THE INFLUENCE OF FOOD ON REPRODUCTIVE STRATEGIES IN A MONOGAMOUS (CHLOROCERYLE AMAZONA)

WILLIAM JAMESDAVIS • AND DOUGLASJ. GRAHAM2 SmithsonianTropical Research Institute, Balboa, Republic of Panama

ABSTP,ACT.--We examined the influence of food accessibilityon the reproductivebehavior of the (Chloroceryleamazona) in Panama.Both sexesinvested equally in nest building, but femalesincubated the eggsmore often than males. Foragingperformance (time elapsed between successfuldives) differed between mates becausethey often used different foraging patcheswithin the breeding territory. Male foraging performance was significantly correlated to fish biomasssampled from preferred foraging patches.Further- more, the level of a male's foraging determined the number of fish he fed to his mate: more successfulforagers courtship-fed their mates more fish than less successfulmales. In turn, the rate of courtshipfeeding influencedwhether a female would lay eggsand the date of laying. Pre-laying foraging performanceof both sexeswas a predictor of the number of fish fed to nestlings.We concludethat disparitiesin the amount of food delivered to ovulating femalesby males,and to nestlingsby both parents,are determined by the distribution of food within the territory. Received14 June1990, accepted 24 February1991.

FOODabundance can affect the timing and rental behavior using game theory shows that successof breeding in (Kallander 1973, conflicts of interest between parents can ac- Murton and Westwood 1977, Drent and Daan count for the occurrenceof multiple parental 1980, Davies and Lundberg 1985). Furthermore, investment strategies (see reviews Maynard food distributionwill influencemating patterns Smith 1977, Wittenberger 1979, Oring 1982). (Oring 1982,Wittenberger and Tilson 1980)and Suchconflicts may ariseif parentshave an un- may determinethe relative contributionof each equalaccess to essentialresources such as food parent to feeding nestlings(Reyer and Wester- (Beissinger1986). We propose that the repro- terp 1985).In plentiful yearswhen femalescan ductive behaviorof both sexescan be strongly adequatelyprovision young without help from affectedby their relativeaccess to food.To test the male, the value and level of paternal care this hypothesis,we examinedthe relationship decreases.In suboptimalyears, however, male betweenfood distribution,foraging, and court- contribution is believed to be critical to off- ship feeding ratesof male Amazon spring survival (Bart and Tornes 1989). The ar- (Chloroceryleamazona). We also examined the gument that there are periods when paternal parental roles of males and femalesbased on care is essentialimplies that food availability is the relative food availability to each parent. an important determinant of parental feeding patterns. The relationship between food avail- METHODS ability and reproductive behavior is seldom quantified. Distributionand ecology.--TheAmazon Kingfisher residesalong lowland streamsfrom southernMexico The issueis not simply overall abundanceof into the Amazonian region of South America. The food,but alsowhether food is equally available speciesis monogamous,with pairs often remaining to eachparent. If not, oneparent may contribute mated for several years. Nests are excavatedin ex- less than its mate in feeding young, indepen- posedearthen banks along streamsor in banksclose dent of any sex differencesdue to anisogamy to fresh water. Amazon Kingfisherseat fish, fresh- or a prior investmentin caring for the young water shrimp,and occasionallyfrogs and aquaticin- (Trivers 1972,Beissinger 1987). Analysis of pa- sect larvae (Davis unpubl. data). Typically, there is one brood per season;nestlings remain in the nest for a minimum of 21 days (Skutch 1957, Davis pers. • Present address: 31112 163rd Avenue, Avon, Min- obs.).Breeding occurs in the dry season,which along nesota 56310 USA. the Caribbeancoast in Panamamay extend from late 2Present address: Le Groupe Dryade Lt•e., 4700 Decemberto July. The end of the breeding season Boulevard Wilfrid-Hamel, Quebec, Quebec GIP 2J9, coincideswith flooding,which can destroyoccupied Canada. nests.A pair defends a breeding territory that con-

