measurements by the DLW technique. When converted to units were also made on fasted birds at night at 36°C. ACORN WOODPECKER ENERGETICS 343

Between measurements, which were made from FIELD METABOLIC RATE (PMR) 17 May-9 August 1985 and 3-26 May 1986, the birds were housed in outdoor flight aviaries and We used the DLW technique to measure FMR were provided ad libitum with water and kibble- of four adult and 30 nestling woodpeckers. All , dry, dog food (Purina Hi-Pro). All four of the adults were feeding nestlings. Birds were adults maintained massand vigor throughout the captured on their territory, weighed to the near- measurements. est 0.05 g (K-Tron model DS-10 balance) and v02 was determined with an open-circuit res- given an intramuscular injection of water (2.5 pirometry system. Details of the methods, ap- pi/g body mass) containing 97 atoms-percent I80 paratus, and calibration proceduresused in these and ca. 12 MBq 3H per ml. Following injection, measurements are presented elsewhere (Weath- nestlingswere immediately returned to their nest ers et al. 1980). For these determinations, birds for isotopic equilibration, whereas adults were were placed in either 4-1 metal metabolism held in cloth bags. After allowing 1 hr for the chambers lined with paper towels or in a hard- labeled water to reach equilibrium with body ware cloth (wire) cage contained within a 14-1 water, we obtained duplicate 50+1 blood sam- Plexiglas metabolism chamber. In the latter ales from a brachial vein and stored them at 4°C chambers, birds clung to the wire in a normal in flame-sealed glass microhematocrit tubes for upright posture. During the day, lower and more later analysis. The adults were then releasedback stable oxygen consumption rates were obtained onto their territory and the nestlings returned to for birds clinging to the wire cagesthan for birds their nest. Approximately I or 2 days later, the restingon the floor of the 4-l chambers,and hence birds were recaptured, reweighed, and a second we report only the former values. At night both set of duplicate blood samples obtained. The chambers gave comparable values. Body tem- elapsedtime between initial and final blood sam- perature (r,,) was determined at the end of each ples averaged 24.1 + 0.29 hr (range = 23.9-25.5 run by inserting a polyethylene-sheathed ther- hr) for “l-day” samples (n = 30) and 49.0 & mocouple into the cloaca to a depth such that no 1.8 1 hr (range = 47.7-5 1.7 hr) for “2-day” sam- decreasein Tb occurred upon slight withdrawal. ples (n = 4; three of them adults). For nestlings, The thermocouple was calibrated against a mer- the time of initial capture ranged from lo:50 to cury thermometer certified by the National Bu- 18: 10. Becauseall nestlings had time to feed be- reau of Standards. fore capture or recapture, errors due to diurnal Nestlings. The v02 of fasted, nestling wood- variation in gut-fill should be minimal. All nest- peckers resting in the dark during the day was lings within a given brood were given the same determined between 4 May to 3 June 1986 at dose of DLW to minimize error due to their Hastings Reservation. For these measurements, breathing exogenousCO, having a different iso- nestlings were removed from their nest in the topic ratio than that of their body. late morning, taken immediately to the labora- Adult woodpeckersproved to be difficult study tory, and placed in an incubator maintained at subjects. Two of the four adults were initially 36-37°C. They were syringe-fed a semiliquid diet captured at their nests before they fed in the (Gerber’s baby food), returned to the incubator morning. One of these (No. 9) was recaptured for 30 min, and then their thermoregulatory in- the following morning at about 06:40, the other dex (TI) was determined (see below). Following (No. 10) was recaptured 2 days later at 11:27. the TI determinations, they were placed in in- The other two individuals were initially captured dividual felt-lined plastic nest bowls housed at around 13:OOand 17:OOas thev came to their within a 4-l metal metabolism chamber main- nests to feed nestlings. These two individuals tained at 36-37°C. After a 1-hr equilibration pe- were recapturedapproximately 2 dayslater. Thus, riod, nestling v02 was determined using the for one of the four adults, gut-fill may have re- open-circuit apparatus described above. Tbwas sulted in a slight overestimate of mass change determined at the end of the run as for adults. and perhapsa 5% error in FMR. Two of the four VO, measurements began no sooner than 3 hr adults that we measured(a male and female from following the last feeding. For both adults and the same nest) were fitted with radio transmitters nestlings, we converted I’O, to metabolic heat (Biotrack Pty.) to aid in tracking them. A 2-g production assuming that 20.1 kJ of heat were transmitter was glued to the feathers of the fe- produced per liter of 0, consumed. male’s back, while a 4-g transmitter was similarly 344 W. W. WEATHERS, W. D. KOENIG ANDM. T. STANBACK attached to the male’s back. The time budget of because most of our DLW measurements were the female was determined after her releasewith based on 1-day samples,the error attributable to the aid of a Radio Shack model TRS 100 micro- incorporation of isotopesinto tissue is probably computer (P. Hooge, unpubl. data). small. Blood samples were microdistilled (Wood et If nestlingsbreathed CO, exhaled by unlabeled al. 1975, Nagy 1983) to obtain pure water, which birds, which shared the nest cavity with them was assayed for tritium activity (Searle model (e.g., adults or helpers), our DLW estimates of Mark III liquid scintillation counter, toluene- CO, production could be in error. In a test of Triton X 1OO-PPO scintillation cocktail) and for this effect, the DLW method was found to over- oxygen- 18 content by cyclotron-generated pro- estimate CO, production by 18-8 1% when kan- ton activation of ‘80 to fluorine- 18 with subse- garoo rats (Dipodomys merriami) breathed air quent counting of the positron-emitting 18Fin a containing 3.4% unlabeled CO, (Nagy 1980). The Packard Gamma-Rotomatic counting system error varied inversely with absolutehumidity and (Wood et al. 1975: analysesperformed at Crock- directly with ambient CO, concentration. Al- er Nuclear Laboratory, University of California, though we are unable to discount the possibility Davis by W.W.W. or at University of California, of a similar error in our study, Howe et al. (1987) Los Angeles by K. Nagy). Using the equations found a mean CO, concentration of only 0.37% of Lifson and McClintock (1966) as modified by in Northern Flicker (Colaptesauratus) nests. As- Nagy (1975) we calculated rates of water flux suming a similar CO, level in Acorn Woodpecker and CO, production from the isotope measure- nests, little error should attend our measure- ments. ments. Overall, we believe our DLW measure- ments of CO, production for individuals to be POTENTIAL ERRORS within f 10% of actual values. Errors in calculated rates of CO, production us- Energy equivalent of CO,. Calculating energy ing the DLW technique can result from analyti- expenditure from CO, production is problemat- cal errors in the isotope measurements or ical because“ animals are periodic eatersbut con- insufficient isotope turnover (Nagy 1980). Al- tinuous metabolizers” (Baldwin 1968). One must though we did not validate the DLW method know not only the animal’s diet, becausethe en- specifically for woodpeckers, in an earlier vali- ergy equivalent per liter CO, varies by up to 32% dation of our technique using Budgerigars,Mel- of the minimal value (2 1.14 kJ/l) depending on opsittacusundzdatus (Buttemer et al. 1986), DLW the substrate being catabolized (see Gessaman measurementsof CO, production differed by less and Nagy 1988a, Weathers and Sullivan 1989) than 6% from values determined simultaneously but also whether the animal is in material and by the Haldane method (mean difference, energy balance. We estimated the diet of wood- -0.04%). The amount ofisotope turnover which peckersin our study by observing what foraging occurredin our woodpeckerswas consistentwith birds ate, by examining stomach contents, and minimal measurement error (Nagy 1980). Final by neck-collaring nestlings.Based on the first two ‘*O concentration averaged 5 1% of initial I80 methods, the diet of adult woodpeckersconsisted (range = 20-7 1o/o), whereas tritium turnover av- of 3 1% acorns and 69% insects;whereas the diet eraged 83% of I80 turnover (range = 60-89%). of neck-collarednestlings was approximately 25% Errors may attend DLW measurementsof rap- acorns and 75% insects (Koenig, unpubl. data). idly growing animals owing to irreversible and For both groups, we assumed an energy equiv- disproportional incorporation of isotopes into alent of 25.5 kJ/l CO*, which was calculated from body tissue (Nagy 1980, Williams and Nagy the fractional diet composition assuming an en- 1985). Although the extent of the error remains ergy equivalent of approximately 26.5 kJ/l CO, uncertain for Acorn Woodpeckers, Klaassen et for insects(Weathers and Sullivan 1989) and 23.0 al. (1989) validated use of DLW for rapidly grow- kJ/l CO, for acorns. The latter value was cal- ing Arctic Tern chicks (Sterna paradisaea). They culated following the methods of Weathers and found that the DLW technique underestimated Nagy (1984) based on the composition of dry CO, production (measured by indirect calorim- acorns (5.5% protein, 15.5% fat, and 74.0% car- etry) by 4% during the first 24-hr measurement bohydrate; average of Q. lobata, Q. chrysolepis, period. The underestimation increased to 16% and Q. agrzfilia; Koenig and Heck 1988; Koenig, during the second day. Because Acorn Wood- unpubl. data). peckersgrow more slowly than Arctic Terns, and Animals that fail to eat enough to meet their ACORN WOODPECKER ENERGETICS 345 energy needs will metabolize body substance. When the chemical composition of the animal’s diet differs from that of the catabolized body tissue,an error will result if the energy equivalent for CO, based on the diet is used to calculate FMR. The magnitude of the error depends upon the proportion of total CO, that is produced from body tissuevs. dietary sources.In our study, three older nestlings lost between 9.1-12.7% of their initial mass during the measurement period. All other individuals gained or maintained their mass. The fastest growing nestlings exhibited mass increasesof 9-18% per day. What CO, en- ergy equivalent to use for growing nestlings is unclear (for discussion, see Weathers and Sulli- Julian day van 1989). Accordingly, we assumed a value of FIGURE 1. Air temperature at the study site in re- lation to time of vear (Julian day 120 is 30 April). Each 25.5 kJ/l CO, for all birds. If the three nestlings datum depicts the average value for the preceding 5- that lost mass metabolized exclusively body fat 6 days based on 17 years of records (1969-1985, in- (as is typical of older nestlingsundergoing weight clusive).The secondorder polynomial curvesrepresent recession)their calculated FMR would be about least squaresfits describedby equations2, 3, and 4 for maximum (Max), mean, and minimum (Min) tem- 9% too low. peratures,respectively. ONTOGENY OF THERMOREGULATION We examined the developmental changein nest- A’s nest was located 3.6 m above ground in a ling thermoregulatory ability by calculating the 0.29-m diameter limb. Nestling B’s nest was thermoregulatory index (TI): located 7.9 m above ground in a 0.30-m diameter oak limb. A small AM radio receiver taped to TI = 100 (7’” - TJ/( Tad - TJ (1) the tree limb outside the nest chamber received where T,, and Tadare the body temperature of the Minimitter signal. The pulse signal was con- nestling and adults, respectively, and T, is the ditioned with a comparator circuit and recorded ambient temperature to which both are exposed with a Campbell 21 x micrologger. Air temper- (seeO ’Connor 1984, Ricklefs 1987). TI, the per- ature within the nest cavity was measured with centage of the adult temperature gradient a Cu-Cn thermocouple that was placed high achieved by young exposed to a cold challenge, enough above the nestlings to avoid contact with was determined for individual nestlings and for the brooding adult(s). Air temperature outside nestlings in broods of four. For these determi- the nest was measured with a shaded thermo- nations, nestlings were syringe-fed a semiliquid couple placed about 1 m away from the nest. A diet (Gerber’s baby food), placed in an incubator 2 1 x micrologger monitered the temperatures at 36-37°C for 30 min, and then placed in an once every 10 set and calculatedthe averageevery artificial nest (felt-lined plastic bowl) housed 10 min. The Mini-mitter transmitters were cali- within a 15°C chamber. After 30 min elapsed, brated againsta thermometer certified by the Na- the nestling’s Tbwas determined to within 0. 1°C tional Bureau of Standards immediately before with a Cu-Cn thermocouple connected to a Bai- they were implanted and again after they were ley/Sensortek model Bat- 12 thermocouple ther- removed from the birds. mometer, and TI was calculated assuming adult Tb = 41.2”C. STATISTICS Unless indicated otherwise, data are presented NESTLING BODY TEMPERATURE as mean + 1 SD. Other statistical procedures Between 4-24 May 1986, we remotely moni- used are described below. tored the Tb of two nestlings in the field using abdominally implanted Mini-mitter model X RESULTS transmitters. Both nestlingswere from nestscon- Figure 1 summarizes 17 years of air temperature taining five nestlings and were 9 days old (and measurements at Hastings Reservation for the approximately 36 g) when implanted. Nestling period 1 March-29 June (Julian days 60-180), 346 W. W. WEATHERS, W. D. KOENIG AND M. T. STANBACK

