Effects of Population Density and Supplemental Food on Reproduction in Song Sparrows

Author(s): Peter Arcese and James N. M. Smith

Reviewed work(s):
Source: Journal of Animal Ecology, Vol. 57, No. 1 (Feb., 1988), pp. 119-136
Published by: British Ecological Society
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Journalof AnimalEcology(1988),57, 119-136

EFFECTS OF POPULATION DENSITY

AND SUPPLEMENTAL FOOD ON
REPRODUCTION IN SONG SPARROWS
BY PETER ARCESE* AND JAMES N. M. SMITHt
TheEcologyGroup,Departmentof Zoology, Universityof BritishColumbia,British
Columbia,CanadaV6T1W5

SUMMARY
(1) Populationdensity and reproductionin the song sparrow(Melospizamelodia,
Wilson)on MandarteIsland,B.C. variedwidelyfrom 1975to 1986.Severalmeasuresof
reproductivesuccess declinedas population density increasedby six times. At peak
density, females producedonly one-quarterthe number of young producedat low
densities.
(2) We providedsupplementalfood to sixteenof seventy-twopairsbeforeand during
the breedingperiodin 1985,a yearof peakdensity,to testthe hypothesisthatthe amount
of food availableperpairdeclinesas densityincreasesand thus regulatesreproduction.
(3) Supplementalfood (i) advancedlayingdate;(ii) increasedclutchsize, the number
of breedingattempts,nestlingweightand the numberof independentyoung produced;
and (iii) reducedbroodparasitismand the intervalbetweensuccessfulnestingattempts.
(4) There was no differencein the subsequentsurvivalor reproductionof fed and
controlyoung.
(5) Supplementalfood was associatedwithreducedadultsurvivalto the nextbreeding
season, perhapsbecauseof increasedcompetitionfor territorieswith feedersafter the
feedingexperiment.
(6) We concludethat food supplyis importantin regulatingreproduction,and that
food availabilityin the breedingperiodcould limit populationsize.

INTRODUCTION

It is clear that food supplycan limit the size of animalpopulations(Lack 1954, 1966;
Watson& Moss 1970).However,it coulddo so by fluctuating:seasonally(Fretwell1972;
Newton 1980), stochastically(Wiens 1977) or in relationto populationdensity(Lack
1954, 1966),or by affectingaggressiveand territorialbehaviour(Chitty1967;Patterson
1980).Further,differentmechanismscouldact alternatelyor at onceto curtailpopulation
growthor causedeclines(reviewin Taitt& Krebs1985).The problemof whenand how
food supplylimits populationsize in a non-migratorysong sparrowpopulationis the
subjectof this paper.
The role of food supplyin populationdynamicshas often been investigatedin birds
becausetheirnumbers,survivalratesand reproductivebiologycan be easilymonitored.
Thepredominantviewwaspresentedby Lack(1954,1966),who contendedthatvariation
* Presentaddress:SerengetiWildlifeResearchCenter,P.O. Box 3134,Arusha,Tanzania.
t Correspondence author.
119
120 Food, reproductionand density

70-
60- .

50- / I
40-

0 30- I
E 20-

10-

61 6 76 78 '80 '82 '84 86

60 62 75 77 79 81 83 85 87
Year
FIG. 1. The number of females breeding on Mandarte Island during 17 years. Data for 1960-63
are from Tompa (1964).

in mortality during the non-breeding period, caused by fluctuations in food supply, is the
primary factor affecting population size in birds. This view has been well supported by
long-term studies of the great tit (Parus major L; e.g. McCleery & Perrins 1985;
Tinbergen, Van Balen & Van Eck 1985).
However, food shortage could also limit population size by regulating reproduction,
particularly if mortality were not wholly compensatory (e.g. Krebs 1970). For example,
Kluijver (1951) and Lack (1966) found that fledging success declined as density increased
in populations of great tits. They suggested that this occurred primarily because at high
density the amount of food available per female decreased and thereby reduced the
number of eggs that a female could lay. However, the roles of mortality, food supply and
population density in the regulation of most bird populations are unknown.
We address this question in two ways: (i) we document changes in reproductive
parameters that accompanied natural fluctuations in the size of the song sparrow
population resident on Mandarte Island, B.C., from 1975 to 1986; (ii) we describe the
results of a food addition experiment conducted in a year of peak population density to
test the hypothesis that density-related reproduction in this population is due to food
shortage.
Density in the song sparrow population on Mandarte Island can be high, but it
fluctuates considerably (Fig. 1). Nearly all breeding habitat is defended even at low
density. Thus, mean territorysize varies by roughly six times. Because the island is small (6
ha), and all birds in the population are colour-marked, we were able to follow the
behaviour and breeding success of individuals in detail. This population thus provides
ideal conditions for studying the roles of food supply, population density and
reproduction in the limitation of population size.