78O The Auk 108: 780-789. October 1991 October1991] FoodAccessibility andReproduction 781 tainsa nestbank and foraging patches,with territorial T^nLEI. Behaviorcategories. aggressiondirected primarily towards birds of the same sex (Remsen 1978, Davis unpubl. data). Category We observed12 matedpairs of C. amazonafrom mid- (abbrev.) Description Decemberto mid-May, 1987and 1988,along the Cas- Active foraging standsaltertly on a perch cajal River in Portobelo National Park, Panama. The (AFOR) or hovers; attention directed moistrain forestalong the banksof thislowland stream toward a foraging area. have beenlargely convertedto cattlepastures. In ear- Passiveforag- Bird's attention is directed to- ly Decemberin both yearsjust before breeding began, ing (PFOR) ward foragingarea while bird we mist-netted and marked birds with colored leg sits low on its perch. bandsandpaint on the rectrices.We recordedchanges Total foraging Combined time bird spent ac- in weather and water level throughout the breeding (TFOR) tively (AFOR) and passively season.Nests located in earthen banks were opened foraging (PFOR). from the top to allow accessto the eggsand nestlings Inactive Bird is perched;few body (Davis 1980). To assessbreeding-population sizes,we (INACT) movements; attention directed counted the number of kingfishersand active nest away from stream;eyes peri- burrows along several streamsin the same general odically closed(sleeping). area as the Cascajal. We observedindividuals through binoculars or spotting scopes,and used focal sampling to record 24 h). Fishused to calculateregression equations were behavior (mean observation period [ñSD] = 156 + caughtby seining.Most (>95%) fish caught by Am- 71 min). We timed specificbehaviors (Table I) to the azonKingfishers were 3-9 cmlong and swam within nearest 5 seconds. Observations were made between I0 cm of the surface. Calculations of biomass from 0700 and 1200. We recorded location and outcome of fish countsinclude only specimensthat met these foraging events,prey size and type, and courtship criteria.We alsoused regression equations to calculate feedings.Prey size was estimatedto the nearestcen- biomassof preycaptured by kingfishers. timeter by comparingprey with the length of the Parental investment.--In 1987 we recorded the time bird's bill (which was known for all tagged individ- and effort (number of visits) that adults spent on nest uals).The kingfishers'habit of beatingtheir food be- excavation and incubation. In 1987 and 1988 we re- fore swallowing provided an opportunity to identify cordedoccurrences of courtshipfeeding (CF) and cop- speciesof most prey items. ulation. Courtshipfeedings included (I) voluntary Preyabundance.--We estimated the number of fish feedingof femalesby males when the fish was offered accessibleto C. amazonaby recordingthe successof head first; (2) involuntary feeding when a female birds as they foragedat specificlocations (foraging wrestled a fish from a male; and (3) reversed feeding patches),and by countingthe number of fish swim- when the female fed the male (< 1% of total number ming within these patches. Becausemost foraging of courtshipfeedings observed). dives occurredin water < I0 cm deep along edgesof In 1988,six femaleson contiguousterritories failed the river or in pools,we countedall fish that entered to lay eggsby 4 March,the middleof the breeding a half-circle of 2-m radius as measuredfrom the edge season.We conductedsupplemental feeding experi- of the stream. We adopted a sampling period of 5 ments to determine if low fish numbers contributed min/count, becausethe averageresident time of ac- to this failure. On alternatingterritories (n = 3), we tively foraging kingfishers(n = 33 observations)in a stockeda plastic-linedpool (45 cm in diameterand patch was 5.7 + 3.7 min. Care was taken to approach 12 cm deep)with a minimum30 fish between0700 the streamslowly so as not to disturb the fish. Once and 0900.Supplemental feedings continued on a ter- the observer was in position, counts began after 5 ritory until the femalelaid her first egg or 28 days min to allow time for fish to habituate. We recorded had elapsed.We recordedthe numberof courtship the identityof specieswhen possible,size (within the feedingsand copulationsfor a period of 30-60 min following categories:0-3, 3.1-6, 6.1-9, and >9.1 cm), after a pool was stocked. and swimming depth estimatedto the nearestcm. We Also in 1988, we conductedan experiment to de- made 2-6 countsat most foraging locations.We an- terminewhether the accessibilityof food or number alyzed only data from the I0 mostfrequently visited of nestlingswould affect the amountof foodparents patcheswithin a male'sterritory, because other patch- broughtto the nest.Seven nests with 12-15-day-old es were used infrequently (-<2 visits recordedper nestlingswere tested.We observedfeedings from patch). blindsduring three 5-h periodson consecutivemorn- We convertedfish countsinto biomass(g) available ingsstarting at 0700.During the firstperiod, we re- per patchby extrapolatingfrom regressionequations cordedfeeding rates without manipulatingfood or that related length rs. wet weight for each species numberof nestlings;at fournests, two control periods (water content of different speciesvaried between were run. At the start of the secondperiod, we con- 15%and 25%of body weight after drying at 100øCfor structeda temporarypool within 20 m of the nest 782 DAVISAND GRAHAM [Auk, Vol. 108