FIGURE 2. Growth and development of nestling Acorn Woodpeckers. Each photograph is of a different individual.

which encompasses the main breeding season. NESTLING GROWTH AND DEVELOPMENT The least squarespolynomial lines fitted to the Brood size is generally three to five, and hatch- data are as follows: lings weigh an average of 4.7 f 0.84 g (n = 187), Max T, = 15.0 - 0.036X + 0.0006X2, or 5.9% of adult mass (80 g). Hatchling Acorn Woodpeckers are very altricial-completely na- r* = 0.964 (2) Mean T, = 9.8 - 0.054X + 0.0006x2, ked and eyelids fused. Their eyes do not open until they are about 10 days old and by 2 weeks r* = 0.966 (3) of age they are still essentially featherless (Fig. Min T, = 5.2 - 0.072X + 0.005X, 2). By 3 weeks of age, nestlings are adult-sized r2 = 0.946 (4) and covered with feathers, although the feathers where X is Julian day. are still in sheaths.Fledging occursin 30-32 days ACORN WOODPECKER ENERGETICS 347

44 42 ,u

i 361 I I I I

FIGURE 3. Nestling Acorn Woodpecker mass in re- 3 lation to age. The solid line connects the means (not shown) of a total of 3,660 measurementson over 300 individual nestlings.The dotted lines enclosethe 95% confidenceinterval.

