The foraging performance of great and blue tits ... - Wiley Online Library

Journal of Animal Ecology 0888\ 57\ 697Ð607

The foraging performance of great and blue tits "Parus major and P[ caeruleus# in relation to caterpillar development\ and its consequences for nestling growth and ~edging weight BEAT NAEF!DAENZER and LUKAS F[ KELLER$ Swiss Ornithological Institute\ CH!5193 Sempach\ Switzerland^ and $Department of Ecology and Evolutionary Biology\ Princeton University\ Princeton NY 97433\ USA

Summary 0[ We analysed the e}ect of prey density and size on the foraging performance of great and blue tit "Parus major L[\ P[ caeruleus L[# parents\ and its consequences for the growth and ~edging weight of nestlings[ Because ~edging weight is a determinant of subsequent survival and therefore _tness\ foraging decisions of the parents play a key role in the reproductive system of tits[ The analysis quanti_es "i# the rate at which energy is delivered to the nestlings in relation to prey size and abundance\ and "ii# the growth rates of nestlings and the resulting ~edging weight in relation to the rate of food delivery by the parents[ 1[ The searching time per prey item increased exponentially with decreasing prey biomass[ During the peak abundance of caterpillars\ the average searching time per item was 1=4Ð2 min instead of 4Ð5 min before and after the peak[ Searching time was signi_cantly reduced when the birds returned to the foraging site where the preceding prey was found[ This accords with the clumped distribution of caterpillars within the canopy[ 2[ The foraging performance "in mg caterpillars per min# was maximal when cater! pillars were both abundant and large\ i[e[ shortly before they left the trees for pupation[ The high feeding frequency and the large prey then caused a peak energy ~ow rate to the nestlings of 3Ð4 times the rate before or after the caterpillar peak[ This suggests that the foraging success and rate of food delivery by tit parents was primarily determined by the abundance and size of prey[ 3[ The growth rate of nestlings\ as well as their ~edging weight was correlated with the rate of food delivery[ Low feeding performance of the parents resulted therefore in poor relative growth rates of only 9=2Ð9=5 of the rate achieved under optimal conditions and\ as a consequence\ in a low ~edging weight[ This indicates that tit parents have restricted options to adjust prey delivery rates according to the require! ments of the brood[ 4[ The results give insight into the chain of causal mechanisms through which an environmental factor "availability of food# has a strong and immediate e}ect on _tness "growth\ ~edging weight and\ thus\ survival of the nestlings#[ The importance of caterpillar size for foraging success and prey delivery rates of parent tits makes clear\ why the phase of best foraging conditions is shorter than the period during which caterpillars are available[ The relationships we quanti_ed give a proximate explanation for the great e}ects that temperature and caterpillar growth have on the between! year variation in selection intensity for laying date observed in other studies[ Key!words] blue tit\ ~edging weight\ foraging\ great tit\ nestling growth\ prey avail! ability\ radio!tracking\ timing of breeding[ Journal of Animal Ecology "0888# 57\ 697Ð607

Þ 0888 British Ecological Society

697

Correspondence] B[ Naef!Daenzer\ Swiss Ornithological Institute\ CH!5193 Sempach\ Switzerland

698 B[ Naef!Daenzer + L[F[ Keller

Þ 0888 British Ecological Society Journal of Animal Ecology\ 57\ 697Ð607

Introduction The timing of reproduction is of great importance in great and blue tits "Parus major and P[ caeruleus# because nestling food\ mainly caterpillars\ is abundant only for a short period[ Beginning to incubate the clutch a few days sooner or later may have con! siderable e}ects on nestling growth and ~edging weight\ and because ~edging weight is a determinant of subsequent survival\ on _tness "e[g[ Kluyver 0840^ Ricklefs 0872^ Tinbergen + Boerlijst 0889^ Gebhardt! Henrich + van Noordwijk 0880#[ Since nestlings com! pletely depend on parental e}orts the foraging per! formance of the parents is a main determinant of reproductive success\ and therefore a crucial link between environment and _tness[ There is selection for parents to time their repro! duction such that the period of peak food demand of their o}spring coincides with the peak of caterpillar availability "e[g[ Perrins 0854^ Tinbergen + Boerlijst 0889^ Noordwijk\ McCleery + Perrins 0884#[ However\ this period of very best foraging conditions is unpredictable for the birds[ The development of caterpillars is a}ected by short!time changes in ambi! ent temperature "e[g[ Perrins 0880\ and references therein#\ whereas the tits have limited options to delay or to accelerate their breeding after the start of incu! bation[ Thus\ short!time changes in temperature can shift the caterpillar peak relative to the timing of the broods "Noordwijk et al[ 0884#[ Between!year vari! ation in weather in the period between egg!laying and the time of peak energy demand "when nestlings are about 0 week old\ Betts 0844^ Balen 0862# causes selec! tion di}erentials for laying date to vary from year to year[ Noordwijk et al[ "0884# emphasize the great e}ect of a single factor\ the temperature after the start of laying\ on the between!year variation in selection intensity[ Understanding how such environmental factors lead to variation in selection\ however\ requires knowledge of the chain of causal mechanisms involved[ Because foraging adult titmice can hardly be observed visually under natural conditions "Smith + Sweatman 0863#\ there is little knowledge of these causal relationships[ In this paper\ we investigate the e}ects of the par! ents| foraging performance on the growth and ~edging weight of nestlings by using new radio!tracking tools[ We quantify searching times and prey delivery rates of tit parents in relation to prey density and size\ and identify the factors determining the energy ~ow to the nest which\ in turn\ is related to nestling growth[ We consider three levels of analysis in the present study[ 0[ The seasonal development of prey available to the tits[ 1[ The parents| searching time per feeding in relation to size and density of prey[ 2[ Nestling growth and ~edging weights in relation to the foraging performance of the parents[