Predictions
We expected that as population density increased, reproductive success would decline
because breeding pairs would be unable to find sufficient food. Because we added
supplemental food in a year of peak population density, we predicted that if food supply
limits reproduction fed pairs would: (i) lay earlier;(ii) lay heavier eggs and larger clutches;
(iii) lay sooner after a previous breeding attempt; (iv) hatch a larger proportion of their
 ANDJ. N. M. SMITH
P. ARCESE 121

eggs; (v) raise heavier nestlings; (vi) suffer less nest predation; (vii) make more nesting
attempts and (viii) raise more young to independence than control pairs. We also
monitored brood parasitism by brown-headed cowbirds (Molothrusater (Boddaert)) and
the subsequent survival and breeding success of offspring and adults from experimental
and control territories.

METHODS
Study population
Song sparrows on Mandarte Island, B.C., Canada, were studied from 1975 to 1986.
Tompa (1964) describes the habitat on Mandarte and the biology of the song sparrows
resident there. Our general methods are described in Smith (1981). In brief, we find
virtually all nests during incubation, and band young as nestlings with coloured plastic,
and numbered aluminium rings. As there is little immigration to the population, nearly all
individuals are colour-marked and of known age. The only exception to this was in spring
1980, when we monitored the breeding activities of the sparrows only occasionally and
banded young-of-the-year as fledglings and independent young. For this reason, the data
on breeding performance in 1980 are much less detailed than in other years.

Experimental design
In 1985, we provided sixteen of seventy-two pairs of sparrows with feeders located
centrally in their territories throughout the breeding period. Two experimental plots of
seven and eight contiguous territorieswere initially selected. We chose to arrange fed pairs
in blocks, rather than randomly, to minimize the number of neighbouring pairs with
potential access to feeders. After all territorial settlement had taken place, there were
sixteen such neighbouring pairs and the remaining forty pairs were designated as controls.
Soon after feeding began, one fed pair lost its territory and feeder to two neighbouring
pairs that had not previously had access to a feeder. This pair disappeared after being
evicted from their territory, even though the female had been incubating. The new pairs
shared equal access to the feeder, thus we included them as experimental pairs. Only the
clutch size and laying date of the evicted pair were included in this analysis.
Preliminary analyses showed that the results from our experimental plots were nearly
identical. However, neighbours did perform slightly better than controls for most
measures. We therefore excluded these birds from our analyses, and pooled data from the
experimental plots.

Feeding schedule
Supplemental food consisted of moistened dog chow (Ralston-Purina Inc., 21% crude
protein), vitamin solution, mealworms (Tenebrio sp.) and millet seed. We provided food
twice daily from 28 February, 5 weeks before the onset of laying, to 24 July, after the last
young had left their nests. We were absent during 9 of 35 days before laying, 7 of 87 days
during the laying and rearing period and 5 of 24 days after the last clutch was initiated.
Before leaving, all feeders were heaped with food, and in most cases food remained in the
feeders on our return.

Assessment of reproductiveparameters
Eggs were weighed to the nearest 0.05 g with an electronic balance. The initial mean
weights of clutches were estimated by assuming that total clutch weight decreased by 15%
122 Food, reproductionand density
over the 13-day incubation period (Rahn & Ar 1974). The age of eggs at weighing was
known from the date of laying or by back-dating from the day of hatch. When comparing
clutch sizes, we only included nests that did not receive a brown-headed cowbird egg
because these brood parasites often remove host eggs.
After hatching, nestlings were weighed (as above) on alternate days from day 1 or 2 to
day 6. The number of fledglings was determined by regular nest checks and by observing
parents feeding newly-fledged young. The number of young reaching independence was
determined from resightings and captures in mist nets during intensive censuses
throughout the summer and fall.
The population was studied in similar detail in 1986, when sixty-one females bred. This
allowed us to determine the number of young recruited from the previous year that
themselves raised young, and to compare the performance of fed and control breedersand
territories between years.

Statistical analyses
Data were transformed (e.g. angular or logarithmic transformation) whenever they
were not approximately normally distributed (Chambers et al. 1983). When transforma-
tions did not normalize the data, non-parametric statistical comparisons were used (Sokal
& Rohlf 1981). Where we present summary data from consecutive years (e.g. Fig. 2a-f),
these data are often not independent because birds frequently bred for several seasons.
We therefore present correlation coefficients for these data as only descriptive statistics
(Sokal & Rohlf 1981).
In analyses involving repeated comparisons of related data, we revised the significance
level according to the Bonferroni inequality. This inequality states that only probabilities
less than or equal to the initial level of significance (i.e. P= 0.05) divided by the number of
tests conducted should be considered statistically significant (Miller 1981). For most
statistical tests we compared the mean values for females or territories in each group.
However, in a few comparisons (i.e. nest parasitism, predation, brood reduction) we used
each nest as a sample because we felt that the events in question were sufficiently
independent (e.g. nest location changed with each attempt).

