IBIS 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, PEl7 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 14 led 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.

As ever more land falls to intensive human use, many bird contents. But the number alive at the start of the next breed- species are increasingly constrained in distribution and ing season might depend largely on overwinter survival, in abundance by the progressive destruction and degradation turn dependent on food supply. In this case, increasing the of their habitats. For effective conservation, better under- winter food supply would have more intluence on breeding standing is needed of the factors that limit numbers within numbers than would decreasing the predation on nest con- areas of remaining habitat. Only then can such areas be tents. managed so as to sustain large populations of desired species. This paper is primarily about the limitation of breeding In this paper, I shall be concerned with the factors that limit densities for two reasons. First, it is in the early stages of bird numbers within the available habitat, concentrating on breeding each year that bird numbers reach their annual the experimental evidence. low, and it is upon the breeders that future additions to the The best we can hope to show by experiment is that some population usually depend. Second, it is in the breeding particular factor limits bird density at a particular place and season, when birds are most conspicuous and tied to fixed time. It is necessary to define the area carefully, for while sites, that they can be counted most readily. In fact, most density may be limited in this area, some individuals may experiments have been concerned with breeding numbers. move out and survive elsewhere, so that total numbers are In addition to breeders, however, some bird populations may unaffected. The emigrants may or may not return at a later contain a large nonbreeding contingent, which may or may date. It is important to specify the time period, because bird not be countable. numbers may be limited by different factors at different times No one is likely to dispute the fact that food supply or and only the last-acting may be crucial in setting the even- other resources could provide a ceiling to the numbers of tual population level. For example, the number of birds pres- any bird. The key question is, in practice, which species are ent at the end of a breeding season might depend largely on limited by resources and which are held at a level lower breeding success, in turn dependent on predation of nest than resources would permit by other factors, notably nat- 397 398 I. NEWTON IBIS 136

Model of limitation of breeding density 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 Surplus (ultimate) cause of death, while disease or predation is the Resource limlt immediate (proximate) cause. The importance of experi- Deficit ments 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 I densities of various external limiting factors, namely food Non-breeding period I Breeding period supply. nest sites, predators and parasites. I have excluded Figure 1. Model showing seasonal changes in bird numbers in experiments that have examined the role of territorial or relation to the carrying capacity of the breeding habitat (thick line). other social interactions in limiting density, which have been In the lower curve (l), overwinter losses are severe and reduce reviewed elsewhere (Newton 1992), and also experiments numbers well below the level that the breeding habitat would sup- on the role of food supply in influencing laying dates and port: in (2) overwinter losses are such that the numbers left in spring clutch sizes. match those that the breeding habitat will support and in (3) over- winter 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 EXPERIMENTAL DESIGN habitat and in (3) by the carrying capacity of the breeding habitat. 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 ural enemies such as predators, parasites or pathogens or same area year-round, or migratory, with individuals spend- human agency. Effective conservation of any species de- ing the nonbreeding and breeding periods in different areas. pends on knowing the limiting factors, for it is these external Numbers are highest at the end of one breeding season and factors which must be altered if an increase in population then decline to the start of the next. But within the nesting is to be achieved. Any factor might be considered limiting if habitat. breeding density can be limited, as birds compete it prevents at population increase or causes a decline. In for territorial space or nest sites. Three scenarios can be reality, no one factor is likely to account wholly for a given envisaged: population level. During a period of food shortage, for ex- (1) In some populations, overwinter losses-from what- ample, some individuals may starve, while other nonstarving ever limiting factors operate in winter-may be so great that, individuals may die from other causes such as predation. In by the start of breeding, the remaining birds are too few to such cases, the main limiting factor can be considered as occupy the nesting habitat fully, so that practically all in- the one which, once removed, will permit the greatest rise dividuals of appropriate age and condition could breed. In in numbers. this case, breeding density is limited by whatever factors act Because populations may be influenced by many different to reduce numbers in winter, and manipulation of these factors, acting individually or in combination, it is often hard winter factors would be needed to produce an increase in to tell the relative importance of each, except by experiment. breeding numbers. Moreover, the crucial factor cannot always be deduced from (2) In other populations, overwinter losses may reduce knowledge of mortality causes, even if such information were numbers to more or less the level that the nesting habitat available. Imagine that the density of a territorial species will support, so that again almost all potential breeders left was limited by some aspect of habitat quality, so that surplus at the end of winter could breed. In this case, manipulation individuals were forced into suboptimal habitat where they of both the factors influencing winter losses and the carrying were eaten by predators (the ‘doomed surplus’ model of capacity of the nesting habitat would be needed to produce Errington [1946]). From a study of mortality, one would an increase in breeding numbers. conclude that predators limited numbers because virtually (3) In yet other populations, overwinter losses may be all the mortality occurred through predation: however, the so light that, after the nesting habitat is fully occupied, a underlying limiting factor was habitat quality, which influ- surplus of potential breeders is left over which move on to enced the density of territories. To change breeding density breed elsewhere or form a nonbreeding component. In this in the long term would entail a change of habitat, not of case, manipulation of the factors influencing the carrying predators. and in each case surplus individuals would be capacity of the nesting habitat would be needed to permit a removed by predators or any other mortality agents avail- rise in breeding numbers. able locally. The important point is that the factors that cause Although, in this model, I have viewed the carrying ca- most mortality in a bird population are not necessarily those pacity of the breeding habitat at the time of settlement as 1994 LIMITATION OF BIRD BREEDING DENSITIES 3 99

