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I B I S 136: 397-41 1
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THE FIRST ALFRED NEWTON LECTURE
Presented at the “Bird Conservation in Action” conference, April 1994
Experiments on the limitation of bird breeding densities: a review
I . NEWTON
Institute of Terrestrial Ecology, Monks Wood, Abbots Ripton, Huntingdon, Cambridgeshire P E l 7 2LS, UK
The breeding densities of birds could be limited by resources, such as food and nest sites,
or they could be held at a lower level by natural enemies, such as predators and parasites.
In this paper, I review the experimental evidence for each of these limiting factors affecting
bird breeding densities. Of 18 experiments involving winter food provision (mostly on tits,
Paridae). 11 led to increased breeding densities compared with control areas. Of four
involving summer food depletion (all on forest insectivores),none led to decreased breeding
densities. In experiments with Red Grouse Lagopus 1. scoticus, fertilizing areas of heather
moor led to increased densities during a period of population increase but did not prevent
a later decline. Of 32 studies on tree-cavity nesters, the provision of nestboxes led to
increased breeding density in 30 (95%)studies, each involving one or more species of hole
nesters. Of 15 experiments involving predator removal (mostly on ducks and gamebirds),
at least 14led to increased hatching success, four out of eight led to increased post-breeding
numbers, and six out of 11 led to increased breeding density. In one experiment, the
removal of strongyle parasites from a Red Grouse population prevented a cyclic decline
on five out of five occasions. Taken together, these experiments confirmed that all main
potential external limiting factors have affected breeding density in one bird species or
another. They also confirmed that the same species has been limited by one factor in
certain areas or years and by another factor in different areas or years.
contents. But the number alive at the start of the next breeding season might depend largely on overwinter survival, in
turn dependent on food supply. In this case, increasing the
winter food supply would have more intluence on breeding
numbers than would decreasing the predation on nest contents.
This paper is primarily about the limitation of breeding
densities for two reasons. First, it is in the early stages of
breeding each year that bird numbers reach their annual
low, and it is upon the breeders that future additions to the
population usually depend. Second, it is in the breeding
season, when birds are most conspicuous and tied to fixed
sites, that they can be counted most readily. In fact, most
experiments have been concerned with breeding numbers.
In addition to breeders, however, some bird populations may
contain a large nonbreeding contingent, which may or may
not be countable.
No one is likely to dispute the fact that food supply or
other resources could provide a ceiling to the numbers of
any bird. The key question is, in practice, which species are
limited by resources and which are held at a level lower
than resources would permit by other factors, notably nat-
As ever more land falls to intensive human use, many bird
species are increasingly constrained in distribution and
abundance by the progressive destruction and degradation
of their habitats. For effective conservation, better understanding is needed of the factors that limit numbers within
areas of remaining habitat. Only then can such areas be
managed so as to sustain large populationsof desired species.
In this paper, I shall be concerned with the factors that limit
bird numbers within the available habitat, concentrating on
the experimental evidence.
The best we can hope to show by experiment is that some
particular factor limits bird density at a particular place and
time. It is necessary to define the area carefully, for while
density may be limited in this area, some individuals may
move out and survive elsewhere, so that total numbers are
unaffected. The emigrants may or may not return at a later
date. It is important to specify the time period, because bird
numbers may be limited by different factors at different times
and only the last-acting may be crucial in setting the eventual population level. For example, the number of birds present at the end of a breeding season might depend largely on
breeding success, in turn dependent on predation of nest
397
398
I. NEWTON
Model of limitation of breeding density
Surplus
Resource limlt
Deficit
I
Non-breeding
period
I
Breeding period
Figure 1. Model showing seasonal changes in bird numbers in
relation to the carrying capacity of the breeding habitat (thick line).
In the lower curve (l), overwinter losses are severe and reduce
numbers well below the level that the breeding habitat would support: in (2) overwinter losses are such that the numbers left in spring
match those that the breeding habitat will support and in ( 3 ) overwinter losses are slight, leaving more birds than the breeding habitat
will support and giving rise to a surplus of nonbreeders. In (1).
breeding density is largely determined by overwinter losses, in (2)
by both overwinter losses and the carrying capacity of the breeding
habitat and in ( 3 ) by the carrying capacity of the breeding habitat.
ural enemies such as predators, parasites or pathogens or
human agency. Effective conservation of any species depends on knowing the limiting factors, for it is these external
factors which must be altered if an increase in population
is to be achieved. Any factor might be considered limiting if
it prevents at population increase or causes a decline. In
reality, no one factor is likely to account wholly for a given
population level. During a period of food shortage, for example, some individuals may starve, while other nonstarving
individuals may die from other causes such as predation. In
such cases, the main limiting factor can be considered as
the one which, once removed, will permit the greatest rise
in numbers.
Because populations may be influenced by many different
factors, acting individually or in combination, it is often hard
to tell the relative importance of each, except by experiment.
Moreover, the crucial factor cannot always be deduced from
knowledge of mortality causes, even if such information were
available. Imagine that the density of a territorial species
was limited by some aspect of habitat quality, so that surplus
individuals were forced into suboptimal habitat where they
were eaten by predators (the ‘doomed surplus’ model of
Errington [1946]). From a study of mortality, one would
conclude that predators limited numbers because virtually
all the mortality occurred through predation: however, the
underlying limiting factor was habitat quality, which influenced the density of territories. To change breeding density
in the long term would entail a change of habitat, not of
predators. and in each case surplus individuals would be
removed by predators or any other mortality agents available locally. The important point is that the factors that cause
most mortality in a bird population are not necessarily those
IBIS
136
which ultimately determine the population level. In any case,
assessing the causes of mortality in a bird population is itself
not straightforward. A bird weakened by food shortage may
succumb to disease, but just before its death it may fall victim
to a predator. For this bird, food shortage is the underlying
(ultimate) cause of death, while disease or predation is the
immediate (proximate) cause. The importance of experiments in clarifying the picture is obvious.
My aim in this paper is to review the field experiments
that have been done to test the effects on bird breeding
densities of various external limiting factors, namely food
supply. nest sites, predators and parasites. I have excluded
experiments that have examined the role of territorial or
other social interactions in limiting density, which have been
reviewed elsewhere (Newton 1992), and also experiments
on the role of food supply in influencing laying dates and
clutch sizes.