RESULTS

ObservationalStudy
Population density and reproduction
Four of six reproductive variables studied were found to be related to female
population size (i.e. breeding density; Fig. 2a-e). Breeding date was only slightly delayed
as density increased (Fig. 2a, r=-0-29). However, by plotting the residuals of the
regression of median laying date against mean temperature in April, the month when
breeding usually began, we found that the strength of the relationship between density
and laying date increased (r= 0-63). This suggests that laying date is delayed at high
population density. Clutch size also declined as breeding density increased (Fig. 2b,
r= -0.61). However, density was unrelated to hatching success in nests that were not
depredated (Fig. 2c, r= -0-24) or to the mean number of breeding attempts made per
female per year (Fig. 2e, r = -017). The proportion of nests failing by day 6 of the
nestling stage was strongly positively related to breeding density (Fig. 2d, r= 0-71).
 P. ARCESE
ANDJ. N. M. SMITH 123
o 130- (a) Cb
0)
3-6- 0
*0
i- 120- 0 0@*
0
S 0v 3.4-
S
'b110- 0
0 .x- 3.2- S
a 100- 0 S
u 3-0- 0
C, o
~0
0;- 2-8-
80I I I I I
.-U

0) -.0- Cc) iR0-6- (d)

u
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0 0 S
04-
0.9. ~ * S
0
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C3 0
.2 *
0-8- 0 c 0-3-
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C- 0-7- 0
0

L- 2-9- Ce)
a
0
0
E
1(f)
a. 2-7- 'j4-4-0'
0 0
0)
2-5- *' 0
C:
E * * .
z? 2.3- * .0 >' 20-0
0~~~~~ C= I ? ,
21-I ,Oa 1-0' 0
0
0

- -I--I--I--I-I-I- ~-0
20 30 40 50 60 70 801M 20 30 40 50 60 70 80
Number of breeding females
FIG.2. Sixreproductive parametersin relationto populationdensity:(a) Mediandateof firstegg
(1 Jan.equalsday 1);(b) meanclutchsize;(c) proportionof eggshatchedin unparasitized nests;
(d) proportionof nestsfailingby day 6 of nestlingperiod;(e) meannumberof nestingattempts
and (f) meannumberof independentyoungper female.

Delayedbreeding,reducedclutchsize and increasednest failureall contributedto our

most striking result: the mean number of independentyoung producedper female
declinedto one-quarterof that observedat low densitiesas breedingdensityincreasedby
six times(Fig. 2f, r= - 0-72).In the followingsection,we reportthe resultsof our food
supplementation experimentto test the hypothesisthat the amountof food availableper
pairdecreasesat highpopulationdensityand limitsreproductionthroughsome or all of
the mechanismssummarizedabove.

Experimental results
Use offeeders
Adult song sparrowsused our feeders to feed themselvesand their nestlings and
fledglings.Pairstypicallyperchedclose by whenthe feederswerefilledand enteredthem
as we left. Fed pairsalso fed themselvesand theiryoung on naturalfood throughoutthe
experiment.Smallnumbersof otherspeciesoccasionallyusedthe feeders,but only briefly
preventedsong sparrowsfrom feeding.
124 Food, reproductionand density
Dateof firstegg

Experimental

cJ)

IL)

Control

April May
FIG. 3. The distributions of dates of first egg laid for fed and for control pairs.

3-6-

3 4-

3-2-
(1)

.1 3.0

C-)
2-8

2-6

4 April- 5 May- 4 June-

4 May 3 June 3 July
Period
FIG.4. Mean (S.E.) clutch size of fed and control females in early, middle and late portions of the
breeding period. N denotes the number of females.

Fledgling song sparrows fed themselves from the feeders as early as 17 days of age. This
is the age when unsupplemented birds begin to feed themselves (Nice 1943, our
observations). However, young of experimental pairs continued to beg and to be fed to
the normal age of independence (24-32 days).

Laying date
Fed pairs laid on average 18 days earlier than controls (Fig. 3). Note, however, that
while some control birds began laying as early as the earliest experimentals, laying of first
clutches continued among controls long after the last experimental pair had finished.
Thus, laying date was much less synchronous among control than among experimental
pairs (Fig. 3).
 ANDJ. N. M. SMITH
P. ARCESE 125
1. Thenumberof nestfailuresbeforefledgingattributedto differentsources
TABLE
in relationto treatment.Percentagesare givenin parentheses
Sourceof nest failure
Treatment N Successful Predation Starvation Deserted
Fed 50 30 (60) 18 (36) 1 (2) 1 (2)
Control 100 45 (45) 45 (45) 5 (5) 5 (5)

TABLE2. Mean (S.E.) numberof days betweenfledgingyoung and initiatinga

subsequentclutchin relationto treatmentand the numberof youngfledged.
Numberof youngfledged
Treatment 0 1 2 3+
Fed 8-1(1-0) 7-3 (0-3) 6.3 (0-6) 10-8(1-5)
N 12 3 6 9
N.S. * * **
Control 8.8 (0-1) 13-8(2-6) 13.5(2-4) 17.3(1-8)
N 44 10 4 3
* P< 005, **P<0.01, one-tailed,two-samplet-tests.