at a mass of about 80 g. Sexual size dimorphism is slight (Stanback, unpubl. data). For descriptive purposes, and to facilitate comparison of woodpeckerswith other kinds of birds, we fit the nestling mass data (Fig. 3) for ages O-26 days, by three equations: Gompertz, Ambient temperature, “C logistic, and Richards (Ricklefs 1983). The mass FIGURE 4. Body temperature (top) and metabolic data are better fit by the Gompertz equation than heat production (bottom) of four fasted, adult Acorn Woodpeckers (mean mass = 73.1 g) measured in the the logistic equation, as indicated by the former’s dark during the day in relation to ambient temperature. lower residual mean square (Table I), although, Sloping lines are least squares regression lines de- as is often the case, the Gompertz fit overesti- scribedby equation 7 for Tb below 20°C and equation mated the asymptote. The shape parameter (M) 6a for heat production. Different symbols denote dif- of the Richard’s equation indicates that the ferent individuals. Gompertz equation is a somewhat better fit (Ta- ble 1). Nonetheless, all three equations provide good fits and for comparative purposes we will where m(t) is nestling mass at t days of age use the logistic equation to describe Acorn (hatching = day 0) and e is the base of natural Woodpecker growth: logarithms. 82.19 RESTING METABOLIC RATE (RMR) m(t) = (5) 1 + 9.79(@226’) Adults. The metabolic heat production (calcu- lated from VO,) of fastedadult woodpeckersrest- ing in the dark during the day is shown in Figure TABLE 1. Growth curve parameters for the Acorn 4. This plot differs from the typical endotherm Woodpecker. A = asymptote (g), K = growth rate con- pattern in lacking a clearly defined thermoneutral stant (days-l), I = age (days) at the inflection point of the growth curve, MS = residualmean squares(squared zone. Furthermore, the least squares regression deviations). The shape factor M = 1.35 for the Rich- line relating metabolism to Ta extrapolates to ards equation, 2 for the logistic, and 1 for the Gom- zero metabolism at Ta = 7X, far above the pertz. woodpeckers measured T,. RMR (W/kg) in- creased linearly with decreasing T, (“C) as fol- Equation A K I MS lows: Logistic 82.19 0.226 10.10 1.23 Gompertz 89.19 0.135 7.93 0.90 RMR (W/kg) = 27.3 - 0.365T,. (6a) Richards 85.74 0.167 2.66 0.67 Converting RMR to units of Id/day, we have: 348 W. W. WEATHERS, W. D. KOENIG AND M. T. STANBACK

TABLE 2. Metabolic rate of adult Acorn Woodpeck- ers.

Metabolic rate(W/k@ PLY- Condition’ Observed dicta+

Active (a) phase Clinging 13.79 + 2.07 (10) 8.97 154

Rest (p) phase Clinging 10.63 ? 1.05 (4) 7.15 148 oc Standing 9.83 * 0.54 (9) 7.15 137 0 Body mass, grams *Mean T. = 35.6’c; range= 33%38.2T. bValues are reportedas K + SD. cPredicted for a 73.1-g nonpasserinebird by the appropriateequation FIGURE 5. Field metabolic rate (FMR) of nestling of Aschoffand Pohl(l970). (circles)and adult (filled squares)Acorn Woodpeckers, and resting metabolic rate (RMR) of nestlings (filled diamonds) in relation to mass. Lines are least squares RMR &J/day) = 177 - 2.49Ta (6b) regressionlines fitted to the nestlingdata and described (s,_~= 11.32, S, = 0.184, by equation 9 for FMR and equation 8 for RMR. Filled r2 = 0.871, IZ = 30). circlesdenote FMR of three nestlingsmeasured during an especiallycool period. At T,s‘ between 33-38°C VO, was minimal and equivalent to 13.8 W/kg during the day and about tributed to their high FMR. We have no expla- 10.1 W/kg at night (Table 2). During the day, T, nation for the fourth nestling’s high FMR. of adults remained constant (X = 42.4 + 0.8 1; n Adult FMR (Fig. 5; shaded squares) ranged = 17) at T, > 20°C and varied directly with T, from 15 1 to 242 kJ/day (X = 195 f 39.2 kJ/ between 0 to 20°C (Fig. 4). The equation relating day; n = 4) and overlapped the FMR of adult- Tb to T, below 20°C is: sized nestlings.

Tb = 38.0 + 0.22T, (7) WATER CONTENT AND FLUX (r = 0.921, n = 9). The fraction of body mass consisting of water Nestlings. The resting metabolic rate (RMR; (TBW) was determined by oxygen- 18 dilution. Id/day) of fasted nestlings measured at T, = 36- Adult TBW averaged 0.670. Nestling TBW de- 37% during the day (Fig. 5) increased linearly creasedwith mass (m, grams) (Fig. 6) according with body mass (m; grams) as follows: to:

RMR @J/day) = 2.25 + 1.00~ (8) TBW = 0.924 - O.O024m, (10) (s,., = 6.10, sb = 0.039, (s,., = 0.0214, S, = 0.0003, r2 = 0.927, n = 55). r2 = 0.782, n = 26).

FIELD METABOLIC RATE (FMR) Nestling FMR increasedlinearly with body mass (m; grams) (Fig. 5) according to: NESTLING FMR @J/day) = -27.1 + 2.40m (9) (s,., = 21.61, s, = 0.241, r2 = 0.780, n = 30). Four of the older nestlings depicted in Figure 5 had FMR’s that lie considerably above the regressionline. Three of these birds, depicted by shaded circles, were nest mates whose nest tree was located on an exposed ridge top. The FMR FIGURE 6. Fraction of nestling Acorn Woodpecker of thesethree birds was measuredduring a period body mass consistingof water in relation to age. Line of especiallycold and windy weather, and it seems is the least squaresregression line described by equa- likely that increasedthermoregulatory costscon- tion 10. ACORN WOODPECKER ENERGETICS 349

Brood of 4

Nestling body mass, grams FIGURE 7. Field water efflux of nestling Acorn Woodpeckersin relation to mass. Solid line is the least FIGURE 9. Thermoregulatoryindex of nestlingAcorn squaresregression line described by equation 11. Woodpeckersexposed as a brood of four individuals to 15°Cfor 30 min in relation to mass.The leastsquares regressionline is described by equation 13. Total water efllux (TWE, ml/day) of nestlings measured in the field with DLW increased with mass (m, grams) (Fig. 7) according to: ponentially with body mass (m, grams) (Fig. 8) according to: TWE = 6.40 + 0.18m (11) (s,., = 3.37, s, = 0.038, log,,TI = -0.5664 + 1.307 log,,m, (12) r2 = 0.463, n = 30). (log,Gs,, = 0.0891, s,, = 0.0507, r2 = 0.930, n = 52). TWE of four adult woodpeckers (mean mass = The above equation predicts a TI of 50% at 54.1 82.25 g) averaged 29.3 -t 4.27 ml/day, which is 1.38 times the value predicted by equation 11. g mass, which would be attained at about 13.5 days of age, or about 44% of fledging age (31 ONTOGENY OF THERMOREGULATION days). A nestling’s ability to maintain Tb during At hatching, Acorn Woodpeckers are ectother- the cold challenge improved if it was tested in a mic and they become competent thermoregula- brood of four, such that a TI of 50% was attained tors rather slowly. We quantified the develop- about 3 days sooner, at a mass of 43.6 g (Fig. 9). ment of thermoregulatory capacity in terms of The relation between TI and nestling mass was the thermoregulatory index (TI): the percentage linear for 52 individuals tested in broods of four of the adult Tb - T. gradient attained following and can be described as: a 30-min exposure to 15°C (see Methods). The TI = -1.86 + l.l9m, (13) TI of nestlings tested individually increased ex- (s,., = 8.13, sb = 0.051, rz = 0.957).