EXPERIMENTAL DESIGN
Most experiments on population limitation in birds fit within
the same conceptual framework (Fig. 1).This is true whether
the population is resident, with individuals remaining in the
same area year-round, or migratory, with individuals spending the nonbreeding and breeding periods in different areas.
Numbers are highest at the end of one breeding season and
then decline to the start of the next. But within the nesting
habitat. breeding density can be limited, as birds compete
for territorial space or nest sites. Three scenarios can be
envisaged:
(1) In some populations, overwinter losses-from whatever limiting factors operate in winter-may be so great that,
by the start of breeding, the remaining birds are too few to
occupy the nesting habitat fully, so that practically all individuals of appropriate age and condition could breed. In
this case, breeding density is limited by whatever factors act
to reduce numbers in winter, and manipulation of these
winter factors would be needed to produce an increase in
breeding numbers.
(2) In other populations, overwinter losses may reduce
numbers to more or less the level that the nesting habitat
will support, so that again almost all potential breeders left
at the end of winter could breed. In this case, manipulation
of both the factors influencing winter losses and the carrying
capacity of the nesting habitat would be needed to produce
an increase in breeding numbers.
( 3 ) In yet other populations, overwinter losses may be
so light that, after the nesting habitat is fully occupied, a
surplus of potential breeders is left over which move on to
breed elsewhere or form a nonbreeding component. In this
case, manipulation of the factors influencing the carrying
capacity of the nesting habitat would be needed to permit a
rise in breeding numbers.
Although, in this model, I have viewed the carrying capacity of the breeding habitat at the time of settlement as
1994
399
LIMITATION OF BIRD BREEDING DENSITIES
Table 1. EKects of winterfood provision on the breeding density of various birds
Species
Great Tit
Parus major
Blue Tit
Parus caeruleus
Willow Tit
Parus montanus
Crested Tit
Parus cristatus
Coal Tit
Parus ater
Black-capped Chickadee
Parus atricapillus
Tufted Titmouse
Parus bicolor
Nuthatch
Sitta europaea
Song Sparrow
Melospiza melodia
Carrion Crow
Corvus corone
Red Grouse
Lagopus 1. scoticus
Black Grouse
Tetrao tetrix
Region
Grade’
(years)
Increase
in density
Reference
Germany
Finland
England
Netherlands
Sweden
Germany
England
Sweden
Sweden
3 (1)
1(3)
2 (1)
2 (5)
3 (2)
3 (1)
2 (1)
3 (2)
3 (1)
Yes
No
Yes
Berndt et al. 1964
Haartman 1973
Krebs 1971
van Balen 1980
Kallander 1981
Berndt & Frantzen 1964
Krebs 1971
Kallander 1981
Jansson et aZ. 1981
Sweden
3 (1)
Yes
Jansson et al. 1981
Scotland
2 (1)
No
Pennsylvania
10)
Yes
A.J. Deadman (unpubl. PhD thesis,
University of Aberdeen. 1973)
Samson & Lewis 1979
Pennsylvania
1 (1)
No
Samson & Lewis 1979
Sweden
3 (2)
Yes
Enoksson & Nilsson 1983
British Columbia
2 (1)
Yes
Smith et al. 1980
Scotland
1(1)
No
Yom-Tov 1974
Scotland
2 (1)
YesZ
Watson & Moss 1979
Sweden
3 (4)
No
Willebrand 1988
Yes
No
Yes
Yes
No
Yes
* See Table 5.
In certain conditions only, see text.
fixed, for some species this is probably an oversimplification.
The numbers of birds that can settle in a given area of nesting
habitat may be variable within limits, depending on the
number of potential settlers available, with more individuals
‘squeezing in’ when the number of contenders is high. In
this case, the numbers of birds left over at the end of winter
could have some influence on breeding density, even in the
third situation described above. In practice this means that
under severe competition for space, some individuals might
accept smaller territories or inferior nest sites, facilitating
higher density (Davies 1978. Newton 1992). As another
modification, numbers may fit the carrying capacity of the
nesting habitat at the start of breeding but then fall below
it, as a result of mortality or as carrying capacity rises with
the seasonal improvement in conditions. Eventually, the
production of young ensures a rise in density to give another,
post-breeding peak. Finally. any given population may fit
one of the patterns described above in some years and areas
and a different pattern in other years or areas.
In some of the experiments reported below, the experimental treatment covered the whole year, while in others
it covered the nonbreeding period only or the breeding pe-
riod only. The commonest type of experiment involved a
single area in which breeding numbers were monitored for
some years, then the treatment was applied and numbers
were monitored for several further years, giving a simple
before-and-after comparison (grade 1 in Tables 1-5). The
weakness of this procedure is that. without a control, one
cannot be certain that a change in breeding numbers was
due to the treatment and not to some other unknown factor
which changed at the same time. The second type of experiment involved two areas, with the treatment applied in
one area while the other area served as a control (grade 2).
If breeding numbers changed more in the experimental than
in the control area, this was taken as evidence that the
treatment influenced numbers. Ideally, the two areas should
be far enough apart that treatment in the experimental area
does not affect birds in the control area, which, if the areas
were close, could move back and forth. The third type of
experiment involved some replication, either by reversing
the treatments, so that after a time the experimental area
became the control and vice versa, or by the simultaneous
use of several experimental and several control areas (grade
3 ) . Such replication strengthens the findings because it in-
$00
IBIS
I . NEWTON
136
Table 2. Limitation of breeding density in birds nesting in tree cavities as shown by the experimental addition or subtraction of nest sites.