tIllI• ATimemales Observed80.7 ½hrs.}N=9

'" n B TimeObserved {hrs.} II males 60.9 N=6 II females92.3 N=6

Total Active Passive Inactive I•eenlng With With Vigilant Foraging Foraging Foraging Mate Conspecific

Activity Fig. 1. Percenttime spentby malesand femalesin variousactivities before the firstcourtship feeding (A) and during the period of courtshipfeeding (B). Open barsrepresent males; closed bars, females. Asterisks indicatelevels of significanceof two-tailed,independent sample t-tests between values in A and B; * = P < 0.05 and ** = P < 0.01. Differences in the number of hours that males and females were observed are due to samplingbias. Early in the breedingseason (A), we were preferentiallyfollowing males. After the startof courtshipfeeding (B), we followedboth sexes,but femaleactivity decreased and femaleswere in view more often than males.

and stockedit with fish. Fish were readily taken from Both mates participated in nest excavation. the pools.At thestart of the third period,we increased We found no difference between the sexes in broodsize by 50%by addingchicks taken from nests the number of digging bouts per observation locatedalong other streams(food was not supple- period during 17 periods at 10 nests (male œ mented).Age and weight of nestlingswere matched to those of the resident chicks. [+SD] = 5.4 _ 6.6, female • = 3.7 _+3.8; paired t-test, t = 0.8, P > 0.1) or in the total amount RESULTS of time spent digging per observationperiod (male œ = 701 + 942.1 s, females • = 606.2 + In 1988 we recaptured 18 of 24 individuals 741.7 s; paired t-test, t = 0.3, P > 0.3). We con- bandedin 1987.Eight pairsremained intact and firmedSkutch's (1957) report that only females on their original territories,while one male and incubate at night and both sexesshare incu- onefemale acquired new mates(unbanded). The bation duties during the day (n = 6 nests). fate of the remaining6 birdsis unknown. These Beforecourtship feeding, the sexesspent equal data indicatea high degreeof site fidelity by percentagesof time foraging(Fig. 1A), but after both sexes. We recorded 3 cases of females the start of courtshipfeeding, femalessignifi- switchingmates: 1 caseafter the pair'seggs had cantly decreasedtheir foraging time and in- hatched (the male fledged their 4 young) and creasedtheir time sitting inactive(Fig. lB). Fur- 2 casesbefore eggswere laid. thermore,females who subsequentlylaid eggs October1991] FoodAccessibility andReproduction 783

showeda more dramaticdrop in percent time A. Layers foraging (TFOR) then nonlaying females(Fig. 105 2: linear regressioncoefficients for laying fe- males 4, 9, and 11 are r = -0.96 [P < 0.001], r 70 = -0.78 [P < 0.003], and r = -0.7 [P < 0.02], respectively;for nonlaying females 8, 7, 6, and 35, 12, r = -0.42 [P > 0.08], r = -0.59 [P > 0.07], r = -0.47 [P > 0.6], and r = 0.08 [P > 0.7], respectively).We obtained similar resultswith 0 percenttime actively foraging (AFOR); all r val- ues for layerswere statisticallysignificant at P DaysBefo• •yin9 < 0.05, while all r values for nonlayerswere nonsignificant(P > 0.05). B. Nonlayers Foragingperformance and resource availability.- 120 - Individual foraging performanceof malesvar- x

ied substantially(Table 2). We definedforaging 90- Ii x x xx ßß x performanceas the time a bird spendsactively e-.-.__._.._..•.ß ß øx xß el• foraging(AFOR) divided by the numberof suc- 60' cessfuldives. High numbersindicate poor per- oßß e formance. Mean fish biomass varied substan- 30- ,'•' • '• o