Nestling mass, grams

Nestling mass, grams FIGURE 8. Thermoregulatoryindex of nestlingAcorn Woodpeckersexposed individually to 15°C for 30 min FIGURE 10. Difference in body temperatureof nest- in relation. to mass. Curved line is the least squares ling Acorn Woodpeckers exposed to 15°C for 30 min regressionline described by equation 12. when in a brood of four vs. when exposedindividually. 350 W. W. WEATHERS, W. D. KOENIG ANDM. T. STANBACK

Time of day

FIGURE 11. Mean 24-hr body temperature(mea- FIGURE 12. Bodytemperature (measured by radio- sured by radiotelemetry)of two free-living Acorn telemetry)of a free-living 15-day-oldnestling Acorn Woodpeckernestlings (represented by differentsym- Woodpecker(triangles), nest temperature (upper solid bols)in relationto age.Curved line fittedby eye. line), and air temperature(lower solid line) in relation to time of day. Verticallines denote the timesof dusk and dawn. The thermal benefit of being in a brood of four is illustrated by plotting the difference in Tb ob- lo-min intervals inside and outside of the two served for each nestling following a 30-min ex- nest cavities that contained telemetered nest- posure to 15°C either singly or with brood mates lings. Over this time period, T, averaged 13.9”C (Fig. 10). In four cases,T,, was higher when cold- (n = 5,016) and nest temperature (T,,) averaged exposedsingly (negative values in Fig. 10). More 17.9”C (n = 4,568). Under these generally cool typically, Tbs’ were higher for nestlings in broods conditions, T,, averaged 3.7”C higher than T,. of four. The thermal advantage of having brood The difference between T,, and Ta was higher at mates was small for nestlings that were lessthan night than during the day (Fig. 12). 40% or more than 60% of fledging age. For nest- DISCUSSION lings of mid-age, Tb was as much as 9.2”C higher when cold-exposed with brood mates. The main breeding season for Acorn Wood- peckers at Hastings Reservation extends from NESTLING BODY TEMPERATURE AND April through June, with the majority of clutches NEST TEMPERATURE being initiated between 15 April and 15 May The mean 24-hr Tb of two free-living nestlings, (Koenig and Mumme 1987). Incubation requires as measured with implanted radiotelemeters, in- 11 days and most nestscontain nestlingsbetween creasedwith age up to about 3 weeks of age and 26 April and 26 May (Julian days 116-l 46). Dur- was constant thereafter (Fig. 11). Lower mean ing this period, the weather at Hastings has yet Tb of younger nestlings was a consequence of to settle into the uniformly balmy days that char- their cooling during periods when adults left the acterize California’s summer. Minimum air tem- nest to forage. This is illustrated in Figure 12, peratures fall below 5°C at night, daytime high which presents 1 day’s Tb record for one of the temperaturesrarely exceed20°C (Fig. l), and cool two nestlings studied (aged 15 days). At night, days with light rain are not uncommon when it was being continuously brooded, the (MacRoberts and MacRoberts 1976, pers. ob- nestling’s Tb was stable and averaged 39.7 f serv.). These generally cool conditions increase 0.39”C. In the morning, the nestling’s T, fell to both adult and nestling energy requirements and about 20°C presumably because the adults left affect several aspectsof the species’ breeding bi- the nest to forage. T, within the nest chamber at ology. this time was about 10°C. The nestling’s T, re- turned to near 40°C at around 06:30, following NESTLING GROWTH the adult’s morning feeding bout. Fluctuations The eggsof woodpeckersare smaller than those in nestling T,, between 1O:OOand 20:00 probably of similar-sized birds, with the exception of the represent variable brooding behavior by the (largely)parasitic Cuculiformes (Rahn et al. 1975). adults. The mean weight of 35 freshly laid Acorn Wood- Between 4-24 May 1986 we measured T, at peckereggs ( 10 different females) was 5.28 g, 90% ACORN WOODPECKER ENERGETICS 351 of the value predicted by the equation TABLE 3. Food items delivered to Acorn Wood- of Rahn et al. (1975) based on a mean female peckernestlings by adults. Data are based on 1,077 hr mass of 78.1 g (Koenig 1980). Thus, the eggsof of feeding watches at 47 nests of 19 different groups between 1979-1982 (Mumme and Koenig, unpubl. Acorn Woodpeckers are small, even by the stan- data). dards of a taxon that lays extremely small eggs.

Acorn Woodpeckersalso have one ofthe shortest No. feedsconsisting of Nestling age No. nest incubation periods of any bird (Rahn and Ar (days) watches acorns insects % acorns 1974) their eggshatching in just 11 days. 1-5 50 55 266 17.1 Despite their extreme altriciality at hatching, 6-10 61 199 735 21.3 nestling Acorn Woodpeckers grow relatively 11-15 56 267 687 28.0 slowly. The growth rate constant K, based on the 16-20 156 306 1,087 22.0 logistic equation (Table l), can be compared with 21-26 71 386 1,499 20.5 26+ 71 402 909 30.7 that of other altricial species,ranging in size from Total 372 1,615 5,183 23.8 small passerinesto large raptors, using Ricklefs’ (1968) regression equation and an asymptotic mass of 82.19 g. Basedon Ricklefs’ equation, the Acorn Woodpecker’s K-value (0.226) is only 69% amounts of tannins (seeKoenig and Heck 1988). of the expectedvalue (0.326) and is close to the Tannins bind proteins (Bate-Smith 1973, Tem- value predicted for tropical species (Ricklefs ple 198 1, Martin and Martin 1982) and depress 1976) which are generally regardedas being slow- the growth rate of domestic chicks when present growing. Slow growth occursin another member in the diet at levels of 0.5% or greater (Vohra et of the genusMelanerpes (seebelow), but it is not al. 1966). Tannins have also been shown to de- a general characteristic of the class Piciformes, press digestibility of acorns by Acorn Wood- as the K-values of other woodpeckersequal those peckers(W. D. Koenig, unpubl.). Extensive ob- expected for altricial birds of their size (R. E. servations of adults feeding nestlings (R. L. Ricklefs, unpubl. data: Dryocopuspileatus K = Mumme and W. D. Koenig, unpubl. data) reveal 0.29-0.33; Picoides borealis K = 0.32; and Pi- that acorn pieces constitute a sizable proportion coidespubescens K = 0.33). of the food items delivered to nestlings (Table Avian growth rates can also be compared in 3). Acorns represent a significantly greater pro- terms of the maximum absolute growth rate (g portion of food items delivered to 1 l- to 1S-day- wet mass/day) calculated at the midpoint of the old and ~26-day-old nestlings than to other ages linear growth phase (i.e., at the inflection point (ANOVA arcsin transformed data: F5,347= 2.4 1; of the growth curve). The inflection point for P = 0.036). Although these data do not reveal Acorn Woodpeckers occursat 10.1 days. At this what fraction of nestling TME derives from time, mass = 40.6 g and absolute growth rate = acorns, they suggestthat the fraction is highest 4.6 wet grams/day. Drent and Daan (1980) sum- when nestlings are growing most rapidly; i.e., at marized absolute growth rate data for altricial 1 l-l 5 days of age. and semiprecocialseabirds and raptors. For these Data available from other melanerpine wood- groups,which grow much slowerthan passerines, peckers suggestthat slow growth may be char- absolutegrowth rate is describedby the equation: acteristic of this taxon. Jackson (1970) docu- (wet g/day) = 0.202 rnO.$‘ where m = adult mass mented growth for a brood of Red-headed in grams. This equation predicts a growth rate Woodpeckers (Melanerpes erythrocephalus). of 5.4 g/day for a bird of the Acorn Woodpecker’s Their growth is best described by the logistic size, a value 1.17 times the observed rate. Al- equation (R. E. Ricklefs, unpubl. data) with a though it may not be appropriate to compare growth rate constant (K = 0.289) that is 88% of woodpeckers with seabirds, these calculations predicted (Ricklefs 1968) based on their asymp- serveto emphasizethat Acorn Woodpeckersgrow totic mass of 80.1 g. Thus, Red-headed Wood- more slowly than most other species. peckersalso grow slowly, although not as slowly Why do Acorn Woodpeckers grow so slowly? as Acorn Woodpeckers. One contributing factor may be the nestlings’ Adult Red-headedWoodpeckers average about diet, which consistsof both insectsand piecesof 90% of the mass of Acorn Woodpeckers (Dun- acorns. Acorns contain relatively little protein ning 1984) and their nestlingsfledge 3 1 days after (3.9 to 7.1% of dry weight) and significant hatching, the same ageas in Acorn Woodpeckers. 352 W. W. WEATHERS, W. D. KOENIG AND M. T. STANBACK