Most studies involved simple before-and-after comparisons, but those marked included control areas and those marked **alsoincluded replication
Species
Area
Nestboxes added, leading to an increase in breeding activity
Starling
New Zealand
Sturnus vulgaris
House Sparrow
New Zealand
Passer domesticus
Tree Sparrow
England
Passer montanus
Tree Sparrow
Germany
Germany
Tree sparrow
Germany
Tree Sparrow
Arizona
Western Bluebird
Sialia rnexicana"
Mountain Bluebird
Sialia currucoides
Mountain Bluebird
Eastern Bluebird
Sialia sialis
Rcdstart
Phoenicurus phoenicurus
Pygmy Nuthatch
Sitta pygmaea**
Mountain Chickadee
Parus gambeli
Great Tit
Parus major
Varied Tit
Parus varius
Blue Tit
Parus cueruleus*
Pied flycatcher
Ficedula hypoleuca
Pied Flycatcher
Habitat
Reference
Farmland
Coleman 1974
Farmland
Coleman 1974
Farmland
Boyd 1932
Creutz 1949
Dornbusch 1973
Gauhll984
Brawn & Balda 1988
Manitoba
Farmland
Pine plantation
Farmland
Ponderosa pine
forest, lightly
managed
Parkland and meadows
Manitoba
Manitoba
Mainly farmland
Mainly farmland
Miller et al. 1970
Miller et al. 1970
Finland
Birch forest,
lightly managed
Pine forest, lightly managed
rarvinen 1978
Arizona
California
Cutforth 1968
Brawn & Balda 1988
Conifer forest,
lightly managed
Second-growth forest
Dahlsten & Copper 1979
Japan
Second-growth forest
Higuchi 1978
Britain
East & Perrins 1988
Higuchi 1978
Pied Flycatcher*
Northern Sweden
Pied Flycatcher
Southern Sweden
Pied Flycatcher
Southern Sweden
Collared Flycatcher
Ficedula albicollis**
Violet-green Swallow
Tachycineta thalassina**
Tree Swallow
Iridoprocne bicolor
Sweden
Ontario
Deciduous woodland,
unmanaged
Deciduous woodland,
managed
Birch forest,
lightly managed
Subalpine Birch
forest, natural
Broad-leaved
woodland, managed
Broad-leaved
woodland, managed
Deciduous woodland.
managed
Pine forest, lightly
managed
Mixed. rural
Purplc Martin
Progne subis
Ash-throated Flycatcher
Myiarchus cineraseens*
Green-mmped Parrotlet
Forpus passerinus'
European Kestrel
Falco tinnunculus
European Kestrel
Ontario
Mixed, rural
Holroyd 1975
Arizona
Brush 1983
Venezuela
Riparian, lightly
managed
Farmland
Netherlands
Grassland
Cavk 1968
Britain
Grassland
Village 1983
Britain
Finland
Arizona
Currie & Bamford 1982
Jarvinen 1978
Enemar & Sjostrand 1972
Enemar & Sjostrand 1972
Enemar & Sjostrand 1972
Gustafsson 1988
Brawn & Balda 1988
Holroyd 1975
Beissinger & Bucher 1992
1994
401
LIMITATION OF BIRD BREEDING DENSITIES
Table 2. Continued
Species
Area
Habitat
~
~
American Kestrel
Wisconsin
Farmland
Ealco sparverius
Goldeneye
Scotland
Forest and lakes,
managed
Bucephala clangula
Goldeneye
Sweden
Forest and lakes
Goldeneye
Finland
Forest and lakes
Goldeneye
Canada
Forest and lakes
Barrow’s Goldeneye
British Columbia
Forest and lakes
Bucephala islandica
Wood duck
Massachusetts
Forest and lakes
Aix sponsa
Wood Duck
New York
Forest and lakes
Wood Duck
California
Marsh
Nestboxes removed or natural holes blocked. leading to a decline in breeding density
Mountain Bluebird
California
Pine-fir forest,
lightly managed
Great Tit*
Britain
Deciduous woodland.
unmanaged
Ash-throated Flycatcher
Arizona
Riparian, lightly
managed
Reference
~~
Hamerstrom et al. 1973
Dennis & Dow 1984
Sibn 1951
Eriksson 1982
Johnson 1967
Savard 1988
McLaughIin & Grice 1952
Haramis & Thompson 1985
Jones & Leopold 1967
Raphael & White 1984
East & Penins 1988
Brush 1983
Note: In addition to the experiments listed above, in two others the addition of nestboxes led to no increase in breeding density: European
Kestrel in an area of farmland in England (Viiage 1990) and BuWehead Bucephala albeola in an area of mainly parkland in British Columbia
(Gauthier & Smith 1987). In one other experiment in oak-pine woodland in California. the blocking of a proportion of nest holes led to no
reduction in the breeding density of songbirds (Waters et al. 1990).
creases the likelihood that any response observed in the
study species resulted from the treatment and not from some
other features peculiar to the area or time period. Statistically, the more the experiment is replicated, the stronger
the conclusions.
The most substantial feeding experiment, which covered
several successive winters, was that by van Balen (1980) in
the Netherlands. It was based in two areas of similar woodland 7 km apart, in one of which food was provided while
the other acted as a control. Before winter feeding began,
EXPERIMENTS INVOLVING FOOD
Table 3. Efects orpredator removal on tetraonids on two islands.
northern Sweden (from Marcstrom et al. 1988)
Circumstantial evidence that bird numbers are influenced
by food supply derives mainly from the observation that,
within species, changes in bird density from year to year,
or from one place to another, often correlate with temporal
and spatial changes in food supplies (Newton 1980). Not all
bird species are amenable to food provision experiments.
Ideally, they should live at high density in the same locality
year round, so that the effects of feeding on their subsequent
numbers can be assessed readily, and they must eat foods
which can be provided readily. These three constraints eliminate most species as easy subjects for experiment, and in
any case care must be taken to ensure than any food provided is nutritionally appropriate and adequate. Most published experiments concern tits (Paridae) which were given
seeds in winter, and their subsequent breeding numbers in
the same area were then measured from the number of nests
in nest boxes, supplied in excess.