tially both within and acrossterritories (Table x 3). Thus, variability in male foraging may be due to an unequaldistribution of goodforaging patches.In fact, we found a greater biomassof DaysBefore Start of SupplementalFeeding fish in territoriesof maleswho displayedthe Fig. 2. Percent time that females spent foraging best foraging performance(territories 4, 9, 2, (TFOR). Layers (A) laid eggsunaided: females 4 (¸), and 12; • = 104.7g) than in territoriesof males 9 (x), and 11 (0). Nonlayers (B) were supplied with with the poorest record (territories 8, 7, and 6; food: females 8 (0), 7 ( x ), 6 (¸), and 12 (.). In A, zero • = 37.8 g; two-tailed t-test, t = 2.39, P < 0.05; correspondsto the datewhen laying began.In B, zero territory 11 was not included in the t-test be- correspondsto the day when supplementalfeedings causeof the extremely low fish count on this started.See text for values of regressioncoefficients. territory). The resultsof a Spearmanrank cor- relation between male foraging performance and total fish biomassper territory (n = 7, r = We had insufficient data to assessthe impact 0.75, P < 0.05, one-tailed) further indicate that of patch quality on female foraging perfor- fish biomasswithin a territory influencedthe mance. However, our data indicate that mates resident male's performance. partition foraging sites within their territory Foragingperformance data are available for (Table 4). The fact that only one parent used 4 birds in both 1987 and 1988 (females 4 and 7; supplementalfeeding pools during our exper- males8 and 3). A cross-yearcomparison shows iments is further indication that the sexes used that performancewas significantly better in 1987 separateforaging areas. than in 1988 (paired t-test, one-tailed: in 1987, Courtshipfeeding.--Courtship feeding perfor- •?= 51.7; in 1988, œ= 68.8; t = -2.6, P < 0.05). mance (minutes between feedings) of males Assumingthat an individual's fishing skill does varied substantially(Table 2). There was no sig- not decreasewith experience,we believe that nificant correlationbetween courtshipfeeding patch quality on average decreasedbetween performanceand percentcapture rate (number yearsand was responsiblefor the observeddif- of successfuldives per numberof dives;Spear- ferencesin performanceacross breeding sea- man rank correlation, r = -0.48, df = 8, P > sons.Therefore, we considerthe variability in 0.05),but there was a significantcorrelation be- patch quality--not the bird's fishing ability-- tween courtship feeding performanceand for- to be an importantfactor affecting breeding suc- agingperformance (Spearman rank correlation, cessof C. amazona;all pairs in 1987 that laid r = 0.63, df = 7, P < 0.05; males 7 and 8 shared eggsdid so at earlier datesthan the samepairs the last rank and male 6 was excluded because in 1988 (Fig. 3). no courtshipfeedings were observed;see Table 784 DAVIS ANY GEartAM [Auk, Vol. 108

TABLE2. Male foragingand courtshipfeeding (CF) performance.

Courtship feeding per- Foragingb Time in view formance performance Capturerate Pair Year• (rain) (min/CF) (rain/success) No. of dives (%) 4 1987 191.9 64.0 -- 0 -- 1988 623.3 105.4 28.7 14 35.7 9 1987 232.5 67.7 24.5 8 62.3 1988 1,145.5 95.5 26.3 31 45.2 3 1987 406.3 65.7 37.9 4 33.3 2 1987 413.9 88.9 26.6 7 28.6 1988 404.9 101.0 62.4 21 23.8

11 1987 102.6 102.6 -- 4 0.0 1988 1,164.8 77.7 12.6 32 59.4 8 1988-B 491.0 NA b 64.2 12 33.3 1988-A 345.1 26.5 NA NA NA

7 1988-B 975.2 NA b 207.4 11 18.2 1988-A 259.0 51.8 NA NA NA

6 1988-B 575.0 NA c 82.1 22 31.8 1988-A NA NA NA NA NA

12 1988-B 652.9 108.8 28.2 7 33.3 1988-A 263.0 65.8 NA NA NA

' Data from both 1987and 1988;the time period BEFORE(B) and AFTER (A) the start of supplementalfeeding in 1988 is given. Other values were calculatedfrom data collectedbetween the datesof the first recordedcourtship feeding and egg laying. Data were not systematically collectedfor pairs 8, 7, 6, 12 in 1987or pair 5. • Not Available(NA) becauseonly 1 courtshipfeeding was observed. cNot Available becauseno courtshipfeedings were observed.