Materials and methods Our analyses are based on data from a radio!tracking study conducted in 0878 and 0889 in an oak!rich deciduous forest near Basel\ Switzerland\ at 169 m asl[ During this study\ the abundance and spatial dis! tribution of caterpillars was recorded throughout the breeding season "Fischbacher\ Naef!Daenzer + Naef! Daenzer 0887#[ In parallel\ the resource selection and home!range use of radio!tagged birds was observed with high spatial resolution "Naef!Daenzer 0882\ 0883#[ In parallel\ data on nestling growth and ~edging weights were collected by the research group of A[ van Noordwijk\ University of Basel "e[g[ Gebhardt! Henrich + van Noordwijk 0880#[ For a detailed description of the study area see Mosimann et al[ "0876# and Gebhardt!Henrich + van Noordwijk "0880#[

NESTLING GROWTH

Approximately 299 nest boxes were inspected at least weekly during the breeding season and daily around the expected day of hatching to record the exact hatch! ing date[ Nestlings were marked individually at day 1 "hatching day 9# and weighed daily to the nearest 9=0 g[ Weighing started on day 1 and ended on day 04 to prevent premature ~edging due to the disturbance[ Weight changes from day 03 until ~edging are small "e[g[ Balen 0862# and the weights on day 04 were denoted as ~edging weight[ The parents were caught and weighed\ while feeding their young 6Ð01 days after hatching[ Winter weights were obtained during roosting inspections in November\ January and March[ Since the studies on nestling growth were focused on the great tit\ the results are based on 4915 weight measurements of great tits\ but only 168 of blue tits[ To evaluate the e}ects of parental performance on nestling growth\ we used a method for growth analysis described by Keller + van Noordwijk "0882\ 0883#[ The method quanti_es the growth rate as an index which is independent of age and actual size of the nestling\ and thus allows the comparison of the growth performance at di}erent ages[ In addition\ because this method accounts for the known genetic com! ponent of nestling growth in great tits\ it enables us to isolate the environmental e}ects on growth[ Details of the technique and its derivation are given in Keller + van Noordwijk "0882#[ Here\ we will only give a brief summary[ Actual daily growth is expressed rela! tive to the expected growth under good conditions[ Expected growth is calculated on the base of a Rich! ards growth function "White + Brisbin 0879#[ In order to include the known genetic variation in ~edging weight in this model we used the average winter weights of both parents as an estimator for the asymp! tote of the expected individual growth curves[ The

609 Foraging performance of great and blue tits

ratio of the realized over the expected growth "Rt# is independent of age and actual size\ and is used as an estimator of the environmental in~uences on growth during the time period over which Rt is calculated[ Rt equals 0 if a nestling grew as expected under good conditions[ Values of Rt below 0 indicate reduced growth due to some environmental in~uence and values greater than 0 can occur due to compensatory growth "van Noordwijk 0877# or estimation errors[ Rt ratios were calculated daily for each single nestling[ Because the time interval between consecutive measurements was usually not exactly 13 h\ the daily weight increments of nestlings were corrected for di}erences in interval length by linear interpolation[

RADIO!TRACKING OF TIT PARENTS


For great tits\ transmitters with a total mass of 899 mg and a life of 49Ð59 days were used[ Blue tits carried radio!tags of 519 mg\ running for 04Ð14 days[ The detection range of the transmitters was 199Ð399 m in dense vegetation and up to 0999 m in open areas[ The birds were trapped with mist nets mounted 9=4Ð0 m from the nest boxes when nestlings were 4Ð6 days old[ The radio!tags were glued into the feathers of the back\ using 39Ð49 mg of cyanoacrylate glue "Raim 0867^ Kenward 0876#[ All birds were released within 09Ð04 min of capture[ The birds adapted to the tags in 9=4Ð1 h and the transmitters remained on the birds| back for 1Ð19 days with a median of 5 days[ Trans! mitter speci_cations and technical details are given in Naef!Daenzer "0882\ 0883#[ The birds were located by triangulation from two _xed stations[ Each station consisted of two phase! shifted six!element Yagis on top of a 4=4Ð00=9 m pole[ The two antennas were positioned at a distance of 59Ð 099 m from each other and the nest box\ rendering the bearings from the central parts of the home!range most accurate "White 0874#[ Data were collected by two persons taking bearings simultaneously[ Fixes were taken once per minute^ if the birds were in ~ight or when the signal reception was disturbed\ it was not possible to get an exact direction within 4 s and bearings were classi_ed as unsuccessful[ The mean rate of successful bearings was 38 2 02)\ i[e[ 11Ð 26 locations per hour[ The triangulation errors were normally distributed with a standard deviation of 20=3>[ At 099 m observation distance\ this cor! responds to a standard deviation of the locations of 21=3 m and 84) of locations within 23=6 m\ respec! tively[ The departures and arrivals of the tagged birds from and at the nest were recorded by a commercial induc! tive switch mounted above the nest hole that was activated by the metal components of the transmitter[ An overview over the home!range size\ and overlaps of great and blue tit home!ranges is given in Naef! Daenzer "0883#[ Intervals between consecutive feed!

ings exceeding 19 min were considered as non!feeding activity and were excluded from the analysis[