Predators
preserved
Productivity
Brood size in August
% of hens with broods
Young per hen
*
3.3 0.1
59%
1.9
Predators
removed
5.5 f 0.1
77%
4.2
Under predator removal,
Yo increase in counts of
Numbers in
breeding season
Lek counts
Transect counts
Capercaillie
Tetrao urogallus
Black Grouse
Tetrao tetriz
174
56
168
80
402
IBIS
I. NEWTON
Table 4. Efects on avian prey of various predator-removal studies: a summary of experimental findings (B = birds, M
measured)
=
136
mammals, ? = not
Experimental
findings for prey
Prey species
Location
Increased Inpost- creased
Pred- Grade
In- breed- breedof
creased ing
ing
ators
re- experi- nest num- nummoved ment’ success bers
bers
Reference
Ruffed Grouse
Bonasa umbellus
Ruffed Grouse
Connecticut
Hill, New York
Valcour Island. New York
MB
3
Yes
No
No
Bump et a/. 1947
MB
1
Yes
No
No
King-necked Pheasant
Phasianus colchicus
Ring-necked Pheasant
Wild Turkey
Meleagris gallapavo
& Northern Bobwhite
Colinus virginianus
Grey Partridge
Per& perdir
Black Grouse
Tetrao tetrix
& Capercaillie
Tetrao urogallus
Ptarmigan
Lagopus lagopus
& Black Grouse
Various ducks
Various ducks
Various ducks
Various ducks
Simulated ground nests
Simulated ground nests
White-winged Dove
Zenaida asiatica
Southern Minnesota
MBz
2
Yes’
No
No
Bump et al. 1947
Crissey & Darrow 1949
Chesness et al. 1968
South Dakota
M
M
3
2
?
Yes
>
Texas
Yes
Yes
Yes
Trautman et al. 1974
Beasom 1974
England
MBL
3
Yes
Yes
Yes
Tapper et a!. 1990. 1991
Sweden
M
3
Yes’
Yes3
Yes’
Marcstrom et al. 1988
Sweden
B4
2
Yes’
No
No
Parker 1984
Minnesota
South Dakota
South Dakota
North Dakota
Manitoba
North Dakota
MB
M
M
3
?
?
?
M6
M
M
B’
Yes
Yes’
Yes
Yes’
No
2
2
>
?
2
2
2
Yes’
-
__
Yes’
Yes
-
-
?
Yes
Baker et al. 1968
Duebbert & Kantrud 1974
Duebbert & Lokemoen 1980
Greenwood 1986
Lynch 1972
Schrank 1972
Blankenship 1966
Texas
’
Sce ‘I’able 5.
’
Excludes raptors, which were left unharmed.
3
Yes
Yes
‘ Supported by statistical analysis.
t
Corvids only.
Great-tailed Grackles Cassidix mexicanus only.
’~Striped skunks only.
Great Tit Parus major breeding numbers in the two areas
were similar and fluctuated more or less in parallel from
year to year (Fig. 2). After feeding began, breeding densities
in the two areas diverged and no longer fluctuated in parallel. Over several years, breeding numbers in the experimental area averaged 40% higher than those in the control
area. The impact of artificial feeding varied between years
depending on the Beech Fagus silvatica seed crop, which was
the most variable major component in the natural food supply. Comparison of numbers in the experimental area in the
years before and after food provision indicated that the extra
feeding doubled the population in poor Beech years but
made little difference in good Beech years (Fig. 2). The fact
that the effects of food provision were most marked in years
when natural food was scarce provided further evidence that
winter food supplies influenced local breeding densities. On
this evidence. the Great Tits in this experiment fitted the
lower curve (1)in Figure 1. in that variation in winter conditions were mainly responsible for variations in breeding
density.
1994
403
LIMITATION OF BIRD BREEDIYG DENSITIES
Table 5. Summary of experiments on the limitation of breeding
density in birds
Appropriate
change in
breeding
density
occurred
Grade of
experiment'
Food provision (winter)
Nest-site provision
Predator reductionz
Parasite reduction
Totals
1
2
3
Total
(Yo)
4
6
8
18
23
1
0
28
5
6
4
32
0
4
1
17
17
11
1
62
ll(61)
30(95)
6(55)
71
8
8
69
0
0
70
0
0
800
0
. A T
.
I
0
-1
.
0
0
,
,
-7 - 8
Temperature ("C)
-9
I
-2 -3 - 4
l(100)
48(77)
.
0
-5
,
-6
,
,
-
-10 -11
Figure 3. Numbers of breeding Great Tits in a study area near
Turku, Finland, in relation to winter temperature (the average temperature in the months December-February). Open circles denote
normal winters and solid circles, winters when much artificial food
was provided. From Haartman (1973).
Grade 1 = simple before-and-after comparison in the same area:
grade 2 = simultaneous comparison between experimental and control area; grade 3 = reversal of treatments between experimental
and control areas or replication of experimental and control areas
(for further details. see text).
2 A total of 16 experiments included only 11 which examined the
effects of predator removal on breeding density.
area and year, sometimes one species responded while the
other did not (e.g. Krebs 1971). Where a response to food
provision occurred, breeding density increased by up to
around 100°/ocompared with that in control areas, and where
the birds were ringed, the increase in breeding density resulted from some combination of increased local survival
and increased immigration, affecting mainly first-year birds
(Krebs 1971. vanBalen 1980, Janssonet al. 1981).Similarly,
in the Song Sparrow Melospiza melodia on Mandarte Island,
western Canada, seed provision in one winter led to improved survival, especially of juveniles, and to increased
breeding density (38%) (Smith et al. 1980).
In an experiment with Carrion Crows Corvus corone. extra
food (hen eggs and chicks) was put out throughout one winter and spring to investigate whether territories would shrink
and extra pairs would settle (Yom-Tov 1974). This did not
happen, although the food was taken and nest sites were
Further north in Europe, Great Tit breeding densities were
greatly influenced by the severity of winter, with the lowest
densities following the coldest winters (Fig. 3). When food
was provided artificially in three winters, the same relationship held with weather but breeding densities were correspondingly higher (Haartman 1973). Other experiments on
tits, covering one or two winters, gave variable results. In
some areas, two species had access to the supplementary
food, and if each of these is counted as a separate experiment,
then, compared with control areas, 8 out of 13winter feeding
experiments led to obvious increases in the subsequent
breeding density (Table 1).The same species responded to
food provision in one area but not another, and in the same
180-
180160
120
U
g 100L
n
0
L
80-
5
40-
a
n
=
/
80-
'
supplementary
feedlng
20-
0
1
1
1
80
62
84
1
86
Year
1
68
.