2). This implies that courtshipfeeding perfor- supportedby the factsthat males increasedthe mance of a male is determined by his foraging number of courtshipfeedings when supplied performance. with fish (Table 5), and that females on food- Mates of males with poor performance laid supplementedterritories (8, 7, and 12) laid eggs few eggs or none. In 1988, when fish counts, while females on nonsupplementedterritories foraging performance,and courtshipfeeding (5, 6, and 13) failed to lay. performancewere low, femaleson territories8, Feedingnestlings.--We observed a large vari- 5, 7, 6, 12, and 13 failed to lay eggsby the mid- ability in nestling feeding rate in both 1987and point (early March) of the 1987breeding season 1988. In all but one pair both parents fed nest- (Table 5). The failure to lay eggsmay be due to lings,although contributions were seldomequal the males' inability to adequately feed their (Fig. 4). In everyinstance where adultsexploit- mates.Specifically, a minimum feedingrate may ed the supplemental food, feeding rates in- be necessaryto supportegg laying (courtship creasedabove that of the controlperiod (Fig. 5; feeding performanceof males8, 5, 7, 6, and 12 averagenumber of fishfed to eachnestling dur- before the start of supplementalfeedings were ing control periods was: 2, 2, 1.3, 1.7, 3.5, 2, 3; all <1 feeding/108 min). This hypothesisis during food supplementedperiods: NA, NA, 4,

TABLE3. Estimatedfish biomassfrom patchesmost frequently visited by males.

Territory a 4 2 9 11 8 7 6 12 Mean biomass(g) 19.5 13.0 7.8 0.0 4.1 5.2 2.0 6.3 No. of patches 8 10 9 10 9 10 10 10 Coefficient of variation b 142 155 121 0.0 173 152 220 189

A continuumbetween territory 4, the farthestupstream, and territory 12, the farthestdownstream. Expressedas percent of the mean:CV = (SD x 100)/•. October1991] FoodAccessibility andReproduction 785

follow parentsas they foraged for food. We did compare prenesting data on foraging perfor- manceof parentsthat fed nestlingsthe most (œ o = 86.7 min) vs. parents that fed the least (œ= 158.2 min) (one-tailed matched t-test; t = - 2.13, o df = 4, P -- 0.05). Within a pair, the parent with the best early foraging performancewill most

15 likely becomethe bestprovider (i.e. displaythe 14- highest feeding rate). 4- o 9- DISCUSSION 3 o 2 1 The accessibilityof fish is of utmost impor- 11 tancefor successfulreproduction in C. amazona. 8 o Becauseforaging patchesvary in quality and 5 patch distribution is unlikely to be uniform, 7 o access to fish across territories will differ. Access 12 to food affectsforaging performance, which in I I I I I • I I turn determines the number of fish that males DEC ,JAN FEB MAFI APFI MAY ,JUN feed their matesbefore egg laying, which in- Month fluences whether females lay eggs. Further- Fig. 3. Laying datesduring 1987 (O) and 1988 (I). more, becausethe sexespartition the available Territories (y-axis)are arranged with respectto lo- foragingsites within their territories,mates may cationalong the stream.Dates of floodingevents that have unequalaccess to food. Suchresource par- destroyednesting banks are indicatedby verticaldot- titioning can potentiallylead to a disparityin ted lines. Data from territories on the Raicero and parental investment(e.g. the amount of food Guancherivers are shown for comparison. fed to nestlingsby each sex). Variableforaging performance.--Variability in 4, 4.5, 3, 4 on territories 15, 4, 9, 11, 8, 7, and foragingperformance is bestexplained by dif- lg, respectively[NA indicatesthat data are not ferential individual accessto prey as opposed available]). In contrast, when nestlings were to differencesin individual foragingability. Prey addedto a nestin absenceof supplementalfood, accessibilityis a function of fish densitywithin parentsdid not increasefood deliveriesto meet a patch,as well as patchcharacteristics such as the increasein demand (Fig. 5; averagenumber water depth, flow rate, turbidity, and substrate of fish fed to each nestling during chick sup- type (Davis 1982,Reyer and Westerterp1985, plementalperiods was 0.8, 1, 1.8, 0.4, NA, 0.67, Davisin prep.). Physicalproperties of a patch 0.8). Presumablyaccess to food affectsnestling can changedramatically following moderateto feeding rates for each parent. heavyrainfall (Davis1980) or by changesin the Logically,nestling feeding rates should be silt load. In fact, the rainy seasonin late 1987 positively correlated with foraging perfor- (Julyto December)was particularly severe and mance of parents, but we could not test this of longduration (communication with localres- deduction becauseit was impractical to record idents). This caused water levels to be consis- feeding activity at a nest and at the sametime tently higher by 50 cm in 1988than in 1987

TABLE4. Percentsimilarity a of patchuse by mates.