CATERPILLAR SIZE AND BIOMASS

The food available was estimated by taking branch samples from the middle and upper canopy\ and by collection of caterpillar frass droppings "e[g[ Gibb 0849^ Tinbergen 0859^ Balen 0862^ Liebhold + Elkington 0877#[ Because of the large e}ort involved\ branch samples were only taken from 29 trees[ A large skylift with a maximum height of 24 m was used to reach the canopy[ Between 3 April and 29 May 0878\ and between 19 March and 2 June 0889\ two to six branch samples were taken weekly from each tree "01 oaks\ six beeches\ six hornbeams and six ashes#[ To calibrate the frass drop samples\ we collected frass droppings also from the same trees from which bran! ches were sampled "Fischbacher et al[ 0887#[ We used large plastic funnels with a diameter of 28 cm "approx[ surface 9=014 m1# to collect the frass droppings con! tinuously in 1Ð2 day fractions[ A total of 0345 branch samples and 634 frass drop samples were collected[ Before cutting\ the branches were wrapped in a trans! parent 799 L plastic bag[ The samples remained in these bags until further processing in the laboratory and were stored under the same temperature con! ditions as in the study area[ All samples were pro! cessed within 6 days after collection[ To count cater! pillars and other invertebrates\ the branches were cut up\ and caterpillars were picked from leaves and twigs[ Caterpillars were weighed to the nearest 0 mg\ and the density and biomass per m of twigs below a diameter of 0 cm was calculated[ Because caterpillar growth continued after the collection of the branches\ weights and densities were attributed to the date of processing "not to the sampling date#[ There was no signi_cant di}erence in growth rates in the bags compared to the _eld "R[ Meury + B[ Naef!Daenzer\ unpublished data#[ The spatial distribution of food in the home ranges of individual tits was assessed by additional col! lections of frass droppings below each individual tree in the home!range of the radio!tracked birds[ For a total of another 590 trees\ frass samples were collected in 1!day fractions[ All frass samples were dried for 01 h\ cleaned from debris and the frass fraction weighed to the nearest 0 mg[ Caterpillar frass drop! ping rates were transformed into biomass per m of branches following the equation given by Fischbacher et al[ "0887#[

ANALYSIS OF FORAGING DATA

In order to quantify caterpillar growth\ we averaged the caterpillar weights for consecutive 1!day periods[ The rare\ but extremely large "×0999 mg# caterpillars of some noctuid species were excluded to avoid biased results[ A growth curve was _tted to these data using

Results CATERPILLAR SIZE AND BIOMASS


The seasonal maximum in mean caterpillar mass in oaks was about 39 mg and was reached mid!May in 0878 and 0889 "Fig[ 0a#[ The growth curves\ however\ di}ered considerably between the consecutive years[ In 0889 the development of caterpillars was restrained by cold weather during April[ However\ from the beginning of May the caterpillars grew very fast and reached the _nal mass within 1 weeks[ The decrease of the average mass after the maximum is due to the appearance of early instars of insect species that hatch later in the season\ not a decrease in mass of individual caterpillars[ There were also considerable di}erences in caterpillar density and its seasonal development "Fig[ 0b#[ After caterpillars had reached the maximum size of ¼39 mg at the last instar\ the densities on trees decreased quickly because the most abundant species ðe[g[ the winter moth "Operophtera brumata L[#Ł pup! ate in the ground[ We observed a large spatial variance in the prey

60 Mean caterpillar mass (mg)

a moving average smoothing algorithm given by Vel! leman "0879#[ These _tted values were denoted as mean caterpillar mass[ Oaks contain up to 09 times the biomass of caterpillars compared with other tree species "Keller + van Noordwijk 0883# and were highly preferred by the foraging titmice[ Therefore\ we restricted the analyses to the growth of caterpillars in oak[ After catching a prey\ great and blue tits return directly to the nest "Smith + Sweatman 0863\ authors| personal observation#[ We therefore considered the last radiolocation preceding a visit at the nest as the foraging site where a prey was found[ If the last radio! location of a trip was less than 2 m from the last location of the preceding trip\ we considered the bird to have returned to the same foraging site[ In total\ 89) of locations were within 34 m from the nest[ Thus\ the ~ight time to and from the foraging sites was a few seconds only[ We found no correlation between the duration of feeding intervals and the dis! tance from the nest "r 9=93 for great tits\ r 9=98 for blue tits#[ Therefore\ the interval between feedings is a reasonable estimate of searching time[ Since single foraging ~ights could not be correlated with actual caterpillar availability\ all data on caterpillar bio! mass:size\ searching time and nestling growth rates were averaged over the same 1!day intervals used for frass collection[ Because the radio!tracking data pro! vide detailed information from a small number of individuals "09 great tit and seven blue tit nests#\ we combined great and blue tit data to analyse foraging sites and searching times[ The e}ects of food delivery rates on nestling growth and ~edging weight were analysed separately for great and blue tits\ respec! tively[

(a) 50 40 30 20 10 0

Mean caterpillar density (n m–1)


>14

(b)

12 10 8 6 4 2 0 20 25 30 35 40 45 50 55 60 65 70 75 80 85 Date, 1 = 1 Mar. 25 1 5 10 March April

20

30

5 10 May

20

Fig[ 0[ "a# Seasonal development of average caterpillar mass on oaks in 0878 "circles\ dotted line# and 0889 "dots and solid line#[ Maximum size was equal in both years\ but the growth curves di}ered considerably due to weather conditions[ "b# Seasonal development of average caterpillar density per m of twigs below 0 cm diameter in 0878 "circles\ dotted line# and 0899 "dots\ solid line#[ Points give averages for consecutive 1! day intervals\ lines were _tted using a moving!average algo! rithm[ For details see text[

biomass available to the birds\ as well as in the sea! sonal development of caterpillars in neighbouring ter! ritories[ Figure 1 gives the mean caterpillar biomass per m of twigs calculated from frass dropping rates of all trees within a 19!m radius of four neighbouring nests "all within a 0!ha plot#[ Both the amplitude and duration of the peak show great local di}erences in the phenology of caterpillar development[ For example\ compared to box 906\ the maximum prey availability of food at box 260 is only about 59) and the peak occurs 0 week earlier[ All curves are of a trimodal shape which re~ects the development of the three taxa forming the largest proportion of prey biomass[ The earliest peak was caused by Geometridae\ mainly the winter moth[ The second peak re~ects the biomass maximum of tortricidae "Tortrix sp[#\ whereas the latest peak was due to larger lepidoptera such as noc! tuids "R[ Meury\ unpublished data#[ SEARCHING EFFORT AND FORAGING PERFORMANCE IN RELATION TO PREY BIOMASS AND SIZE

In accordance with the _ndings by Tinbergen "0859# and Smith + Sweatman "0863#\ we observed the tit

150

60 Great tit Blue tit 50

120

–1

Mean caterpillar biomass (mg m )

40 Frequency (%)

90 017

60

372

371

10 0 55

60

65 70 75 Date, 1 = 1 Mar.