Clutch size
Fed pairs produced larger clutches than controls throughout the breeding period,
though only slightly so in the latter third of the season (Fig. 4). Overall, fed females laid on
average one-half an additional egg compared to controls (3-31+ 0.11 vs. 2-77 + 0-15
(mean+S.E.), respectively; t = 3.45, P<0.001, one-tailed). Thus, supplemental food
restored clutches to approximately the sizes that were observed at much lower breeding
densities (Fig. 2b). This strongly suggests that the observed decline in clutch size at high
breeding density is caused by reduced food availability.

Egg mass
Mean egg mass varied greatly among female song sparrows (range 2-20-3 75 g), and
clutches of three heavy eggs of some females frequently equalled in total weight clutches of
four lighter eggs of other females. Despite this variation, we found no difference in mean
egg mass between treatments (3-08 ?0.09 g vs 3.03 +0.05 g for 15 fed and 34 control
females). Furthermore, egg mass was unrelated to the subsequent size or survival of
nestlings and independent young. Since we have no information on the composition or
volume of different eggs, the source of variation in egg mass remains to be determined.

Hatching success
We tabulated the proportion of eggs that hatched in nests that were not depredated
prior to hatching to test for an effect of food on hatching success. A slightly higher
proportion of eggs were hatched in the nests of fed birds than in the nests of controls (78%
vs. 70%, means for 14 fed and 29 control females), but this differencewas not statistically
significant (t = 0-9, P>01, d.f.=41).
126 Food, reproductionand density
TABLE3. Meanmass (g) of nestlingsin relationto age and treatment
Age (days)
Treatment 1 2 3 4 5 6
Control 4.20 5.50 8.13 10-55 13-80 15-55
S.E. 0.17 0.15 0-25 0.34 0.47 0-31
N 14 55 23 47 20 60
N.S. * N.S. * N.S. *
Fed 4-43 6.32 8.93 11-63 14-54 16-81
S.E. 0.31 0.17 0.24 0.32 0.42 0.30
N 13 48 15 46 28 48
*t-tests;adjustedprobabilitylevelis 0-008(see Methods).

Sources of nest failure

The proportion of experimental nests that failed to fledge any young due to predation,
starvation or desertion was lower than that observed for controls in each case (Table 1).
Overall, 15% more experimental nests produced at least one fledgling than did control
nests (Gw= 2-98, P< 0.05, d.f.= 1, one-tailed). However, experimental broods were
initially larger on average than control broods because their clutches were larger and the
proportion of eggs hatching was slightly higher than in control nests (see above). Thus,
the total proportion of experimental nests that fledged at least one young could have been
higher than that observed for controls even if the rate of nestling loss in the two groups
was equal.
Assuming that predation rate is independent of brood size, we expected that differences
in predation between fed and control nests would not be affected by initial differences in
clutch size or hatching success. Indeed, the differencein the rate of total nest failure due to
predation between fed and control broods was small (36% vs. 45%, respectively), and not
statistically significant when separated from other causes of failure (Gw= 1.96, P> 0 10,
d.f. = 1). This suggests that if supplemental food reduced total nest failure, it probably did
so by affecting each contributing variable to a small degree.

Speed of re-nesting
Fed females nested more quickly after fledging one, two or three or more young.
However, fed and control females took equal time to re-nest following a nest failure
(Table 2). Though our sample sizes are small for some of these comparisons, our results
suggest that additional food acted primarily by lessening the amount of time needed to
tend fledglings.

Number of nesting attempts

Experimental pairs initiated more breeding attempts on average than did controls
(281 + 0'21 vs. 2-24?+ 014; t=2-27, P<0-02, d.f.= 54, one-tailed). This likely resulted
because fed females began breeding earlier and re-nested more quickly after fledging
young.

Nestling weight
The young of fed pairs outweighed control young from soon after hatching, to at least
six days of age. (Table 3). However, these differences were not all statistically significant
after correcting for the number of tests conducted (see Methods). We found no difference
in the adult sizes of young from experimental and control broods (Smith & Arcese 1988).
 ANDJ. N. M. SMITH
P. ARCESE 127
5-0-
82
a, 8
80
E 4.0-
4? 81
?^ 76 78 O:Fed
Q~1~ ~ 77
oa 3.0- 83
0 - *84
U

1 2-0-
'O 79
0. 75
1.0-
1.0- 86 Control

10 0o 30 40 50 60 70 80
Number of breeding females

FIG. 5. Mean number of independent young produced by fed and control females in 1985 in
relationto thenumberof breedingfemalesandthemeannumberof youngproducedin previous
years.