Pairs in 1987 Pairs in 1988 4 9 4 9 • 11b 8 7 6 12b No. of visits 12 22 44 49 53 55 59 52 59 Timeforaging -- -- 35 42 27 48 54 32 52 ' Percentsimilarity (PS): PS = 1 - 0.5•;[pl - p21where pl andp2 reflect the use of a specificpatch by the male and female of a breedingpair respectively.Usewas measured byboth the percentage ofthe total number of visits to all patches and by the percentage oftime spent in a patch. • One memberof a pairforaged a proportionof its timein secludedbackwaters or sidetributaries. 786 DAVISAND GRAHAM [Auk,Vol. 108

TABLE5. (A) Pre-layingsupplemental food experimentconducted after 4 March in 1988.Results are shown relativeto Beforeand After the startof the experiment.Pairs marked with an asteriskreceived supplemental feedings.(B) Comparabledata on pairslaying eggsbefore 4 March.NA = not available.

Male CF performance Eggslaid? (min/CF) No.of CFs Observationtime(h[days]) Pair Before After After Before After Before After A. Pairs included in experiment 8* No Yes 26.5 1 20 44.2 [30] [10]a 5 No No -- 0 NA NA NA 7* No Yes 51.8 1 6b 37.7 [23] [3] 6 No No -- 1 NA 16.6 [11] NA 12' No Yes 65.8 6 17 20.9 [20] [14] 13 No No -- NA NA NA NA B. Pairslaying eggswithout help from supplementalfeeding 4 Yes -- 105.4 7 -- 32.9 [23] 9 Yes -- 95.5 12 -- 72.0 [38] 2 Yes -- 101.0 3 -- 6.7 [9] 11 Yes -- 77.7 14 -- 43.3 [26] Behaviorwas not systematicallyrecorded after foodwas supplied, therefore hours of observationare not reported. Femaleforaged from supplementalfeeding pond more than male. along the CascajalRiver. In 1988, frequent re- if mates fished from the same limited number movalof gravelfor roadrepair along the upper of sites,each bird mayunknowingly waste time sectionof territory 11 producedlarge quantities in a patch that has not recoveredfrom its last of silt during periods of low water level. Silt- disturbance.Partitioning of foragingsites has ation could accountfor no fish in territory 11 alsobeen reported in the BeltedKingfisher (Ce- (Table 3) and the lower fish countsand foraging ryle alcyon;Davis 1982). performancesrecorded from territories down- Courtshipfeeding.--Two hypotheses have been stream (8, 5, 7, 6, and 12) as comparedwith developed regarding courtship feeding: (1) territoriesupstream (2, 9, 4, and 15). courtshipfeeding is not criticalto egg produc- Disparity in territory quality is further in- tion but plays a vital role in the initiation or creasedby the use of foragingsites along trib- maintenance of bonds between mates (Lack utaries or backwaterpools. Although smaller 1940, Morley 1949, Tasker and Mills 1981) and tributariesoffer an abundantfood supply,Am- (2) courtshipfeeding providesessential nutri- azonKingfishers seldom nested along them be- ents required by femalesto lay eggs(Royarea causenests located in low banks,typically found 1966,Krebs 1970, Nisbet 1973). Both hypotheses along tributaries,are more vulnerableto pred- have merit. When food is abundant and needs atorsand flooding(Brooks and Davis 1987).The are low (or in large birds that lay a few small demand for safe nesting banks may result in eggs), courtship feeding appearsto be nutri- habitatsaturation along larger rivers, where fish tionally nonessentialfor laying females (Poole availabilityis not necessarilygreater than along 1985).On the other hand, in speciesfor which their tributaries.An irregular distribution of foragingis energeticallyexpensive, the energy nestingbanks could producea mosaicof ter- gained from courtship feeding by males may ritoriesthat differ in size and vary substantially trigger egglaying (Hunt 1980).Female Amazon in foragingsite quality (Davis 1982). Kingfisherswho received few courtshipfeed- Patchpartitioning and patchquality within ings in 1988 failed to lay eggsuntil fish were a territory may produceunequal access to food made available in artificial pools. When prey and, subsequently,a significantdisparity in for- becameavailable, courtship feedings substan- agingperformance between sexes. One possible tially increased,and eggswere laid within 3 to advantageof patchpartitioning by matesis an 4 weeks (Table 5). increasein total yield from their territory. This The nutrition hypothesisassumes that the is becausea significantrecovery period exists female'senergy budget is insufficientfor both after a dive during which fish are inaccessible self-maintenanceand egg formation.If so, one within a patch(5-10 rain; unpubl.data). Hence, would expect ovulating females to minimize October1991] FoodAccessibility andReproduction 787