80

85

Fig[ 1[ Seasonal development of caterpillar biomass given for four neighbouring nest boxes in a 0!ha plot[ There is con! siderable small scale variance in the date and the amplitude of peak caterpillar abundance[ Curves give the average biomass over the trees within a 19!m radius from the nests as assessed by collection of frass droppings[ Numbers represent nest box numbers[


30

20

373

30

parents to make series of consecutive catches at the same location[ Although radiolocations provide lim! ited information on the exact position of the bird "¼1=3 m horizontally and no vertical information# vis! ual observations using hand!held antennas suggest that often the same branch of a tree was visited[ More than 49) of the sites were visited only once\ however\ up to nine consecutive visits at a location were observed[ The frequency distribution of the number of repeat visits is given in Fig[ 2[ Fourteen per cent of the ~ights were _rst returns to the preceding site[ Three and more visits at the same site occurred rarely[ In total\ repeated visits to a site amounted to 16=8 and 17=3) of the known locations for great and blue tits\ respectively[ In order to compare the frequency dis! tribution of the number of repeat visits with the small scale spatial distribution of caterpillars we analysed the number of caterpillars found in branch samples of less than 099 cm twig length[ In these 35 samples\ the frequency distribution of the number of caterpillars found is similar to the frequency distribution of run length of birds "Fig[ 2#[ This may indicate that the tits returned to places where small groups of caterpillars were found[ However\ the spatial resolution in both caterpillar distribution and bird location patterns does not allow for a detailed analysis of this aspect[ The searching time per food item was determined to a great extent by the average prey biomass in the respective territories[ Figure 3[ gives the relationship between prey biomass and mean searching time for newly chosen sites\ and for returns to the preceding foraging site\ respectively[ The statistical analysis was

0 1

2 3 4 5 6 7 8 9 unknown Bars: number of consecutive visits Line: number of caterpillars

Fig[ 2[ Frequency distribution of the number of consecutive successful visits at one foraging site[ Black columns] great tit "n 0475 visits#\ grey columns] blue tit "n 0434 visits#[ The line gives the frequency distribution of caterpillar numbers in branch samples of less than 099 cm twig length "n 35#[

7

6 Mean searching time (min)


5

4

3

2

1

0 0

100 20 40 60 80 Caterpillar biomass (mg m–1)

Fig[ 3[ Average time intervals between consecutive feedings of great and blue tits "{searching time|# in relation to cater! pillar biomass available within a 19!m radius of the nest[ Dots and solid line] _rst visits "y 8=4x−9=16\ r −9=56#[ Circles and dotted line] returns to the preceding foraging site "y 2=1x−9=06\ r −9=35#[ For statistical analysis see Table 0[

done by multiple regression using prey density and size separately\ and is given in Table 0[ Searching at a new or at the preceding place was introduced as a


Table 0[ Multiple regression of the searching time per foraging ~ight of adult great and blue tits on caterpillar density and size "both log!transformed#\ accounting for searches at new sites or returns to the preceding site\ respectively

Constant ln "mean caterpillar mass\ mg# ln "mean caterpillar density\ n m−0# Dummy variable Return to preceding site 9 Search at a new place 0

Coe.cient "SE#

t "46#

P

5=36 2 9=71 −0=32 2 9=14 −9=34 2 9=04

6=76 −4=60 −2=97

³9=9990 ³9=9990 9=992

1=32 2 9=13

8=84

³9=9990

Dependent] searching time per prey item[ n 50 1!day!periods\ R1adj[ 9=57\ F2\46 33=16\ P ³ 9=9990[


–1

8 120 6 90

4 60

2

30 1989

0 55

Lines: mean caterpillar biomass (mg m )

150 Symbols: mean searching time (min ± SD)

dummy variable to test for the e}ect of searching at a preceding site "0 new place\ 9 preceding place#[ On one hand\ we detected an exponential decrease of the searching time with increasing average caterpillar biomass "Fig[ 2#[ When the available biomass was below 19 mg m−0\ i[e[ 9=4Ð0 caterpillar m−0\ the mean searching time per item could be as long as 3Ð5 min[ In contrast\ at high prey availabilities average searching times were around 1=4 min[ Both caterpillar density and size "the components of biomass# had signi_cant e}ects on the average searching time "Table 0#[ Fur! thermore\ the average searching time was reduced by 1=3 min when the birds returned to the preceding site[ In this case\ the feeding intervals were often below 1 min[ The multiple analysis explains 57) of the vari! ance in searching time[ The proportion of variance in searching times explained by caterpillar density and size was 33) for _rst visits\ and 07) for returns to the preceding site\ respectively[ Therefore\ foraging success during series of visits at the same site was much less a}ected by the average caterpillar density than in _rst visits "Fig[ 2#\ which indicates that small! scale concentrations of caterpillars were exploited[ As a result of the seasonal changes in prey size and density "Fig[ 0#\ there was a remarkable reduction of the searching e}ort during the peak abundance of caterpillars "Fig[ 3#[ Compared to the time before and after peak abundance\ the reduction in average search! ing time was ¼39)[ This indicates that the devel! opment of caterpillar populations may have a two! fold impact] _rst\ the rate at which food is delivered to the nest depends on density and size of prey[ There! fore\ these environmental variables directly a}ect the growth conditions for the nestlings[ Secondly\ increas! ing searching e}ort when prey is rare and:or small may impact the parents| costs to satisfy the requirements of the brood[ There is evidence that brood size also had an e}ect on the observed average feeding intervals "Fig[ 5\ ANOVA\ d[f[ 4\ F 01=89\ P ³ 9=9990#[ This indi! cates that the parents feeding large broods made an e}ort to increase their feeding rates in order to ful_l the larger requirements of the brood[ However\ this reduction was not proportional to the number of nest!