1
1
70
72
40
20-
°
1
1
1
1
1
1
,
1
10
20
30
40
50
80
70
80
Beech crop index
Figure 2. Left: Numbers of Great Tit pairs
in two woodland areas in the Netherlands,
before and after the provision of extra food
in one area (from winter 1966-1967). Right:
Numbers in the experimental area in years
before and after the provision of extra food,
shown in relation to the Beech crop. Redrawn from van Balen (1980).
404
I. NEWTON
present in excess. So this experiment went against the idea
that food limited breeding density in Carrion Crows in a
direct and simple way. However, one might not expect a
sudden increase in a bird such as this, in which individuals
are long lived and territories normally remain stable for
years, despite some fluctuation in natural food supply. The
result might have been different if food had been provided
over a longer period (and not just in one winter and spring)
or if the existing birds had been removed to enable different
ones to settle. That food could act at the level of the individual
territory in shorter-lived species was shown in an experiment in which Sunflower Helianthus sparsijolius seeds were
provided in winter to Wood Nuthatches Sitta europaea, which
then took smaller territories than in another winter, so that
density was increased (Enoksson & Nilsson 1983).
In Red Grouse Lagopus 1. scoticus, burning or fertilizing
areas of heather (the food plant) promoted an increase in
breeding density 1year later over the previous year, as well
as over that in control areas nearby (Miller et al. 1970). This
occurred when the experiment was started in years with
low or moderate densities, but in a later trial, fertilizing an
area failed to halt a big decline (Watson & Moss 1979). The
Red Grouse in the area concerned underwent marked fluctuations, and these experiments suggested that the birds
could respond to an improved food supply during a period
of increase but not during a period of decline.
Artificial feeding of Black Grouse Tetrao tetrix in winter
started in Finland as a widespread management procedure
in an attempt to stop their decline in numbers. The birds
were provided with oats at lekking sites throughout the winter. Although the birds took the food, long-term population
decline continued, as did shorter-term cycles in numbers.
The only obvious effect of the feeding was change in the
local distribution of the grouse, which were attracted from
wide areas to leks where food was provided (Majakangas
1987). The procedure also was evaluated experimentally in
Sweden, where Black Grouse were fed at two leks for 4 years,
while those at three other leks in the same area were left as
controls. No differences in body-weights or survival were
noted between birds at the two types of lek (Willebrand
1988). This last experiment was in an area of abundant
natural winter food (Birch), but the conclusion from both
studies was that Black Grouse numbers were not limited by
winter food. This was in line with other studies which pointed to habitat deterioration as causing long-term decline and
to predation as the main year-by-year limiting factor (Angelstam et al. 1984, Marcstrom et al. 1988).
Turning to manipulation of summer food supplies, a problem hangs over the experiment of Franzblau & Collins (1980),
who placed extra food (Tenebrio larvae) in five territories of
Rufous-sided Towhees Pipilo erythrophthalmus montanus part
way through the breeding season. No change was detected
in the sizes of these territories before and after food provision
or in comparison with five control territories where no food
was provided. It may have been unreasonable to expect a
change in territory size during the course of a breeding season, when the adult population is normally static.
IBIS
136
Experiments involving reduction of food supplies caused
by the use of insecticides have been tried in summer, as an
adjunct to forest-insect control programmes. The chemicals
most often used in these programmes include DDT. carbaryl
and fenitrothion, applied in a wide range of dosages and
spraying regimes. In some studies, no effects of spraying
were apparent on local bird breeding densities. while in
others the reported declines may have been due more to
direct poisoning of birds by the pesticide than to reductions
in their food supplies (Pearce & Peakall 1977, Peakall & Bart
1983, Spray et al. 1987). However, in the study by Cooper
et al. (1990) in West Virginia, the chemical used was diflubenzuron, a growth regulator which kills insect larvae but
is nontoxic to birds. These authors counted the songbirds
present in three sprayed 59-ha plots for comparison with
those in three similar-sized unsprayed plots. Plots were separated by at least 150 m to minimize spray drift. Spraying
was done in early May, and bird counts followed from late
May to mid-July. No significant differences in the numbers
of 21 common species. or in their combined numbers, were
found between treated and untreated plots. Many species
were shown to turn to alternative foods on the sprayed plots,
and one species (Red-eyed Vireo Vireo olivaceous) studied in
detail was found to forage over larger areas than in unsprayed plots. The findings suggested that breeding density
was not affected in the same year by reduced summer food
supply, but the birds had settled by then and alternative
food sources were available. Similar results were obtained
in other studies involving the same chemical (Richmond et
al. 1979. DeReede 1982. Stribling & Smith 1987). The general conclusion from studies involving diflubenzuron was
that breeding densities of insectivorous species. after the
time of settlement, were not affected by reductions in the
larval insect component of the diet.
To summarize, some species in feeding experiments showed
clear evidence that breeding numbers were influenced by
winter food supplies, at least in some years or areas. Others
showed no evidence that they were influenced by food supplies in the years and areas concerned, but in some cases
the food may have been provided for too short a period or
at the wrong time of year. Reduction of insectivorous food
supplies in summer spray programmes caused no reduction
in the breeding densities of local songbirds.
EXPERIMENTS INVOLVING NEST SITES
While food supply could potentially limit the numbers of all
birds, in some species breeding density is often held at a
level lower than food would permit by shortage of some other
resource, notably nest sites. Limitation by nest sites is evident mainly in species which use special sites, such as cliffs
or tree cavities. The evidence is partly correlative, in that
spatial or temporal variations in the breeding density of such
species often parallel spatial or temporal variations in nestsite availability, and breeding pairs are absent from areas
which lack nest sites but which seem suitable in other re-
1994
LIMITATION OF BIRD BREEDING DENSITIES
spects (nonbreeders may live there). Those cliff nesters, such
as some hirundines, which have taken to nesting on buildings have thereby spread over huge areas from which they
were formerly absent.
Most experiments on nest-site provision have involved
species which normally nest in tree cavities but cannot excavate their own holes. Such species readily accept appropriately designed nestboxes. In any experiment involving
nest sites, one has to be sure that the acceptance of new
sites has allowed extra pairs to nest and has not merely
entailed shifts of existing pairs from other sites. The process
of density limitation depends on defence of the nest site, or
of the territory containing it, by the pair in occupation, so
that other pairs are excluded. Experimental demonstrations
of nest-site shortages provide some of the clearest examples
of resource limitation in birds. They also show the action of
successive limiting factors, for once the shortage of nest sites
has been rectified, numbers usually increase to a new higher
level, at which they may be assumed to be limited by other
factors.