Similarly long nestling periods are suggestedby velop the ability to regulate their T,, very slowly, the data on other temperate melanerpine species even for a slow-growing species. As a conse- compiled by Jackson (1977) and may be even quence, there is a 2-week period, between the longer in some tropical species. For example, time they are l-3 weeks old, when nestlings are Skutch (1969) reported that the young of the relatively large, poorly feathered, and unable to Golden-naped Woodpecker (Melanerpes chrys- effectively maintain Tb when cold-challenged. auchen), which are only about 70% of the mass These characteristicsmake it theoretically pos- of Acorn Woodpeckers in California, fledge at sible for adults to manipulate a nestling’s energy 33-36 days of age. requirements by varying the amount of brooding Melanerpine Woodpeckers frequently feed on that the chick receives. When insectsare limited, low-protein, fruit diets (Short 1982). Thus, slow adults could brood chicks less, thereby permit- growth rates may be a more general adaptation ting them to become hypothermic, which would found within the rather than a trait pe- decreasetheir food needs. Because older nest- culiar to Acorn Woodpeckers and their diet high lings undoubtedly respond to low T, by increas- in acorns. Also worthy of note is the high fre- ing their metabolic heat production, lack of con- quency of unusual social organization within this tinuous brooding coupled with low T, would genus: at least eight of 21 species(38%) recog- increase their energy expenditure. Thus, with- nized by Short (1982) including the Acorn holding brooding to curtail nestling energy de- Woodpecker, are known or probable cooperative mands would be limited to young nestlings in- breeders.Although distinguishing causefrom ef- capableof increasingendogenous heat production fect is problematical, we believe that low-protein in response to low T,. Such a scenario presup- diets, slow growth, and cooperative breeding, poseslow nest-cavity temperatures. three highly unusual traits found regularly within Nest-cavity temperatures during the breeding this genus, are interrelated. seasonat Hastings Reservation are often so low (Fig. 1) that nestlings less than 3 weeks old rap- NESTLING HOMEOTHERMY idly become hypothermic unless they are brood- The age at which individual altricial nestlings ed continuously. For birds in general, the age at attain effective homeothermy (defined arbitrarily which brooding ceasestends to coincide with the as the ability to maintain 75% of the adult T,, - development of effective endothermy (Dunn T, gradient upon exposure to 15-25°C for some 1973). This does not appear to be true for Acorn time period) was summarized for 22 speciesby Woodpeckers, for whom brooding declines al- Dunn (1975) (for an analysis of the cooling meth- most linearly with time after the first 4-5 days od, see Ricklefs 1987). Based on Dunn’s data, of the nestling period (M. T. Stanback, W. D. the age at which effective homeothermy is at- Koenig, and R. L. Mumme, unpubl. data). This tained (Y, days) varies inversely with growth rate is supported by our Tb data for free-living nest- as follows: lings, which indicate that brooding is intermit- tent well before nestlings are capable homeo- Y= 16.6 - 18.8K (14) therms. The average daily T, of free-living (s,.~ = 1.64, sb = 2.45, r2 = 0.747, n = 22), nestlings younger than 2 weeks of age is lower than that of older nestlings (Fig. 11). This is un- where K is the logistic equation growth-rate con- doubtedly due to episodes of hypothermia re- stant. Although equation 14 is derived from a sulting from brooding adults leaving the nest to heterogeneousdata set, it describesthe data well. forage, as was clearly the case at dawn for a 15- For 11 of the speciesconsidered by Dunn, the day-old nestling (Fig. 12). Apparently, the amount observed age at which effective homeothermy of time that adults can devote to brooding is was attained is within 10% of the predicted value, constrained by the adults’ foraging and/or other compared with a mean difference from predicted activity requirements. Thus, one important con- of 16% (range = O-45%) for all 22 species.Equa- tribution of nest helpers is to aid in brooding tion 14 predicts that nestling Acorn Woodpeck- nestlings. ers (K = 0.226) should attain 75% of the adult T,, - T, gradient by 12.4 days of age. The ob- NESTLING ENERGY BUDGET served value, 19.5 days, is 57% greater than pre- In its simplest form, a nestling’s energy budget dicted; the largest departure from predicted yet consistsof the following components of the total observed. Nestling Acorn Woodpeckers thus de- metabolized energy (TME): ACORN WOODPECKER ENERGETICS 353

TME=BMR+HI+TR+A+TE (15) where BMR is the basal metabolic rate (including the costof biosynthesis),HI is the heat increment of feeding (SDA), TR is the cost of thermoreg- ulation, A is the cost of physical activity, and TE is the energy accumulated in tissue (growth). Gross energy intake can be calculated from TME provided assimilation efficiency is known, We used our metabolism and growth data to calculate the nestlings’ energy budget (see Ap- pendix 1). The increase in TME with age was Nestling age, days sigmoidal (Fig. 13) with TME reaching 90% of FIGURE 13. Energy expenditure of nestling Acorn its asymptotic value (ca. 170 kJ/day) by 15 days Woodpeckers as a function of age. TE = energy ac- cumulatedin new tissue (i.e., growth), RMR = resting of age. metabolic rate of fasted young during the day, FMR = Total metabolized energy per chick over the field metabolic rate (measured with doubly labeled nestling stage (age O-31 days) was 3,853 J (Ap- water), and TME = total metabolized energy(i.e., field pendix 2). Of the total, RMR comprised about metabolicrate + growth). SeeAppendix for calculation 47%, whereasactivity, HI, and thermoregulation methods. combined accounted for about 40%. The energy accumulated in growth (TE) was only 13% of TME, which is the lowest fraction observed yet this we calculate the nestlings’ mass-independent for any altricial bird. Gross growth efficiency (ex- metabolic rate as 2.46 kJ day-l g-o.67.The mass- pressedas TE/TME) averages0.24 (range = 0.17- independent BMR of adults (76 g) is 3.64 kJ 0.29) in 13 altricial species (Wijnandts 1984, day-l g-o.67for nighttime measurementsand 4.98 Klaassen et al. 1989); substantially higher than kJ day-’ g-o.67during the day. Bucher (1987) the Acorn Woodpecker’s average of 0.13. Two comparedthe metabolic intensity of nestling birds factors that may contribute to the Acorn Wood- by calculatingthe ratio of hatchling to adult mass- pecker’s relatively inefficient growth are: (1) the independent metabolism. The ratios for Acorn growth depressingeffects of tannins contained in Woodpeckersare, respectively, 0.68 and 0.50 for the partially acorn diet, and (2) a relatively large nighttime and daytime adult BMR values. These maintenance energy requirement. Slow growth values are the highest reported for any altricial prolongs the time that nestlings remain in the bird (Bucher 1987) and indicate that the met- nest and thereby increases the total energy re- abolic intensity of nestling woodpeckersis com- quired for maintenance (basal metabolism plus parable with that of precocial species.An inher- thermostatic costs), whereas fast growth de- ently high metabolic rate is thus another factor creasesthe cumulative maintenance energy re- that reduces the woodpecker’s grossgrowth ef- quirement and thereby increases gross growth ficiency. efficiency. For example, Arctic Terns Sterna The energy devoted to growth can also be ex- paradisaeu (Klaassen et al. 1989) produce semi- pressedas a fraction of the chick’s BMR (Dunn precocialchicks that weigh 115 g when they fledge 1980; but seeWilliams and Prints 1986). For the at 2 1 days of age. The nestling terns’ TME, 4,442 Acorn Woodpecker, this value (TE/BMR) de- kJ, is only 16% greater than that of the Acorn creasesin a more or lessexponential fashion from Woodpecker, despite the fact that fledgling terns hatching levels of about 0.9 to 0 at the end of are 44% larger than fledgling woodpeckers.The the growth period. Such a pattern is typical of terns’ higher grossgrowth efficiency (0.23) results birds in general, and other speciesthat have been partly from their relatively fast growth rate. studied exhibit initial values between 2.50-0.70 In addition to slow growth, nestling wood- (Ricklefs 1983). Acorn Woodpeckers are thus on peckers seem to have an unusually high main- the low end of the observed range. tenance energy requirement. Although we did not measurehatchling RMR, the relation of nest- ADULT ENERGETICS ling RMR to mass is strictly linear (Fig. 5). The The RMR of adult Acorn Woodpeckers is un- RMR predicted for a 4.7-g hatchling from the usual in two respects.First, the plot of RMR vs. Figure 5 data (Equation 8) is 6.95 Id/day. From T, lacks a thermoneutral zone (Fig. 4). This cir- 354 W. W. WEATHERS, W. D. KOENIG AND M. T. STANBACK