1990 60

65

70 75 80 Date, 1 = 1 Mar.

85

0

90

Fig[ 4[ Average time intervals between consecutive feedings of great and blue tits in relation to the seasonal changes in caterpillar biomass in 0878 "squares# and 0889 "circles#[ Bars indicate standard deviations[ Solid symbols] _rst visit of a site[ Open symbols] unknown foraging sites[

lings[ The mean interval between feedings of about 2=1 min in large broods "6Ð09 nestlings# is similar to the minimum searching time realized when prey biomass was very high "Fig[ 5#[ In addition to the increased feeding rate parents with large clutches also could have compensated by foraging for a longer pro! portion of the day[ Unfortunately\ we have no data on the total proportion of the day spent for foraging at disposition[ Furthermore\ the sample of broods is small and the observation period per brood was only a few days[ This makes it impossible to discriminate seasonal and brood size e}ects statistically[

NESTLING GROWTH AND FLEDGING WEIGHTS IN RELATION TO FORAGING PERFORMANCE

The main factor for the growth of the nestlings is the rate at which energy "in mg caterpillars min−0#

6

5 Mean searching time (min)


4

3

2

1

0

4

5

6

7

9

10

Brood size Fig[ 5[ E}ect of brood size on the average time between con! secutive feedings[ Bars indicate standard errors[ Feeding intervals in large broods were smaller\ but the reduction was not proportional to the number of nestlings\ which indicates that the parents could not achieve the feeding rate required by large broods[


is delivered to the nest[ Given the strong e}ect of caterpillar size and density on searching time\ and therefore feeding intervals\ we assume that these results are representative for all broods in the forest[ For all 1!day intervals where nestling weights were recorded\ we calculated the expected prey delivery rates following the equation given in Table 0 and using the average caterpillar density and size at a given date "considering both species being single prey loaders\ and that 29) of all foraging ~ights were returns to the preceding site#[ Furthermore\ we considered that great tits were highly selective for large caterpillars[ In a comparison of nestling diet and prey availability in 0889 in the same area\ Naef!Daenzer\ Naef!Daen! zer + Nager "unpublished data# have found that the average mass of the caterpillars in the diet was 1=5 times the mean mass of caterpillars available in the trees[ The expected prey delivery rate is therefore expressed as 1=5 "average caterpillar mass:expected search time#[ The resulting expected delivery rates range from 7 to 35 mg min−0 per parent[ We found a positive relationship between the expected prey delivery rate\ and the average growth rate of great and blue tit nestlings "y 9=06 ¦ 9=902x\ r 9=47\ n 23\ P ³ 9=990\ data of great and blue tits pooled\ Fig[ 6a#[ Growth rates close to those expected under ideal conditions "Rt 0=9# were reached if more than 24Ð39 mg min−0 were delivered per parent[ With lower delivery rates\ the relative growth rates dropped rapidly to less than 9=4[ Furthermore\ there was a strong correlation between ~edging weight and foraging performance of the parents[ The relationship corresponds to a logistic curve with an asymptote of 05=6 g for great tits

"y 05=7:ð0 ¦ exp "9=42Ð9=01 = x#Ł\ r 9=67\ n 13\ P ³ 9=990^ Fig[ 6b#[ For the blue tit there was a similar trend[ Since only seven 1!day intervals with ~edging weights were available\ no function was _tted to these data "two out!laying blue tits of only 5=1 g each were excluded from the analysis#[ In the great tit\ a prey delivery rate of less than 19 mg min−0 per parent resulted in very low ~edging weights of 00Ð02 g[ This is close to the minimum mass at which a great tit can ~edge[ Fledging weights below 02 g were rarely observed ðin our study n 03 "2=2)# out of "303#Ł[ Juveniles of such poor condition are likely to starve before ~edging[ According to these results there was remarkable seasonal variation in the average ~edging mass of great tits[ In both years ~edging weights were maximal from day 64Ð74 "mid!May\ Fig[ 7#\ when caterpillar size was maximal\ although density had already declined at that time[

Discussion Our results con_rm the notion advocated by Drent + Daan "0879# that variation in food availability has a pervasive in~uence on reproductive performance[ This corresponds with the _ndings of several other studies that document the e}ects of food abundance on nest! ling growth and ~edging weights "e[g[ Balen 0862^ Bryant 0864\ 0867^ Perrins 0880^ Keller + van Noord! wijk 0883#[ Experimental studies have also demon! strated that nestling growth performance is positively correlated to food availability "e[g[ Hogstedt 087^ Smith + Arcese 0877^ Simons + Martin 0889#\ and that tits readily respond to spatial and temporal vari! ation in prey size and density "Smith + Dawkins 0860^ Smith + Sweatman 0863#[ Our study supports these _ndings\ and provides quantitative models of the mechanisms that relate nestling growth and the result! ing ~edgling condition to food availability[ In addition\ our data illustrate that analysing the proximate controls of reproductive performance by local food supply can be a successful way to under! stand how reproductive traits of a species are shaped by food supply as an ultimate factor that _nally a}ects survival[ The proximate e}ects of food availability on foraging performance\ and thus nestling growth presented here explain why a di}erence in timing even of a few days between the peak food availability and the peak energy requirements of a brood lead to di}erences in reproductive success\ and consequently\ to large selection di}erentials "Perrins 0880^ Nager + van Noordwijk 0884^ van Noordwijk et al[ 0884#[ A brood of tits is ideally timed if the nestlings are 09Ð07 days old when the caterpillars reach their maximum size\ but have not yet left the trees for pupation[ Such broods receive a boost of energy allowing a large number of well conditioned young "up to 02 in our study area# to ~edge\ which would be impossible before and after the caterpillar peak[ Van

18


(b)