Some studies have examined the response of the entire
cavity-nesting guild to nest-site provision or removal, enabling species differences in the degree of site limitation to
be assessed. In Ponderosa Pine Pinus ponderosa forest in Arizona, Brawn & Balda (1988) studied hole-nesting birds on
five 8-ha plots of different structure. On three plots they
counted all hole-nesting birds for 4 years, then added nestboxes and continued the counts for another 4 years. The
other two plots were left as controls: no boxes were provided,
but counts were continued throughout (Fig. 2).
The degree to which sites were limiting varied between
species and between plots, depending partly on the number
of dead snags present. Overall breeding densities (all hole
nesters combined) increased significantly after box provision
on the two plots with fewest natural sites. Increases occurred
progressively for 4 years (when the study ended), giving in
the fourth year overall densities 230% and 760% higher than
previously. On these plots, more than 90% of the hole nesters
found were in boxes. Three species responded strongly, so
were most clearly limited by nest-site availability before boxes were installed, namely the Violet-green Swallow Tachicinata thalassina. Pygmy Nuthatch Sitta pygmaea and Western Bluebird Sialia rnexicana. The last increased from 20 pairs
per km2 before box provision to 78-88 pairs per km2 after
box provision. Three other hole nesters did not respond significantly. In these same years, no sigruiicant density changes
occurred on the two control plots where no boxes were
provided. Similarly. in the third experimental plot, which
had the most natural sites, densities remained unchanged,
and only 3Oyo of the hole nesters used boxes. On this plot,
cavities seemed already surplus to needs, and the occurrence
of some box nests was attributed to birds switching from
natural sites. Different responses of species to nestbox provision might have depended on the degree to which boxes
were acceptable substitutes for natural sites, as well as reflecting different degrees of limitation and competitive abilities. In the presence of limited nest sites, dominant species
405
may obtain enough sites, and subordinate ones increasingly
obtain nest sites as more become available and the needs of
the dominants are satisfied. The role of competition for nest
sites in limiting the breeding densities of other hole nesters
has been shown experimentally by Dhondt & Eyckerman
(1980).van Balen et al. (1982) and Gustafsson (1988).
The results from 32 studies on nestbox provision are summarized in Table 2. Most were simple before-and-after studies, but some included control areas and replication. They
included a range of 25 species, from songbirds to ducks and
raptors. In 92Yo (30 of 32) of these studies, breeding density
of one or more species increased after box provision, suggesting that limitation by shortage of nest sites is widespread
among hole-nesting birds. However, many experiments were
in young managed woods, deficient in old and dead trees,
so may not be typical of all woods. Moreover, studies which
did not lead to increased breeding density were perhaps less
likely to be published. It is uncertain, therefore, how typical
of forest in general these findings might be. Nonetheless,
increases of two- to four-fold in breeding density were observed commonly and increases of 5-20-fold occasionally.
As expected, the increases were more marked in species that
defended little more than the nest site, such as Pied Flycatcher Ficedula hypoleuca and Tree Sparrow Passer montanus, than in species such as tits, which held large territories.
In Finland, Haartman (1971) recorded that following box
provision Pied Flycatchers could increase from virtual absence to densities of 2000 pairs per km2, greater than all
other species together in those areas.
As indicated above, nest sites are not always limiting for
hole-nesting birds, especially in mature forest with abundant
natural sites. In an oak-pine forest in California, Waters et
al. (11990) found 176 cavities on a 37-ha plot, a minimum
estimate of the total present. In 1 year they blocked 67 of
these cavities and in another year 106, yet in neither year
did the density of hole-nesting birds (or nests found) decline
more than in a nearby control plot. Evidently cavities were
surplus to needs in this forest.
Several studies (notably on Pied Flycatcher) showed that
numbers increased abruptly the year after boxes were installed, implying that large numbers of potential occupants
were generally available. Without the boxes, these birds
presumably would not have bred but would have remained
as part of a large nonbreeding contingent unable to breed
because of shortage of sites. In these species, limitation of
breeding density followed scenario (3) in Figure 1, because
in any 1 year more potential breeders had survived the
winter than could be supported by the nesting habitat. Other
studies showed that, following box provision, numbers increased slowly over several years (as in the Brawn & Balda
[1988] study), implying that no more than a small surplus
was present in any 1year and that reproduction or continued immigration contributed to the longer-term increase.
Whatever the species and its rate of increase, numbers eventually levelled off, regardless of the number of extra boxes
provided. The implication was that, once the shortage of
nest sites was rectified, another factor took over to limit
4 06
I. NEWTON
numbers at a higher level. Evidence for various tits and
raptors showed that this second factor was food supply
(Newton 1979, Dhondt & Eyckerman 1980).In such species,
then, densities in different areas were limited by either nest
sites or food, whichever was in shortest supply.
Hole nesters are not the only birds that have responded
to the experimental provision of nest sites. Population increases of other species have been noted following the provision of baskets or artificial stick nests in trees (Viage 1990).
rafts (as island substitutes, Crawford & Shelton [1978]). pylons (as tree substitutes, Steerihoffet at. [1993]) and buildings
(as cliff substitutes, Newton 119791). It seems that shortage
of nest sites can limit the distributions and breeding densities
of a wide range of bird species.
EXPERIMENTS INVOLVING PREDATORS
Observational evidence suggests that predators can have the
following effects on bird breeding densities. depending on
circumstances (Newton 1993):
(1) No obvious reduction in breeding density. This is apparent in some species which suffer considerable predation
but are demonstrably limited by other factors (examples
include the nestbox species just discussed). It is also apparent
in some large species (such as certain swans) which, in present conditions, are virtually immune to predation and often
have a large nonbreeding surplus of mature adults.
(2) Hold breeding density at an approximate equilibrium
well below the level that resources would permit (as in the
Grey Partridge Perdix perdix in some areas, Potts [1980]).