TABLE 4. Conditionssurrounding adult Acorn Woodpeckerfield metabolicrate (FMR) determinations.

Bird Mean T. no. Gender Mass (9) Date PC) (lE% Social groupb 9 F 78.4 8-9 May 10.2 242 10 M 86.1 8-10 Mav 9.8 208 3 breeders,no nonbreedinghelpers 42 M 84.5 4-6 June< 20.2 178 ’ pair only 43 F 79.4 16-18 June 22.4 151 4 birds; 3 breeders+ 1 nonbreedinghelper

a Date that bird’s FMR was determined by doubl labeled water. b Number of birds cooperating in the breeding e t?art at this bird’s nest. cumstanceresults partly from an unexpectedand and seabirds,both of which have relatively high progressive hypothermia at T,s‘ below 2O”C, FMR (Nagy 1987, Weathers and Sullivan 1989), which reducesRMR through the Q10effect. It is and thus they may not apply to relatively non- very unusual for an 80-g bird to become hy- volant speciessuch as the Acorn Woodpecker. pothermic at such relatively high temperatures Parental effort of breeding birds studied with following only 3 hr of fasting. Whether this rep- the DLW method has been evaluated in terms resentsan adaptive responseserving to conserve oftheFMR/BMRratio (Dijkstra 1988, Weathers energy or an inability to regulate Tb in unclear. and Sullivan 1989). This ratio is highestin adults In any event, as a consequenceof hypothermia, that are feeding nestlings, for whom it ranges resting energy expenditure is reduced at mod- from 2.0 in ground-foraging passerinesto 5.2 in erate temperatures.Although a similar hypother- some seabirds, and averages 3.6-3.7 in nonpas- mia was reported for the Green Woodhoopoe serine species. The BMR of an 82.3-g Acorn Phoeniculuspurpureus(Ligon et al. 1988) which Woodpecker (the mean mass of our FMR birds) is also a cooperatively breeding, cavity-nesting is 71.8 Id/day (Table 2) which gives a FMlU bird, it apparently resulted from the semistarved BMR ratio of 2.7. Thus, from this perspective condition ofthe birds used by Ligon et al. (1988) as well, the energyrequirements of breeding adult as Green Woodhoopoesin good condition do not Acorn Woodpeckers seem to be somewhat low. become hypothermic (J. B. Williams, M. A. du In reality they may be even lower than our es- Plessis, and W. R. Siegfried, pers. comm.). timates, as the radio transmitters worn by two The second unusual trait is that the Acorn of our birds may have increased their FMR Woodpecker’s BMR is much higher than ex- (Gessaman and Nagy 1988b). pected for a bird of its size (Table 2). The BMR The FMR of our four adult Acorn Woodpeck- of the Great Spotted Woodpecker Dendrocopos ers ranged widely from 15 1 to 242 M/day (Table major is also about 40% higher than predicted 4) with two of the adults’ FMR overlapping that (Gravrilov, unpubl. data, in Kendeigh et al. 1977) of older nestlings(Fig. 5). The wide range in FMR which suggeststhat a high BMR may character- can be explained in part as follows. The adults ize the family Picidae. If hypothermia at rela- with the highest FMR (Nos. 9 and 10) were the tively high T, representsan adaptative response female and one of the males at a nest with three serving to conserve energy, then a high BMR breeding adults (two males, one female; no non- would be regardedas counteradaptative. Recon- breeding helpers). Both birds wore radio trans- ciling this paradox will require additional data mitters and it is likely that this increased their on woodpecker metabolism. energyexpenditure. Gessaman and Nagy (1988b) The average FMR of the four breeding adults found a 41-50% increase in the energy expen- that we studied (195 Id/day) can be compared diture of flying pigeons that wore radio trans- with DLW measurements of other speciesusing mitters equal to 2.5-5% of their mass. Although the predictive equations of Weathers and Sulli- the female wore the smaller of the two trans- van (1989). Basedon theseequations, our wood- mitters (2 g), her FMR was higher than the male’s. peckers’ FMR is 77% of that predicted for an Transmitters weighing 4 g have been shown to 82.3-g nonpasserine feeding nestlings and 91% reduce Acorn Woodpecker activity (P. Hooge, of that expected for breeding birds in general. unpubl.) and this may partially account for the The predictive equations are biased in favor of male’s lower FMR. aerial-foraging insectivores (swifts and swallows) Another factor that probably contributed to ACORN WOODPECKER ENERGETICS 355