(a)

1

16

Mean fledging mass (g)

Mean relative growth rate (Rt)

0.8

0.6

0.4

0.2

14

12

10

8

0

–0.2

6 5

10

15

20

25

30

35

40

45

5

10

15

20

25

30

35

40

45

Foraging performance (mg min–1) Fig[ 6[ "a# Correlation of the relative growth rate Rt of blue and great tit nestlings with the rate of food delivery to the nest[ Dots great tit[ Circles blue tit[ Age of nestlings ×7 days[ y 9=06 ¦ 9=902x\ r 9=47\ n 23\ P ³ 9=990\ data of both species pooled#[ "b# Fledging weight of blue tit "circles# and great tit "dots# nestlings in relation to the rate of food delivery to the nest[ The logistic curve _tted to great tit data has the equation y 05=7:ð0 − exp "9=42Ð9=01x#Ł\ r 9=67\ n 13[

Mean fledging mass (g)

18

16

14

12

10 55

60

65

70 75 80 Date, 1 = 1 Mar.

85

90

Fig[ 7[ Average ~edging weight of great tits in 0878 "circles# and 0889 "dots# in relation to date[ Dotted line 0878] y −54=14 ¦ 1=04x−9=903x1\ R1 9=73\ n 00[ Solid line 0889] y −67=75 ¦ 1=25x−9=904x1\ R1 9=71\ n 02[ Fledging mass was maximal when caterpillars were large\ but had not yet left the trees for pupation[ See also Fig[ 0[


Noordwijk et al[ "0884# demonstrated that these broods\ indeed\ provide a large proportion of the recruits in the next breeding season[ However\ weather conditions after the onset of incubation\ local variance in the development of caterpillar populations "Fig[ 1#

and other unpredictable environmental factors may shift the caterpillar peak in relation to the average onset of breeding[ Thus\ there is considerable variance in the cohort of breeding birds that take most pro_t of the caterpillar peak[ These relationships are contrasted by studies reporting that the juvenile survival declines with ~edging date "Kluyver 0840^ Perrins 0854\ 0869#\ indi! cating that juveniles from early broods survive better\ even if they do not pro_t from best feeding conditions[ Analysing long!term data from Vlieland and the Hoghe Veluwe\ Verboven + Visser "0887# found a signi_cant e}ect of both date and ~edging weight on the local recruitment rates of juvenile great tits[ Although the causal explanation for a date!related e}ect is unclear\ this indicates that other environ! mental factors also a}ect juvenile survival and may counteract selection for having the chick!rearing per! iod coincide with maximum food availability[ Prob! ably these factors concern the post!~edging period and the survival of juveniles during winter[ Our data are not free of some drawbacks[ The time between two feedings of an individual bird is only a rough estimate of searching e}ort[ We observed tits to make excursions out of the territories "often to take a bath# or to stop feeding for 29Ð59 min[ Nonetheless\ the very large number of feedings per day "Gibb 0844^ Balen 0862# and visual observations "Smith + Sweat! man 0863^ personal observation# indicate that vir! tually all of the time between feedings is spent search! ing for prey during feeding activity[ Another handicap



is that taking bearings once a minute gives not a very detailed representation of a bird|s foraging track "Naef!Daenzer 0883#[ This makes it impossible to assess the small scale patterns in the searching behav! iour and to quantify exactly where which amount of searching e}ort was allocated[ In particular\ we provide no information on those sites where tits sear! ched unsuccessfully and then moved on[ Because the total searching e}ort between feedings may include visits of more than one site\ standard models of patch use decisions do not apply to these data[ Hence\ the analysis is focused on the searching e}ort of tit parents and the resulting energy ~ow to the nest in relation to variation in prey abundance and size on the level of bird territories\ and during the season[ These mechanisms are striking in several aspects[ It appears that a large proportion "57)# of the variation in searching time per food item was deter! mined by the density and size of caterpillars\ on one hand\ and by their small scale spatial distribution\ on the other[ This functional response causes con! siderable seasonal changes in the energy ~ow to the nest\ but also a}ects the overall searching e}ort of the parents[ Birds having their brood when prey biomass is maximal save about 39) in searching e}ort\ com! pared to broods raised before or after the peak[ This may have a considerable impact on the total costs of reproduction[ In accordance to results given by Smith + Sweatman "0863# we observed a high selectivity in space for short time intervals[ In about 29) of the records with known location\ the birds had returned to the preceding site to catch another prey[ The frequency distribution of the length of series of visits is strikingly similar to the data given in Smith + Sweatman "0863\ p[ 0115# and accords to the clumped distribution of caterpillars[ Although up to nine visits were made at the same site\ runs of several visits were rarely observed\ which is consistent with the observation that rarely more than _ve caterpillars were found on one twig[ Returning to the preceding site yields to the birds a considerable {gain| in searching e}ort[ During repeated visits\ the average searching time is reduced by 1=3 min[ We conclude from our results that most tit parents come close to achieving the maximum rate of prey delivery that is possible at a given prey density[ There! fore\ the adult birds may not be able to provide su.cient food to their nestlings when prey availability is low\ despite their e.cient use of resources[ When the searching e}ort is high "before and after the caterpillar peak# the parents have to work harder to satisfy the requirements of the brood[ This is in accordance with observations of Balen "0862# who has demonstrated that a small average prey size is compensated by a larger total number of feedings per day[ As a conse! quence\ the timing of breeding in relation to the cater! pillar peak may also have considerable e}ects on the total costs of reproduction\ condition and survival of the parents "see also Nur 0873\ 0875#[