( 3 ) Cause marked fluctuations in breeding density, either
irregular or regular (cyclic),as suggested for some northern
gallinaceous birds exposed to periodic heavy predation (Lack
1954, Keith 1963, Angelstam et ul. 1984, Keith & Rusch
1988).
(4) Cause decline to extinction, as in some birds of oceanic
islands exposed to introduced rats and cats (Atkinson 1985).
Predator-removal experiments have not been concerned
in distinguishing these different types of impact, only in testing whether an effect was apparent, in other words, in distinguishing (1)from the rest. Most concerned ground-nesting game birds and ducks, stimulated by the commercial
interest of hunting.
One of the best predator-removal studies was conducted
on two forested islands in the Baltic Sea off northern Sweden
(Marcstrom Pt al. 1988). These islands were large enough to
sustain populations of several mammalian predators but also
were joined to the mainland in winter by sea ice, enabling
predators to move freely on and off. Mammalian predators
(mainly Fox Vulpes vulpes and Marten Martes martes) were
removed from one island but were left on the other. After
5 years, the treatments were reversed for four further years,
so that the experimental island then became the control and
vice versa, giving 9 years of study in all. The effects of predator removal were measured on four species of grouse, mainly Capercaillie Tetruo urogallus and Black Grouse. Where
IBIS
136
predators were removed, more young were produced and
subsequent breeding numbers were higher than where predators were left (Table 3). The conclusion was that mammalian predation limited the breeding density of the game
species concerned.
On these islands, as on the mainland. the mammalian
predators fed mainly on rodents and only secondarily on
game birds. It was observed that predation on game birds
was reduced and post-breeding populations were higher in
years when voles were numerous. Where predators were
left alone, grouse breeding success was correlated with vole
abundance, as most young grouse were produced in the peak
vole years, but no such relationship occurred where predators were removed. This was consistent with the view that
predators turned more to grouse when voles were scarce
and confirmed that predation was mainly responsible for
synchronizing grouse productivity with vole abundance. as
suggested by observational data (Angelstam et aI. 1984).
However, the removal of Foxes and Martens had no significant effect on vole abundance itself during two 4-year cycles, suggesting that these predators did not drive the vole
cycle.
The findings from a total of 1 5 predator-removal studies
involving various avian prey species are summarized in Table 4. Eight studies involved gallinaceous birds, six involved
ducks (including two with simulated nests) and one involved
doves. The parameters that were measured most commonly
included nest success, post-breeding numbers (or ratio of
large young to adults) and subsequent breeding numbers.
In 14 studies in which nest success was measured. all showed
an increase under predator removal; in eight stuhes in which
post-breeding numbers were measured, four showed an increase and of 11 studies in which breeding numbers were
measured, six showed an increase. Improved nest success
was not always reflected in increased post-breeding numbers, and. similarly, an increase in post-breeding numbers
was not always reHected in increased subsequent breeding
numbers. Overall. it seems that, in about half the studies in
Table 4, breeding density was limited by predation, even
though all species experienced heavy predation at some stage
of their lives. These studies were discussed in greater detail
by Newton (1993). They conform to the first (lower line)
scenario in Figure 1.
Almost all the species studied were ground nesters, which
as a group may have been more vulnerable to predation
than were other birds which nest in safer sites. None of the
species studied formed the main prey of the predators concerned, as the predators were generalists which fed mainly
on other prey (such as voles or lagomorphs) and therefore
were sustained mainly by other prey. These are precisely
the circumstances in which marked effects on vulnerable
subsidiary prey species might be expected, because the predators are buffered against decline in their subsidiary prey.
Predation was influenced not only by the numbers and types
of predators present but also by the availability of alternative
prey (such as rodents) and by habitat features such as nesting
cover. In all the experiments, the effects of predator removal
invariably were short lived, and when control stopped, the
1994
LIMITATION O F B I R D BREEDING DENSITIES
experimental areas were soon recolonized and predation
rates reverted to normal. The maximum breeding densities
achieved under predator removal were about twice as high
as in areas where predators were left. These effects were
similar to those found in food-provision experiments but
were trivial compared with those achieved with invertebrates, in experiments or in biological control programmes,
in which density differences of 100-fold or more followed
from the addition or removal of predators (Sih et al. 1985).
In several predator-removal studies, experimental and
control areas were adjacent to one another, leaving them
open to the effects of movements. The killing of predators
in one area may have affected both predator and prey numbers over a wider area, including the control area, and the
prey may have redistributed themselves each year, so that
any potential gains from predator removal in one area might
have been nullified by dispersal to the adjacent area so as
to even out the densities. Only five of the studies were on
islands or other well-separated areas, which would reduce
the probIem of movements (Crissey & Darrow 1949, Trautman et al. 1974. Greenwood 1986. Marcstrom et al. 1988,
Tapper et al. 1990). Another problem in some studies was
that predator numbers were not monitored apart from the
totals killed. It is hard to remove every last predator from
any area, especially with continuing immigration, so unless
their numbers in both treatment and control areas are monitored independently, it is impossible to assess the effectiveness of the removals.
Because most experiments were short lived, they could
not be expected to show long-term effects nor whether
breeding numbers increased to the maximum level possible.
Nor could they show whether predation regulated, rather
than merely limited, prey population density. If the experiments had been continued longer, it is theoretically possible
that the prey may have increased to the point at which
predators could no longer reduce their numbers to former
levels (the predator pit hypothesis). This was the outcome
of a predator-removal study on rabbits, providing evidence
for the existence of two equilibrium densities in the presence
of predators (Pech et al. 1992). It is also possible that, if
habitat quality (food and cover) had been changed instead
of predator numbers, a bigger and more lasting rise in density might have occurred.
EXPERIMENTS INVOLVING PARASITES
AND PATHOGENS
Empirical and modelling studies have suggested that parasites could have the same effects on host populations as
predators have on their prey, leading to either (1) no obvious
reduction in breeding density, (2) an equilibrium level lower
than resources would permit, (3) marked fluctuations in
abundance or (4) decline to extinction. Natural experiments,
involving the accidental introduction of a disease or disease
vector to a new area, have occurred from time to time,
sometimes with devastating effects on the local avifauna,
407
with the best-documented examples involving Hawaiian buds
(Warner 1968. van Riper et al. 1986).