250' 1.0

200' 0.8 o 150' 0.6 100' 0.4

50' oa

0 lg 3cl 4r 1 r 15 4 9 11 8 7 1987 ...... 1988Cascajal ...... Territory

8.5 5.7 3.8 7.7 5.3 6.9 11.4 1.9 3.6 6.6 Hours Observed Fig. 4. Nestlingfeeding rates. Right scale(proportion of total feedingtrips) refersto the stippledbars (malesonly). Left scale(biomass delivered; wet wt.) refersto the open (male)and solid (female)bars. Data from 1987are shownalong the left while datafrom 1988are shownon the right. The numberof hourseach nest was observedis shown along the bottom.

unnecessaryactivities to conserve energy. In courtshipfeeding may occur over a period of this study we observedthat as the date of egg monthsat levels too low to initiate laying. Low layingapproached, female kingfishers who were ratesof courtshipfeeding delay laying and may fed by their matesprogressively decreased the reducefledgling survival. Delayed nesting can time spent foraging and increasedtime spent increasethe chicks'vulnerability to floodsthat inactive. We proposedthat an energy saving is comeat the end of the breeding season.In 1987 realized by femaleswho stopforaging and rely and 1988 we recorded both egg and nestling on their mates for food (see Krebs 1970). De- creasedforaging by ovulatingfemales may also have functionsother than energy conservation. For example,an ovulating femalemay stopfor- aging becausethe act of diving to catcha fish could damagea developingegg. This possibil- ity, the "gravid female" hypothesis,has been usedto explain reducedactivity levels in other birds (Nisbet 1977, Newton 1979, Wheeler and Greenwood 1983). Males who display high courtshipfeeding performanceare more likely to sire offspring than poor performers for several reasons.First, a female may deserta male who is a poor pro- vider. We observed two cases in which a female switched to a neighboring bachelor male. A skewed sex ratio favoring males in our popu- lation (unpubl. data), may promote female de- 15 4 9 11 8 7 lg Territory sertion. Second,poor courtshipfeeding perfor- manceapparently inhibits egg laying. In 1988, Fig. 5. Delivery rate of fish during nestling aug- mentation. Open bars:control period; solid bar: food downstreampairs failed to lay eggsuntil they added; hatched bar: nestlings added. Missing bars were provided with supplementalfood (which indicate that neither parent fed from the artificial malesreadily used to increasetheir feedingrates; pool or that chickswere not added to the nest. Both Table 5). Apparently,during periodswhen fish sexeswere involved in feedingyoung, exceptfemale are readily available, courtship feeding is re- 11. Data from both sexeswere pooled to calculaterates stricted to a period of 2-3 weeks followed by for each pair tested.See text for data on the number egg laying, but when food is difficult to catch, of fish fed to nestlings. 788 DAVISAND GRAHAM [Auk,Vol. 108