Brood reduction
We tallied the number of experimental and control broods that lost one or more
nestlings before fledging to test if brood reduction is determined by food availability. We
included here only those nests that survived to hatching and omitted nests where there was
evidence of predation, i.e. bite marks, chewed remains near the nest or disturbed nest
lining. Nestlings were lost in 25-5% (14 of 55) of control broods, but in only 13-3%(4 of
30) of experimental broods. Thus, brood reduction was nearly twice as common in
control nests, but this difference was not statistically significant (Gw= 1.75, P>0 1,
d.f.= 1).

Cowbirdparasitism
During the period when cowbirds were known to be laying, parasitism was strikingly
less frequent in experimentalnests. Only 7 of 38 (18%) experimental nests were parasitized
as compared to 42 of 94 (45%) control nests (G,= 7-96, P< 0.005, d.f. = 1).
Because we have observed female song sparrows chasing cowbirds from their nests
(Smith, Arcese & McLean 1984), we hypothesized that supplemental feeding allowed
females to guard their nests more diligently. In support of this, we found that fed females
spent less time off their nests between periods of incubation than did control females
(6.28+0-55 min vs. 8.17+0.33 min, t=2-98, P<0-01, d.f.=46, two-tailed). Possibly
more importantly, fed females frequently foraged for only short periods while off their
nests and spent much of their 'off-time' perched above the nest, preening or surveying
their territory. In contrast, control females often fed continuously and well out of sight of
their nests between incubation periods.

Survivalfrom fledging to independence

We tabulated the proportion of fledged young that reached independence from fed and
control broods to determine if supplemental food influenced the survival of young during
the period following fledging and previous to independence from their parents. The
median percentage of fledglings surviving to independence for thirteen fed pairs during
this period was 83%, as compared to 73% for twenty-nine controls. This difference is not
statistically significant (P> 0 50; Mann-Whitney U-test).
128 Food, reproductionand density
TABLE4. The number of independent young from 1985 that recruited to breed, and
that raised independent young in 1986, in relation to treatment
Treatment
Fed Control
Total independent 58 40
Total recruitingto breed 12 (20.7%) 11(27.5%)
Totalraisingindependentyoung 5 (8.6%) 5 (12.5%)

TABLE5. The number of adults on fed and control territories that survived to breed
or disappeared between July 1985 and May 1986
Fate
Sex Treatment Survivedto breedagain Disappeared
Male Fed 7 8**
Control 33 9
Female Fed 6 9*
Control 28 14
* P=008, **P=-003, Gwtests,two-tailed.

Production of independentyoung
Experimental pairs produced nearly four times more independent young on average
than did controls (Fig. 5, P< 0 001, U-test). Further, while production of young among
controls matched the level that would be expected given the high density in 1985 (Fig. 5),
the number of young produced by fed pairs equalled that observed at population densities
one-quarter to one-half as high. Clearly, supplemental food ameliorated the effects of
high breeding density on reproduction.

Recruitment and breedingsuccess offed and control young

We tallied the number of fed and control young that survived and raised independent
young in 1986 to test if subsequent recruitmentand breeding performance was affected by
supplemental food received early in life. However, the proportion of 1985 young that
attempted to breed, and of those that raised young, was independent of whether they had
received supplemental food (Table 4).

Survival offed and control adults

Surprisingly, fed adults survived more poorly to the subsequent breeding season than
did controls (Table 5). We had expected that adult survival would be unaffected or
enhanced by supplemental feeding. We address this result further in the Discussion.

Comparisonsof breedingperformance across years

For reasons given earlier, we did not randomize experimental territories across the
population. Our results could therefore have been influenced by initial differences in the
territory or individual quality of birds chosen for each treatment. We tested for such
influences by comparing the number of young raised by birds that bred both in 1985 and
subsequently in 1986, when no manipulations were conducted.
 ANDJ. N. M. SMITH
P. ARCESE 129
If supplemental food was primarily responsible for the enhanced reproduction of fed
birds in 1985, these birds should have performed more poorly in 1986 when no food was
provided. In contrast, control birds should have performed better in 1986, because
average reproductive success was slightly higher than in 1985 (Fig. 5). As expected, only
29% of birds (4 of 14) that received food in 1985 and also bred in 1986, subsequently
produced as many young. In comparison, 75% of control birds (45 of 60) produced as
many or more young in 1986 (Gw= 10 0, P<0.001, d.f. = 1). Further, the reproductive
success of fed and control birds that survived from 1985 was equal in 1986 (P>0 5, U-
test).
We also compared the performance on sixteen territories where both the male and
female had been replaced by 1986, but which remained about the same size (i.e. changed
by less than 20%). This allowed an independent test of the effects of territoryquality upon
the reproductive success of the pair occupying it. Of these territories, nine were controls
and seven were supplemented in 1985. We expected that the number of young produced
on previously supplemented territorieswould drop in 1986, when no food was provided,
and would remain similar on controls. As predicted, the median number of young
declined by four on previously supplemented territories, whereas the median number
produced on controls remained unchanged (P < 0-01, U-test). Moreover, the number of
young produced on these territories was equal in 1986 (P>0.2, U-test), but differed
fivefold in 1985 (P <0.001, U-test). These comparisons show that the enhanced breeding
success on supplemented territoriesin 1985 was caused by food addition rather than by a
non-random choice of territories or birds.