Because the parents are not free to increase their feeding rate when the brood requires more food\ chan! ges in prey availability have an immediate e}ect on the growth of the brood[ Relative growth rates of 9=7 and more were measured\ where about 39 mg:min was delivered by each of the parents[ Under these con! ditions the ~edging weight reached a constant level of 05=7 g[ A reduction of the delivery rate to 04 mg:min per parent resulted in a dropping of the relative growth rate down to 9=3[ Under such poor conditions the ~edglings reached a _nal weight of 02Ð03 g only[ In comparison with data given by Tinbergen + Boerlijst "0889# and Verboven + Visser "0887# this indicates a considerable reduction in the expected survival of those nestlings] full grown "06 g# nestlings at Hoghe Veluwe were recaptured in the next breeding season with a probability of 9=05[ In contrast\ the recapture rate of nestlings with a ~edging mass of 02Ð03 g was below 9=94 "Tinbergen + Boerlijst 0889] 0007\ Fig[ 1#[ From this comparison\ we conclude that the survival of juvenile birds is causally a}ected by the energy!~ow to the brood during the nestling phase[ Most "but not all# experimental manipulations of brood size reported reduced growth and body mass of ~edglings in enlarged broods "Dijkstra et al[ 0889#[ For birds with similar feeding ecology\ our results from great and blue tits provide an explanation of the causal mechanism involved[ Parents simply are not able to increase food delivery su.ciently to satisfy the increased energy demand of enlarged broods[ Our data suggest that this is the consequence of the quan! tity of food available to the birds and not of a lack of parental e}ort] both great and blue tits with large broods did decrease their searching times signi_cantly\ but not proportional to brood size "Fig[ 5#[ The large seasonal variation in food availability and the inability of parents to compensate for it has implications for the interpretation of brood size manipulation experiments with similar variation in seasonal food availability[ In such systems\ the e}ects on reproductive success of the large seasonal ~uctuations in food availability are likely to be much larger than the e}ects of the manipu! lations[ This was\ indeed\ observed by Gebhardt!Hen! rich "0889# and Gebhardt!Henrich + van Noordwijk "0880# who performed brood size manipulations in the same population for which we presented data here[ Under such conditions\ negative results of brood size manipulation experiments both in their e}ects on o}! spring and parents "costs of reproduction# can only be interpreted if data are available that show that the experiment did\ in fact\ signi_cantly alter the con! dition experienced by the nestlings and:or the parents[ Moreover\ it is likely that some of the observed vari! ation among populations and species in their response to brood size manipulation experiments "Dijkstra et al[ 0889# or hostÐparasite interactions "Richner et al[ 0882^ Christe et al[ 0885# could be explained by small!scale and seasonal variation of food abundance in the di}erent habitats[


Acknowledgements We gratefully acknowledge the co!operation with A[ N[ van Noordwijk\ N[ Zbinden and H[ P[ P_ster[ S[ Gebhardt!Henrich and R[ Nager assisted in the collection of growth data[ Radio!tracking in the _eld was carried out by M[ Fischbacher\ S[ and P[ Abeg! glen\ J[ Barandun\ E[ Benelli\ Th[ Degen\ M[ Donatz\ A[ Hediger\ M[ Impekoven\ S[ Krahenmann\ R[ Naef\ M[ Nuber\ M[ Roost\ R[ Rutishauser\ F[ Widmer[ The following companies gave technical support] Quarz AG\ Monchaltorf\ Philips AG Zurich\ Fenner AG Sissach "electronics#^ Wicker and Burki AG\ Rumlang "tracking antennas and poles#[ Two reviewers\ A[ N[ van Noordwijk\ R[ G[ Nager and N[ Zbinden gave very helpful comments on the manu! script[ The project was _nancially supported by the Swiss National Science Foundation\ Grant no[ 2=042Ð 0=77 and the Karl Mayer Foundation[ Capture and tagging of the animals was approved by the Swiss Federal Department of Forestry and Environment[ Transmitters and receiving equipment was licensed by the Swiss Federal PTT "PTT!801995:81093#[

References


Balen\ H[\ van "0862# A comparative study of the breeding ecology of the great tit "Parus major# in di}erent habitats[ Ardea\ 50\ 0Ð82[ Betts\ M[ "0844# The food of titmice in oak woodland[ Jour! nal of Animal Ecology\ 13 "1#\ 171Ð212[ Bryant\ D[M[ "0864# Breeding biology of house martins "Delichon urbica# in relation to aerial insect abundance[ Ibis\ 006\ 079Ð105[ Bryant\ D[M[ "0867# Environmental in~uences on growth and survival of nestling house martins "Delichon urbica#[ Ibis\ 019\ 160Ð172[ Christe\ Ph[\ Richner\ H[ + Oppliger\ A[ "0885# Begging\ food provisioning\ and nestling competition in great tit broods infested with ectoparasites[ Behavioral Ecology\ 6\ 016Ð020[ Dijkstra\ C[\ Bult\ A[\ Bijlsma\ S[\ Daan\ S[\ Meijer\ T[ + Zijlstra\ M[ "0889# Brood size manipulations in the kestrel "Falco tinnunculus#] e}ects on o}spring and parent survival[ Journal of Animal Ecology\ 48\ 158Ð174[ Drent\ R[H[ + Daan\ S[ "0879# The prudent parent] energetic adjustments in avian breeding[ Ardea\ 57\ 114Ð141[ Fischbacher\ M[\ Naef!Daenzer\ B[ + Naef!Daenzer\ L[ "0887# Estimating caterpillar densities on trees by col! lection of frass droppings[ Ardea\ 75\ 010Ð018[ Gebhardt!Henrich\ S[ "0889# Temporal and spatial variation in food availability and its e}ect on ~edgling size in the great tit[ Population Biology of Passerine Birds "eds J[ Blondel\ A[ Gosler\ J[ Lebreton + R[ McCleery# pp[ 064Ð 075[ Springer\ Heidelberg[ Gebhardt!Henrich\ S[ + van Noordwijk\ A[J[ "0880# Nestling growth in the great tit[ I[ Heritability estimates under de}erent environmental conditions[ Journal of Ecological Biology\ 2\ 230Ð251[ Gibb\ J[ "0849# The breeding biology in the great and blue titmice[ Ibis\ 81\ 496Ð428[ Gibb\ J[ "0844# Feeding rates of great tits[ British Birds\ 37\ 38Ð47[ Hogstedt\ G[ "0870# E}ect of additional food on reproductive success in the magpie Pica pica[ Journal of Animal Ecology\ 49\ 108Ð118[