TABLE 5. Time budgetof adultfemale Acorn Wood- The adult with the lowest FMR (No. 43) ben- pecker(No. 9) feedingnestlings and herestimated field efited from both warm weather and the presence metabolicrate. of helpersat the nest (Table 4). In sum, the FMR of the four adults that we studied varied in ac- Activity Energy Duration, CO$~OI expended cordancewith expectations.Namely, it was high- category hrlday D kJ est in the two birds wearing radio transmitters Nighttimerest 10.00 1.0 29.0 that were studied during cool weather and lowest Daytime perching 9.66 2.0 56.0 for the two birds without transmitters that were Preening 1.06 2.2 6.8 studied during warm weather. Further, among Eating 0.53 2.2 3.4 the latter group, FMR was lowest for the adult Plying 1.54 12.0 53.6 from the nest with helpers. As emphasized by Othera 1.20 2.3 8.0 Nagy (1989), the DLW method is now sufficient- Total 23.99 156.8 ly sensitive to detect small differences in FMR ’ ’ Includes:feeding young, “moving,” displaying,gleening, drilling holes. b BMR = basalmetabobc rate. between individuals. ECOLOGICAL CONSEQUENCES the high FMR of adults Nos. 9 and 10 was the The physiological properties of Acorn Wood- cooler weather that prevailed during the time peckers documented here are generally consis- that they were studied. The other two adults (Nos. tent with those expected of a speciesthat is se- 42 and 43) experienced much warmer condi- verely food- or nutrient-limited. Adults become tions, which would have reduced their thermo- hypothermic at relatively high ambient temper- static costs (Table 4). atures (Fig. 4) as would be expectedif the ability We can estimate adult No. 9’s thermostatic to cope with the additional thermoregulatory de- costsfrom our time budget data (Table 5) using mands of low temperature was difficult. Nestling metabolic cost assignments for the various ac- growth is slow, and young, like adults, become tivity categoriesbased on our measurements of hypothermic very easily until they are over 2 BMR. The energy cost assignments in Table 5 weeks old (Fig. 11). Older young experience high follow Buttemer et al. (1986) except for flight thermoregulatory demands due to their cool nest which was estimated from the female’s mass us- microclimate. Because of the nestling’s slow ing the nonpasserine equation of Rayner (1982). growth and high thermoregulatory demands, the The nighttime BMR predicted for a bird of No. total energycost ofreproduction in Acorn Wood- 9’s size is 2.9 kJ/hr (Table 2). FMR calculated peckers is relatively high. Yet because this cost from No. 9’s time budget is 157 Id/day, which is spreadout over a long nestling phase, the pro- is 65% of the value measured with DLW. The portion of the adult’s daily energy budget de- differencebetween measured FMR and FMR es- voted to reproduction (parental effort) is fairly timated from the time budget (= 85 Id/day) rep- low. resents the energy cost of thermoregulation and Acorn Woodpeckers typically live in foothill equals 35% of the measured FMR. Basal plus and montane areasthroughout their range, which thermostatic coststhus equal about 155 Id/day, extends from southern Oregon to northern Co- or 64% of the female’s total FMR, a fraction lombia. Given the relatively cold conditions to comparable to that of other birds (Walsberg which nestlings are therefore typically exposed 1983). We emphasize that the female’s actual during the spring breeding period, nestling and thermostatic costsare uncertain becauseour es- adult hypothermia is potentially advantageous timate of them relies on assumed activity costs. in reducing energy demands and prolonging life We are least confident of our flight cost assign- when conditions are poor. ment. If the energy cost of flight was 50% higher At least three features of the Acorn Wood- than we estimate, due to the effect of wearing a pecker’s life history help mitigate the potentially radio transmitter, thermostatic costs would be costly effectsof these characteristics.The first is reduced to 58 W/day; which, although smaller, nesting in cavities, which provides an improved is still 24% of FMR. Clearly, thermoregulatory thermal environment for breeding birds (Mer- costsare partly responsiblefor the relatively high tens 1977). The second is relatively low preda- FMR of adults Nos. 9 and 10, although the exact tion rates, even compared to other cavity-nesting magnitude of their contribution is uncertain. species(Koenig and Mumme 1987) which re- 356 W. W. WEATHERS. W. D. KOENIG AND M. T. STANBACK duces the potential costs of a lengthy nestling slow development of nestlings and their extend- period. The third is cooperative breeding. Be- ed vulnerability to external conditions. Thus, the causeAcorn Woodpeckers typically live in fam- Acorn Woodpeckers’ unusual social behavior mily groups of three to five adult birds (up to as may be related to their unusual physiology. many as 15) all of which participate in brooding ACKNOWLEDGMENTS and feeding of young, the high cost of reproduc- tion and the time and energy demands of nest- We thank the owners of Oak Ridge Ranch for access lings are typically spread out among several to their land. K. V. Snipesprovided valuable assistance with many of the measurements, including field r,, adults. ontogeny of endothermy, and determination of RMR Why do Acorn Woodpeckers, which breed with help from D. R. Powers. P. Hooge helped collect communally in groups of up to 15 individuals data in the field. K. A. Nagy helped with the labeled and have substantial food reserves available in water analysis. A. J. Bloom designed the electronics the form of stored acorns, have such extremely for interfacing Mini-mitter transmitters with the Campbell CR2 1 micrologger.R. E. Ricklefs and Mike low nestling growth rates?Such slow growth may Bowersassisted with the growth curve calculations.M. have a phylogenetic component and characterize J. Murray helped remove transmitters from the nest- melanerpine woodpeckersin general. Even at this lings. D. J. Anderson, W. A. Buttemer, E. Greene, and taxonomic level, however, slow growth is prob- K. A. Nagy provided helpful comments on the manu- script. Support was provided by NSF through grants ably related to diet, as virtually all specieswithin DEB 80-22765, BSR 85-05490, and BSR 87-18195 to this genus depend substantially on fruit or other WWW, BSR 84-10801 and DEB 87-04992 to WDK, low-protein foods. These unusual features, along a NSF graduate fellowship to MTS, and by the Cali- with the high frequency of cooperative breeding fornia Agricultural Experiment Station. in this genus, may be related and represent an LITERATURE CITED adaptive complex of life-history characteristics. ASCHOFF,J., AND H. POHL. 1970. Der Ruheumsatz In the caseof Acorn Woodpeckers,slow growth von Vijgelen als Funktion der Tageszeit und der is probably related to the low protein and high Kornerarosse.J. Omithol. 111:38-47. tannin content of the acorns upon which they BALD~&, R L. 1968. Estimation of theoretical cal- depend. Koenig and Mumme (1987) have doc- orific relationships as a teaching technique: a re- umented that Acorn Woodpeckers at Hastings view. J. Dairy Sci. 51:104-111. BATE-SMITH,E. C. 1973. Haemanalysis of tannins: Reservation generally are unable to breed suc- the concept of relative astringency. Phytochem- cessfully without accessto stored acorns during istry 12:907-g 12. the spring. This suggeststhat energetic or nutri- BRYANT,D. M., AND C. J. HAILS. 1983. Energetics tional requirements needed to reproduceare sim- and growth patterns of three tropical bird species. Auk 100:425439. ply not provided by the available insects on a BUCHER,T. L. 1987. Patterns in the mass-indepen- territory. Supplemental food is necessary, and dent energeticsof avian development.J. Exp. Zool. this is typically provided by stored acorns. Yet Suppl. 1:139-150. the low-protein content of acorns, compounded BUT~EMER,W. A., A. M. HAYWORTH,W. W. WEATH- by the high level of tannins, which are known to ERS, AND K. A. NAGY. 1986. Time-budget esti- mates of avian energy expenditure: physiological bind proteins and reduce their availability to an- and meteorologicalconsiderations. Physiol. Zool. imals (e.g., Robbins et al. 1987) may produce 59:131-149. conditions of protein limitation in breedingAcorn CALDER,W. A., III. 1982. A proposal for the stan- Woodpeckers. dardization of units and symbols in ecology.Bull. Ecol. Sot. Am. 63:7-10. Physiological constraints appear to alter costs DIJKSTRA,C. 1988. Reproductive tactics in the kes- and benefits in ways that influence the functional trel Falco tinnunculus.Ph.D.diss., Univ. of Gro- consequencesof behaviors. In this case, protein ningen, Groningen, The Netherlands. limitation is consistentwith many of the unusual DRENT,R. H., ANDS. DAAN. 1980. The prudent par- physiological characteristics of Acorn Wood- ent: energeticadjustments in avian breeding..Ar- dea 68225-252. peckersdocumented here. Protein limitation may DUNN,E. H. 1973. Energyallocation ofnestling dou- also be an important factor influencing the costs ble-crested cormorants. Ph.D.diss., Univ. of and benefits of cooperative breeding. The addi- Michigan, Ann Arbor. tional brooding and feeding capabilities provid- DUNN, E. H. 1975. The timing of endothermy in the develonment of altricial birds. 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p. 161-220. In D. S. Famer, J. R. King, and K. with DLW, and TE. Resting metabolic rate (RMR) and C. Parkes [eds.], Avian biology. Vol. VII. Aca- FMR were estimated from Equations 8 and 9, respec- demic Press,New York. tively, and the mean nestling mass predicted for each WEATHERS,W. W., C. J. SHAPIRO,AND L. B. ASTHEI- day. For nestlings 5 days old and younger, FMR was MER. 1980. Metabolic responses of Cassin’s assumedto equalRMR, sinceEquation 9 predictsFMR Finches (Curpoducus cassinii) to temperature. < RMR for this age group. RMR calculated from Comp. Biochem. Physiol. A. Comp. Physiol. 65: Equation 8 does not accountfor possiblereductions in 235-238. RMR due to nestlinghypothermia and thus may over- WEATHERS,W. W., AND K. A. NAGY. 1984. Daily estimate the actual value. Such an error would result energyexpenditure and water flux in black-rumped in an underestimation of the proportion of FMR at- waxbills (EM/da troglodytes).Comp. Biochem. tributable to HI, activity, and thermoregulation. The Physiol. A. Comp. Physidl. 77:453-458. energy content of nestlings(EC, kJ) was calculatedby WEATHERS.W. W.. AND K. A. SULLIVAN. 1989. Ju- multiplying the dry mass predicted (Equation 10) for venile’ foraging proficiency, parental effort, and each age by the assumed energy density of nestling avian reproductivesuccess. Ecol. Monogr. 59:223- tissue(23.4 kJ/g dry mass). The daily increment in TE 246. @J/day)was obtainedby subtractingthe previousday ’s WILLIAMS.J. B., AND K. A. NAGY. 1985. Water flux EC (kJ) from the current day’s value. and energeticsof nestling Savannah Sparrows in The energy density of lean, dry, nestling tissue av- the field. Phvsiol. Zool. 58:515-525. eragesa fairly constant20.1 kJ/g for most species(Dunn WILLIAMS,J. B., AND A. PRINTS. 1986. Energeticsof 1973).Nestling fat contentvaries widely amongspecies, growth in nestling SavannahSparrows: a compar- however, ranging from about 8-50% of dry mass (re- ison of doublv labeled water and laboratory esti- viewed by Ricklefs 1983). Becauseavian body fat con- mates. Condor 88:74-83. tains about 37.7 W/g (Ricklefs 1974), the energy den- W~JNAND~~,H. 1984. Ecologicalenergetics of the long- sity of nestling tissue is fairly sensitive to variation in eared owl (Asio otus). Ardea 72:1-92. its fat content. Although we did not measure the fat WOOD,R. A., K. A. NAGY, S. MACDONALD,S. T. WA- content of woodpeckernestlings, our impressionis that KAKLJ~A,R. J. BECKMAN, AND H. KA.u. 1975. it is rather low and we can estimate it with sufficient Determination of oxygen-18 in water containedin accuracyas follows. Specieswith unreliable food sup- biological samplesby chargedparticle activation. plies (e.g., some seabirdsand aerial-feeding passerines Anal. Chem. 471646-650. and swifts)tend to accumulaterelatively largeamounts of fat-up to 50% ofdry mass(O ’Connor 1978, Bryant and Hails 1983, Ricklefs 1983). In most species,lipid APPENDIX 1 content is much lower; on the order of 8.6 to 25% of dry mass (calculatedfrom Ricklefs 1983). Given the We based our nestling energybudget calculations(Fig. latter rangein fat content, the energydensity of typical 13; Appendix 2) on nestling mass predicted by the nestlingsis 21.6 to 24.5 kJ/a drv mass. For our cal- logistic equation (Equation 5) rather than on actual culations, we assumed an intermediate value of 23.4 mass,because day-to-day variations in observedmean kJ/g dry mass, equivalent to a fat content of 17.6%. nestling mass tended to obscurethe central trend with Assuming the fat content of Acorn Woodpeckers is respectto the energyaccumulated in body tissue (TE). within the usual range of 8-25%, our estimated TE Total metabolized energy(TME) was calculatedas the values should be within 7% of the true value. sum of the field metabolic rate (FMR), as measured ACORN WOODPECKER ENERGETICS 359