DISCUSSION

Population density and reproduction

Our observational results show that the reproductive performance of song sparrows on
Mandarte Island depends on breeding density. We suggested that the mechanism
underlying this relationship is that the average amount of food available per pair
decreases as the number of breeders increases. The results of our experimental food
addition strongly support this hypothesis. We therefore conclude that the primary cause
of low reproduction at high densities is food limitation.
When supplemental food was provided at peak density in 1985, fed birds nested earlier,
laid larger clutches, produced heavier nestlings, re-nested more often and raised four
times more young to independence than did unfed controls. Supplemental food was also
associated with reduced parasitism by cowbirds, a reduction in the proportion of nestlings
dying from causes other than predation before fledging, and a shorter time interval
between fledging young and initiating a subsequent brood. These results, with those of
our observational study (Fig. 2), show that density-related depression of reproduction
can be ameliorated by giving birds unlimited, high quality food before and during the
breeding period. In this respect, our study is unique among food addition experiments
(Table 6; reviews in Ewald & Rohwer 1982; Davies & Lundberg 1985; Taitt & Krebs
1985).

The social disruptionhypothesis

Tompa (1964) suggested that high population density caused sufficient social
disruption and stress in breeders to depress reproduction (see also Christian 1950). Our
 TABLE6. Summary of the effects of supplemental food on reproduction in several bird
Laying Clutch Egg Hatch Nestling Fl
Study Species date size weight success weight s
Krebs (1971) Parus ater L N N
Jones (1973) Parus major N N -
Kallander (1974) P. major A I -
Yom-Tov (1974) Corvus corone L A N I N
Von Br6mssen & Jansson (1980) Parus cristatus L A N I
Von Bromssen & Jansson (1980) Parus montanusConrad A N N
Smith et al. (1980) Melos'r imelodia A N
Hogstedt (1981) Pica pica (L) A I I I (I)
Newton & Marquiss (1981) Accipiter nisus (L) A I
Dijkstra et al. (1982) Falco tinnunculusL A (I)
Ewald & Rohwer (1982) Agelaius phoeniceus (L) A N N -
Harper (1984) cited in Davies & Lundberg (1985) Erithracusrubecula L N I
Davies & Lundberg (1985) Prunella modularis L A N R
Hochachka & Boag (1987) Pica pica A N N
This study Melospiza melodia A I N (I) I
A = advanced; I = increased, N = no effect; R = reduced; 1= improved winter survival; 2 = little or no effect on winter surviva
brood interval reduced; 5 = adult survival reduced after feeding stopped; ( ) = weak or inconsistent effect; '-' = no data, or d
question.
 ANDJ. N. M. SMITH
P. ARCESE 131