Only recently have attempts been made to remove disease
organisms from wild populations by using chemicals to remove disease vectors from the local environment (Kissam et
al. 1975) or parasites from individual hosts and host nests
(Brown & Brown 1986. Hudson 1986, M~ller1990, Chapman & George 1991) and vaccination programmes to reduce
disease impacts (Hudson & Dobson 1990). However, almost
all the published work on birds so far has concerned effects
on individual survival and breeding performance, and few
studies have examined the effects of parasite removal on
breeding numbers.
One such study concerned the effects of the strongyle
worm parasite Trichostrongylus tenuis on Red Grouse. Removal of this parasite from individual grouse, using an anthelminthic drug, led to increases in both the breeding success and survival of individual grouse compared with
untreated individuals (Hudson 1986, Hudson et al. 1992).
Treatment of the majority of the grouse in the same way
prevented a cyclic decline in numbers on five occasions on
four different moors compared with trends in control areas
(P. Hudson, pers. comm.). The conclusion was that treatment of this particular parasite at the level of the grouse
population could prevent the periodic crashes in grouse
numbers previously attributed to this parasite. Red Grouse
in these areas thus conformed to the first (lower line) scenario in Figure 1,at least in the crash years.
A second study concerned the effects of parasitic Brownheaded Cowbirds Molothrus ater on the rare Kirtland’s Warbler Dendroica kirtlandii, now restricted to a small area of
Michigan (Rye1 1981, Mayfield 1983, Probst 1986, Weinrich
1988). A marked decline in warbler numbers between the
1960s and 1970s coincided with a period of heavy cowbird
parasitism, when warbler breeding success was reduced to
less than one young per nest. Following a period of cowbird
removal, warbler breeding success increased three-fold and
the decline in breeding numbers stopped. However, the warbler breeding population did not recover to its former levels.
So while cowbird parasitism clearly affected warbler nest
success, it remained uncertain whether it also affected
breeding numbers. Indeed, other factors were suggested
(Mayfield 1983). So this particular experiment was inconclusive with respect to breeding density. It is probably only
a matter of time before other experiments reveal the effects
of parasitism on breeding bird population levels. in addition
to effects on individual performance.
DISCUSSION
The experiments discussed above are summarized in Table
5. Many were simple before-and-after studies, but 27% included a control area, and another 27% also involved reversal of treatments or replication. Despite their various designs, field experiments have served to confirm that, within
areas of suitable habitat, the main potential limiting fac-
408
I. NEWTON
tors-whether resources or natural enemies-have affected
the breeding density of one bird species or another. They
also have confirmed that the same species can be limited in
breeding density by different factors in different areas or in
different years. The provision of food or removal of predators
Icd in extreme cases to a doubling of breeding densities compared with control areas, but provision of nestboxes often
led to much bigger increases-5-20-fold
in the most extreme cases.
A n obvious drawback of experiments is that they are possible only on certain species which have food supplies, nest
sites. predators or parasites that lend themselves to manipulation, are common enough for experiment and remain in
the same area long enough to assess the effect of the manipulation. For each of the species studied, experiments were
done on whatever limiting factor previous observation had
suggested might have been important in the area concerned.
A s a sample, then, the experiments which have been made
were predisposed to give positive results, and they could give
no indication of what would be the effect of manipulating
some quite different factor in the species concerned (such
as predation where breeding density appeared to be limited
by nest sites). If species for each type of experiment had been
selected from the available avifauna at random, rather than
0 1 1 the basis of prior knowledge, the number of positive
results would probably be much less than the 77% recorded
for the experiments reported here. In addition, all experiments so far have examined particular limiting factors individually. None has explored the possible interactions between different limiting factors, such as parasitism and food
shortage; this is an obvious opening for future work.
Because of thc small areas amenable to experiment, the
response to an experiment could be measured only in terms
of local breeding density, giving no indication of any possible
wider impacts resulting from local manipulation. For example. if some local treatment had caused more birds to
survive than could be accommodated in local nesting habitat, this could (through emigration) have led to increased
breeding densities over areas larger than the study site. Conversely, if the treatment had favoured immigration, densities
in surrounding areas might have been unaffected or deprcsscd as a result of thc experiment.
The evidence provided by experiments is as good as we
a r e likely to get, but even when a positive result was obtained. there is still the possibility that some unknown limiting factor changed in parallel to the one studied and caused
thc change in numbers. And even where change in some
particular factor did change numbers, it is not safe, of course,
lime that all changes in numbers were due to this same
factor. A given factor may be sufficient for some changes
but not nccessary to explain them all. Despite these caveats,
cxperiments are an improvement over observing natural
changes because in experiments it is the observer who brings
a bout the change.
Experiments on the limitation of breeding density reveal
little about the limitation of numbers at other times of year
or about the limitation of total population size at the start
IBIS
136
of breeding, consisting of breeders and nonbreeders. The
main practical problem in most bird species is that, in contrast to breeders, nonbreeders are often nonterritorial and
inconspicuous or flocking and range over much larger areas
than breeders. This behaviour makes them hard to count
accurately and to keep track of during experiments. However, whatever limits the numbers of breeders in a population must also indirectly set a ceiling on the numbers of
nonbreeders. Thus, once all available breeding habitat is
occupied, with no room for further settlers, an upper limit
is set on both the number of breeders and the annual output
of young. In due course, this must eventually limit the numbers of nonbreeders, which can increase only up to the point
where the annual additions (from reproduction and exit from
the breeding sector) match the annual losses (from mortality
and entry to the breeding sector). The numbers of nonbreeders would then stabilize at that level (Newton 1992). The
theoretical maximum ratio of nonbreeders to breeders was
calculated by Brown (1969) for a range of bird species with
different reproductive and mortality rates. In the most extreme examples, nonbreeders could outnumber breeders.
The existence of a theoretical maximum for the numbers of
nonbreeders (set by the numbers of breeders) does not of
course exclude the possibility that environmental constraints might restrict their numbers below this level. The
important point, however, is that whatever limits the breeding numbers of a species can also influence the total spring
population of breeders and nonbreeders, either directly or
indirectly.
I am grateful to Professor D. Jenkins for helpful discussion over many
years and for critical comments on this manuscript.
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