mortality due to late flooding (also see Davis have a profound effect on their respectiveabil- 1980).Because laying occurred3-4 weeks later ities to catchfish and, hence, feed their young. in 1988 than 1987 (Fig. 3), it was the first nests thatwere destroyedby floodingin 1988,where- ACKNOWLEDGMENTS asonly secondattempts were destroyedin 1987. This study was conductedduring Davis' post-doc- Variablenestling feeding rate.--The effectof food toral fellowship at the SmithsonianTropical Research availabilityon parentalbehavior has been stud- Institute (STRI) in Panama. We thank Martin Moy- ied in the (Ceryle rudis; Reyer nihan for his supportand encouragementthroughout 1980, 1984;Reyer and Westerterp1985). Reyer the study and RichardCooke, who helped to identify and Westerterp(1985) report that the amount fish. The logistical support of STRI's staff was indis- of food delivered to nestlings by males was pensable,with specialthanks to Maria Luz Jimenez. strongly influenced by accessibilityto high- FranceMarcoux, Tom Gumbart,and Felicity Arrengo provided invaluable field assistance.Comments from quality prey. In our study,accessibility to prey Linda Mealey, Weyland Ezell, Peter Lent, Steve Em- also appearsto affect parental behavior. For ex- len, and two anonymousreviewers are also appreci- ample,we observeda dramaticrise in feeding ated. rateswhen food was made available during the nestlingaugmentation experiment. On the oth- LITERATURE CITED er hand, an increaseddemand achieved by add- ing chicksto nestsdid not significantlyaffect BART,J., & A. TORNES.1989. Importance of monog- amous male birds in determining reproductive either the proportion or amount of food deliv- success: evidence for House Wrens and a review ered to nestlingsby parents.Feeding rate ap- of male-removal studies. Behav. Ecol. Sociobiol. parently is controlled more by vagariesin food 24: 109-116. availabilitythan nestlingdemand. We conclud- BEISSINGER,$. R. 1986. Demography,environmental ed that the largevariability observedin nestling uncertainty,and the evolution of mate desertion feeding rate (Fig. 4) was likely causedby a het- in the Snail Kite. Ecology67: 144S-1459. erogeneousdistribution of fish within territo- 1987. Anisogamy overcome:female strate- ries, such that parents had unequal accessto gies in Snail Kites. Am. Nat. 129: 486-$00. fish. BROOKS,R. P., & W. J. DAVIS. 1987. Habitat selection by breeding Belted Kingfishers(Ceryle alcyon). We proposethat food constraintsimposed by Am. Midi. Nat. 117: 63-70. a variable and unpredictableenvironment is the DAVIES, N.B., & A. LUNDBERG. 198S. The influence principal factor selectingto maintain monog- of food on time budgetsand timing of breeding amy in C. amazona.Before laying, for example, of the Dunnock Prunella modularis. Ibis 127: 100- low or unpredictable food supply may limit a 110. male'sability to courtship-feedhis mate,as well DAVIS,W.J. 1980. The BeltedKingfisher: its ecology as restrict his ability to attend to additional fe- and territoriality. MS thesis. Cincinnati, Ohio, males.Later in the season,vagaries in food sup- Univ. Cincinnati. ply coupledwith a patchy distribution of for- ß 1982. Territory sizein A4egacerylealcyon along a stream habitat. Auk 99: 3S3-362. aging sitescan lead to low foragingperformance by one or both parents. If energy demands of DRENT,R. H., & S. DAAN..1980. The prudent parent: energetic adjustmentsin avian breeding. Ardea youngare high, low foragingperformances may 68: 228-282. force both parentsto provide food to nestlings HUNT,G.L. 1980. Mate selectionand matingsystems as opposedto searchingfor additional mating in seabirds. Pp. 113-144 in Behavior of marine opportunities. . Vol. 4, Marine birds (J. Berger, B. Olla, Parental investment theory cites various rea- and H. Winn, Eds.). New York, Plenum Press. sons for differencesin parental roles of males KALLANDER,H. 1973. Advancementof laying of Great and females. These include physiological sex Tits by the provision of food. Ibis 116: 36S-367. differences, differences in additional mating KREBS,J.R. 1970. The efficiencyof courtshipfeeding in the Blue Tit Parus caeruleu$. Ibis 112: 108-110. opportunities,scarcity of breeding habitat,and LACK,D. 1940. Courtshipfeeding in birds.Auk difference in prior investment in offspring 169-178. (Trivers 1972, Silver et al. 1985; also see refer- MAYNARDSMITH, J. 1977. Parental investment:a pro- ences in Winkler 1987). We propose that un- spectiveanalysis. Anita. Behav. 2S: 1-9. equal accessto food resourcesshould be added MORLEY,A. 1949. Observationson courtship-feed- to this list. The fact that mates exploit different ing and coifion of the Marsh-tit. Br. Birds42: 233- foraging patcheswithin their territory could 239. October1991] FoodAccessibility and Reproduction 789

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