experiment was not designed to test this hypothesis. However, some observations suggest
that high density per se was not the main cause of poor reproduction. First, territorial
aggression was frequent in 1985 (e.g. Arcese 1987; Arcese, Stoddard & Hiebert 1988)
regardlessof whether owners were supplied with extra food. Second, intrusion pressureby
non-territorial males (Arcese 1987) was equal on fed and control territories, as was the
rate of turnover in territory ownership during the breeding period (unpublished results).
We therefore suggest that high levels of territorial aggression can not explain the poor
performance of control pairs.
Mechanisms of the regulation of reproduction
We now consider our experimental results in turn, and discuss them with regard to the
findings of other food addition experiments.
Supplemental food has caused an earlier onset of reproduction in several species (Table
6), and was previously shown to advance breeding in our study population (Smith et al.
1980). Our results confirm that food is an important proximate stimulus for the onset of
breeding in birds (Perrins 1970). We also found that median laying date was related to
population density and to mean temperature in April, the month during which breeding
usually commenced. Temperatureprobably affects food availability through its effects on
plant and insect phenology, and density presumably acts mainly by reducing the foraging
area of females.
Of fourteen food supplementation studies listed in Table 6, only five (36%) reported
increases in clutch size. Davies & Lundberg (1985) suggested that larger species might
respond more readily to supplemental food because the formation of eggs limits their
reproductive output (Winkler 1985). Smaller species, on the other hand, may be limited
more by their ability to feed young. Our results are contrary to this hypothesis. We
observed a large increase in clutch size among fed song sparrows, a species in which
females weigh about 23 g (Fig. 4).
Dijkstra et al. (1982) found that European kestrels increased their clutch size in
response to supplemental food, but only to the extent predicted by an observed negative
relationship between clutch size and laying date. In our population, however, we would
not expect such a result because there is no consistent relationship between clutch size and
laying date (W.M. Hochachka, unpublished).
We therefore consider two other explanations for differences among species in their
responses of clutch size to food addition. First, the quality of food supplied may be critical
(Ewald & Rohwer 1982). In a previous experiment we used millet seed (Smith et al. 1980),
a relatively poor quality food, to supplement a high-density song sparrow population on
Mandarte in winter and early spring. We did not, however, observe a subsequent increase
in clutch size. This finding is consistent with the suggestion that high quality food is
essential for enhanced egg production (Ewald & Rohwer 1982).
Second, the relationship between food availability and clutch size may be non-linear
(Fig. 2b), such that clutch sizes are strongly depressed only at very high densities. We
suggest that except at very high densities, or in unfavourable years (Dijkstra et al. 1982) or
habitats (Newton & Marquiss 1981), clutch size is limited by genetic and developmental
factors, rather than by the availability of high quality food. In agreement with this, our
food addition did not cause clutch sizes to increase above the levels observed at low
densities (Fig. 2b, Fig. 3).
Smith & Roff (1980) showed in song sparrows that the interval between fledging young
and starting a new clutch increased with the number young fledged. They suggested that
132 Food, reproductionand density
raising larger broods diminished the probability of raising additional broods in a season.
In this study, supplemental feeding during the breeding period reduced inter-brood
intervals among experimental pairs when at least one young fledged (Table 2). However,
the interval between failed nests was unaffected. This supports Smith & Rof's (1980)
hypothesis that the time needed to feed fledglings is the primary determinant of the
interval to re-nesting. Tinbergen (1987) reduced the cost of parental care in great tits by
manipulating brood size, and also found shorter inter-brood intervals and a higher
probability of re-nesting.
Supplemental food appears to have had its smallest beneficial effect during the nestling
period. When examined separately, the effects of food on hatching success, nestling
weight (Table 3), predation and starvation (Table 1), brood reduction and fledgling
survival were small. However, their cumulative effects were substantial. Overall, the
probability of eggs from fed pairs surviving to become independent offspring exceeded
that for controls by three times (mean egg survival per pair was 40% for sixteen fed pairs
and 15% for forty controls; P < 0-01, U-test).
We observed a striking reduction in brood parasitism by brown-headed cowbirds in the
nests of fed pairs. Smith, Arcese & McLean (1984) suggested that the ability of song
sparrows to recognize and defend against cowbirds is an important determinant of
whether their nests are parasitized. Our present results suggest that food supplementation
altered the behaviour of pairs such that their time available for nest defence was increased.
We suggest that this was the primary cause of the reduction in parasitism, and it may also
have contributed to the slight reduction in nest predation (Table 1).
Our most important result was a fourfold increase in the number of young raised to
independence by fed pairs. Moreover, this level of young production compares closely to
what we have observed at low population densities (Fig. 5). This result provides the
strongest support for the hypothesis that the amount of food available to breeders is the
primary factor limiting reproductive success at high density.
Our experimental design involved two blocks of treated territories. We considered
whether this might have biased our results by comparing the number of young produced
by individuals, and on territories, across years. Neither the fed or control territories or
birds of 1985 differedin reproductive success in 1986, when density was slightly lower and
average reproduction was slightly higher (Fig. 5). Although these comparisons are
indirect, they show that the improved breeding success of fed pairs in 1985 resulted from
food addition rather than from a non-random choice of territories or birds.

Food addition experiments and population density

Adding food at different times of the year is the most direct method to test if food
supply limits reproduction or survival (e.g. Krebs & Delong 1965; Yom-Tov 1974). Such
experiments are especially valuable in populations where long-term, density-related
processes have been observed. If in this case adding food raises reproductive success or
survival towards levels observed at low density, food is implicated as a limiting factor.
Food addition studies in breeding bird populations have so far produced mixed results
(Table 6). However, too few food supplementation studies have reported on more than a
few aspects of reproduction (Table 6), and just one was conducted in a population where
density-related reproduction was known to occur (Jones 1973).
The failure of food addition to enhance reproduction could be due to: (i) reproduction
being limited by some factor other than food supply during the breeding period; (ii)
density in the study population being below the level at which reproduction is depressed;
 ANDJ. N. M. SMITH
P. ARCESE 133
TABLE floatersforat least1-month
7. Numbersof adultsobservedas non-territorial
during1 August 1985to 1 March1986,in relationto theirexperimentalstatusin
1985
Seenas floater Not seen to float
Fed Control Fed Control
Males 4 1 11 41 *P =0.02
Females 5 2 10 40 *P=0.03
* Two-tailedFisher'sExacttest.

or (iii) the added food being of insufficient quantity or quality. Explanation (iii) was
discussed above and can be ruled out by insuring that the added food is unlimited in
quantity and high in essential nutrients. Explanation (ii), however, can only be rejectedby
conducting experiments in high-density populations that are known to display density-
related properties.
Our results are probably due in part to the fact that we conducted our experiment in a
year of peak population density, when reproduction in the control population was lower
than in any previous year. Therefore, experiments are now needed on lower density
populations to test if food can similarly enhance reproduction. We predict that such
experiments will produce considerably less striking results. If so, this could explain part of
the variation with regard to the results of other food supplementation experiments (Table
6, Ewald & Rohwer 1982; Davies & Lundberg 1985).