APPENDIX 2. Parameters of the nestling Acorn Woodpeckers’ energy budget.

Age@ws) Mass!(g) E@ (W T@ &J/day) RMRd &J/day) FMR’ @J/day) TME’ &J/day)

0 7.6 16.8 0.0 9.9 9.9 9.9 9.3 21.5 4.7 11.6 11.6 16.3 : 11.4 27.5 6.0 13.6 13.6 19.6 3 13.8 35.1 7.7 16.0 16.0 23.7 4 16.6 44.8 9.7 18.8 18.8 28.5 5 19.7 57.0 12.2 22.0 22.0 34.2 6 23.3 72.1 15.1 25.6 28.9 43.9 27.3 90.3 18.3 29.5 38.4 56.6 : 31.5 112.0 21.7 33.8 48.6 70.3 9 36.0 137.0 25.0 38.3 59.4 84.4 10 40.7 165.1 28.1 42.9 70.5 98.6 11 45.3 195.7 30.6 47.5 81.6 112.2 12 49.8 227.9 32.2 52.1 92.4 124.7 13 54.1 260.8 32.8 56.4 102.8 135.6 14 58.1 293.2 32.5 60.4 112.4 144.9 15 61.8 324.4 31.1 64.0 121.2 152.4 16 65.1 353.4 29.1 67.3 129.0 158.1 17 67.9 379.9 26.5 70.2 135.9 162.4 18 70.4 403.5 23.6 72.6 141.9 165.4 19 72.5 424.1 20.6 74.8 146.9 167.5 20 74.3 441.9 17.7 76.5 151.2 168.9 75.7 456.9 15.1 78.0 154.7 169.8 ;: 77.0 469.6 12.6 79.2 157.6 170.3 23 78.0 480.1 10.5 80.2 160.0 170.5 24 78.8 488.7 8.7 81.0 162.0 170.7 25 79.5 495.8 7.1 81.7 163.6 170.7 26 80.0 501.6 5.8 82.2 164.9 170.7 27 80.4 506.3 4.7 82.7 165.9 170.6 28 80.8 510.1 3.8 83.0 166.8 170.6 29 81.1 513.2 3.1 83.3 167.4 170.5 30 81.3 515.6 2.5 83.5 168.0 170.4 31 81.5 517.6 2.0 83.7 168.4 170.4 Sum 501 1,802 3,352 3,853 nCalculated as: mass(g) = 82.19/( I + 9.79e-0fz6’),where f = daysof age. bNestling energycontent (EC) calculatedas: kJ = [l - (0.924 - 0.0024 x m)] x 23.4 x m, wherem = massin grams. 5Daily incrementin tissueenergy (TE) calculatedby subtractrngthe previousday ’s EC from the currentday ’s EC. d Restingmetabolic rate (RMR) of fastednestling calculated as: Id/day = 2.25 + M. e Field metabolicrate calculatedas: kJ/day = -27. I + 2.40m. exceptfor daysO-5, for which FMR wasassumed to equal RMR.