Keller\ L[F[ + van Noordwijk\ A[J[ "0882# A method to isolate environmental e}ects on nestling growth\ illus! trated with examples from the great tit "Parus major#[ Functional Ecology\ 6\ 382Ð491[ Keller\ L[F[ + van Noordwijk\ A[J[ "0883# E}ects of local environmental conditions on nestling growth in the great tit Parus major L[ Ardea\ 71\ 238Ð251[ Kenward\ R[ "0876# Wildlife Radio Tagging[ Academic Press\ London[ 111 pp[ Kluyver\ H[ "0840# The population ecology of the great tit\ Parus major[ Ardea\ 28\ 0Ð024[ Liebhold\ A[M[ + Elkington\ J[S[ "0877# Estimating the den! sity of larval gypsy moth\ Lymantria dispar\ using frass drop and frass production measurements] sources of vari! ation and sample size[ Environmental Entomology\ 06\ 132Ð 153[ Mosimann\ P[\ Naef!Daenzer\ B[ + Blattner\ M[ "0876# Die Zusammensetzung der Avifauna in typischen Waldge! sellschaften der Schweiz[ Orn Beob\ 73\ 164Ð188[ Naef!Daenzer\ B[ "0882# A new transmitter for small animals and enhanced methods of home!range analysis[ Journal of Wildlife Manage\ 46\ 579Ð578[ Naef!Daenzer\ B[ "0883# Radiotracking of great and blue tits] new tools to assess territoriality\ home!range use and resource distribution[ Ardea\ 71\ 224Ð236[ Nager\ R[ + van Noordwijk\ A[J[ "0884# Proximate and ultimate aspects of phenotypic plasticity in timing of great tit breeding in a heterogeneous environment[ American Naturalist\ 035\ 343Ð363[ Noordwijk\ A[J[\ van "0877# Sib competition as an element of genotypeÐenvironment interaction for body size in the great tit[ Population Genetics and Evolution "ed[ G[ de Jong#\ pp[ 013Ð026[ Springer Verlag\ Berlin[ Noordwijk\ A[J[\ van\ McCleery\ R[H[ + Perrins\ C[M[ "0884# Selection for the timing of great tit breeding in relation to caterpillar growth and temperature[ Journal of Animal Ecology\ 53\ 340Ð347[ Nur\ N[ "0873# The consequences of brood size for breeding blue tits[ I[ Adult survival\ weight change and the cost of reproduction[ Journal of Animal Ecology\ 42\ 368Ð385[ Nur\ N[ "0875# Is clutch size variation in the blue tit "Parus caeruleus# adaptive< An experimental study[ Journal of Animal Ecology\ 44\ 872Ð888[ Perrins\ C[M[ "0854# Population ~uctuations and clutch size in the great tit "Parus major L[ # Journal of Animal Ecology\ 23\ 590Ð536[ Perrins\ C[M[ "0869# The timing of birds| breeding seasons[ Ibis\ 001\ 131Ð144[ Perrins\ C[M[ "0880# Tits and their caterpillar food supply[ Ibis\ 022 "Suppl[ 0#\ 38Ð43[ Raim\ A[ "0867# A radio transmitter attachment for small passerine birds[ Bird!Banding\ 383\ 216Ð221[ Richner\ H[\ Oppliger\ A[ + Christe\ Ph[ "0882# E}ect of an ectoparasite on reproduction in great tits[ Journal of Ani! mal Ecology\ 51\ 692Ð609[ Ricklefs\ R[E[ "0872# Avian postnatal development[ Avian Biology\ Vol[ 6 "eds D[S[ Farner + J[R[ King# pp[ 0Ð72[ Academic Press\ London[ Simons\ L[S[ + Martin\ T[E[ "0889# Food limitation of avian reproduction] an experiment with the cactus wren[ Ecol! ogy\ 60\ 758Ð765[ Smith[ J[N[M[ + Arcese\ P[ "0877# E}ects of supplemental food on growth and adult size in the song sparrow[ Pro! ceedings of the XIX International Ornithological Congress Ottawa\ 1\ 0305Ð0312[ Smith\ J[N[M[ + Dawkins\ R[ "0860# The hunting behaviour of individual great tits in relation to spatial variations in their food density[ Animal Behavior\ 08\ 584Ð695[ Smith\ J[N[M[ + Sweatman\ H[P[A[ "0863# Food!searching behaviour of titmice in patchy environments[ Ecology\ 44\ 0105Ð0121[



Tinbergen\ L[ "0859# The natural control of insects in pine! woods[ I[ Factors in~uencing the intensity of predation by songbirds[ Archives of Neerlands Zoology\ 02\ 154Ð232[ Tinbergen\ J[M[ + Boerlijst\ C[M[ "0889# Nestling weight and survival in individual great tits "Parus major#[ Journal of Animal Ecology\ 48\ 0002Ð0016[ Velleman\ P[F[ "0879# De_nition and comparison of robust nonlinear data smoothing algorithms[ Journal of the Amer! ican Statistical Association\ 64\ 598Ð504[ Verboven\ N[ + Visser\ M[ "0887# Seasonal variation in local

recruitment of great tits] the importance of being early[ Oikos\ 70\ 400Ð413[ White\ G[C[ "0874# Optimal locations of towers for tri! angulation studies using biotelemetry[ Journal of Wildlife Management\ 38\ 089Ð085[ White\ G[C[ + Brisbin\ I[L[\ Jr "0879# Estimation and com! parison of parameters in stochastic growth models for barn owls[ Growth\ 33\ 86Ð000[ Received 07 September 0886^ revision received 11 September 0887