Adult survivaland competitionfor territories

We were surprisedto observe reduced survival among fed adults. It is possible that this
was caused by additional effort expended in breeding. This seems unlikely, however, given
the high success of experimental pairs, and the results of a time budget study that show
that fed birds spent much less time foraging and more time perching than controls (P.
Arcese, unpublished results). Also, we have no evidence to suggest that avian predators
concentrated their effort on the fed areas during the winter of 1985-86.
Another possibility is that juveniles were attracted to supplemented territories after
gaining independence, and that fed adults subsequently experienced high intrusion
pressure in the non-breeding period when young birds became territorial (Tompa 1964).
We have some evidence to support this explanation. First, high intrusion pressureby non-
territorial birds is known to cause territory loss in this population, and takeovers by
yearlings account for up to 40% of disappearances of territorial males (Arcese 1987).
Second, we observed that dispersal by yearlings from experimental territories was
dramatically reduced, and that early dispersers from control territories often developed
home ranges that included supplemented territories(P. Arcese, unpublished). Finally, fed
adults were more often observed as non-territorial floaters during the subsequent non-
breeding period than were controls (Table 7). Because adult song sparrows on Mandarte
show strong year-round fidelity to their territories, we suspect that the floating adults we
observed had been evicted by juveniles seeking territories in areas that were previously
supplied with feeders.
A similar finding was reported by Kluyver (1970) in the great tit population resident on
Vlieland, Netherlands. He found a negative correlation between the winter survival of
adults and the size of the juvenile population. Then, after reducing young production to
about 40% of normal by removing eggs from nests, Kluyver observed an increase in adult
134 Food, reproductionand density
survival in the following years, and a return to lower adult survival after the experiments
ceased. Kluyver (1970) suggested that juveniles were the main agent of reduced adult
survival in the non-breeding period because they compete with adults for territories. Our
results suggest a similar effect in the song sparrows on Mandarte Island.

Population regulation in the song sparrow

We now consider the regulating influence of food supply in the breeding versus the non-
breeding season in the song sparrow population on Mandarte Island. The addition of
food in one winter increased survival only slightly among non-territorial females,
indicating that winter food availability may be only a weak or sporadic limiting factor in
our population (Smith et al. 1980). However, reproductive success is strongly depressed at
high population densities (Fig. 2f). This suggests that population size in spring could be
limited by the production of young during the previous breeding season.
In support of this idea, the breeding population on Mandarte decreased by 11 pairs
following 1985, even though over-winter mortality among adults was equal to the average
of the 11 previous years (P. Arcese, D. Ludwig & J. N. M. Smith, unpublished). Thus,
reproduction in 1985 was insufficient to compensate for a reduction in population size
that resulted from a usual amount of adult mortality during the non-breeding period.
Our results outline a mechanism that could limit the number of breeding pairs of song
sparrows that is relatively independent of the level of over-winter mortality. In contrast,
in the great tit density-dependent reproduction has little effect on the number of breeding
pairs, but the roles of food supply and mortality during the non-breeding period are
substantial (McCleery & Perrins 1985; Tinbergen, Van Balen & Van Eck 1985). Fretwell
(1972) and Wiens (1977) also emphasize the importance of over-winter mortality to the
regulation of migratory sparrow (Emberizidae) populations. However, we have little
evidence that the over-winter mortality of adult song sparrows varies markedly on
Mandarte (P. Arcese, D. Ludwig & J. N. M. Smith, unpublished).
Martin (1987) argues that the influence of food supply on population size in birds
during the breeding period has been underestimated. We suggest that density-dependent
reproduction, mediated by food supply, is a more important factor limiting the
population size of passerine birds than is currentlyrecognized. This may be especially true
in sedentary populations with little immigration, as in the case of the song sparrow
population on Mandarte Island. This mechanism does not, however, account for the wide
fluctuations in population size that occur below the limit imposed by food supply (Fig. 1).

ACKNOWLEDGMENTS

P. Bets, S. Groves, A. Helbig, W. Hochachka, M.-J. Houde, J. Merkt, R. Moses, D. Reid,

J. Russell, A. Tompa and M. Waterhouse helped with field work. We thank D. Chitty, J.
Eadie, W. Hochachka, C. Krebs, D. Ludwig and J. Myers for their comments; especially
Dennis Chitty for discussions of Kluyver's experiment. We receive support from
N.S.E.R.C. (Canada), the Canadian Wildlife Service, University of B.C., the Frank M.
Chapman Memorial Fund and Josselyn Van Tyne Memorial Fund. The Tsawout and
Tseycum Bands of Saanich, B.C. kindly allowed us to work on their island.
 ANDJ. N. M. SMITH
P. ARCESE 135

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(Received 3 February 1987)