Table 1. EKects of winterfood provision on the breeding density of various birds

Grade’ Increase Species Region (years) in density Reference

Great Tit Germany 3 (1) Yes Berndt et al. 1964 Parus major Finland 1(3) Yes Haartman 1973 2 (1) No Krebs 1971 Netherlands 2 (5) Yes van Balen 1980 Sweden 3 (2) Yes Kallander 1981 Blue Tit Germany 3 (1) No Berndt & Frantzen 1964 Parus caeruleus England 2 (1) Yes Krebs 1971 Sweden 3 (2) No Kallander 1981 Willow Tit Sweden 3 (1) Yes Jansson et aZ. 1981 Parus montanus Crested Tit Sweden 3 (1) Yes Jansson et al. 1981 Parus cristatus Coal Tit Scotland 2 (1) No A.J. Deadman (unpubl. PhD thesis, Parus ater University of Aberdeen. 1973) Black-capped Chickadee Pennsylvania 10) Yes Samson & Lewis 1979 Parus atricapillus Tufted Titmouse Pennsylvania 1 (1) No Samson & Lewis 1979 Parus bicolor Nuthatch Sweden 3 (2) Yes Enoksson & Nilsson 1983 Sitta europaea Song Sparrow British Columbia 2 (1) Yes Smith et al. 1980 Melospiza melodia Carrion Crow Scotland 1(1) No Yom-Tov 1974 Corvus corone Red Grouse Scotland 2 (1) YesZ Watson & Moss 1979 Lagopus 1. scoticus Black Grouse Sweden 3 (4) No Willebrand 1988 Tetrao tetrix

* See Table 5. In certain conditions only, see text. fixed, for some species this is probably an oversimplification. riod only. The commonest type of experiment involved a The numbers of birds that can settle in a given area of nesting single area in which breeding numbers were monitored for habitat may be variable within limits, depending on the some years, then the treatment was applied and numbers number of potential settlers available, with more individuals were monitored for several further years, giving a simple ‘squeezing in’ when the number of contenders is high. In before-and-after comparison (grade 1 in Tables 1-5). The this case, the numbers of birds left over at the end of winter weakness of this procedure is that. without a control, one could have some influence on breeding density, even in the cannot be certain that a change in breeding numbers was third situation described above. In practice this means that due to the treatment and not to some other unknown factor under severe competition for space, some individuals might which changed at the same time. The second type of ex- accept smaller territories or inferior nest sites, facilitating periment involved two areas, with the treatment applied in higher density (Davies 1978. Newton 1992). As another one area while the other area served as a control (grade 2). modification, numbers may fit the carrying capacity of the If breeding numbers changed more in the experimental than nesting habitat at the start of breeding but then fall below in the control area, this was taken as evidence that the it, as a result of mortality or as carrying capacity rises with treatment influenced numbers. Ideally, the two areas should the seasonal improvement in conditions. Eventually, the be far enough apart that treatment in the experimental area production of young ensures a rise in density to give another, does not affect birds in the control area, which, if the areas post-breeding peak. Finally. any given population may fit were close, could move back and forth. The third type of one of the patterns described above in some years and areas experiment involved some replication, either by reversing and a different pattern in other years or areas. the treatments, so that after a time the experimental area In some of the experiments reported below, the experi- became the control and vice versa, or by the simultaneous mental treatment covered the whole year, while in others use of several experimental and several control areas (grade it covered the nonbreeding period only or the breeding pe- 3). Such replication strengthens the findings because it in- $00 I. NEWTON IBIS 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 Habitat Reference

Nestboxes added, leading to an increase in breeding activity Starling New Zealand Farmland Coleman 1974 Sturnus vulgaris House Sparrow New Zealand Farmland Coleman 1974 Passer domesticus Tree Sparrow England Farmland Boyd 1932 Passer montanus Tree Sparrow Germany Farmland Creutz 1949 Tree sparrow Germany Pine plantation Dornbusch 1973 Tree Sparrow Germany Farmland Gauhll984 Western Bluebird Arizona Ponderosa pine Brawn & Balda 1988 Sialia rnexicana" forest, lightly managed Mountain Bluebird Manitoba Parkland and meadows Cutforth 1968 Sialia currucoides Mountain Bluebird Manitoba Mainly farmland Miller et al. 1970 Eastern Bluebird Manitoba Mainly farmland Miller et al. 1970 Sialia sialis Rcdstart Finland Birch forest, rarvinen 1978 Phoenicurus phoenicurus lightly managed Pygmy Nuthatch Arizona Pine forest, lightly managed Brawn & Balda 1988 Sitta pygmaea** Mountain Chickadee California Conifer forest, Dahlsten & Copper 1979 Parus gambeli lightly managed Great Tit Second-growth forest Higuchi 1978 Parus major Varied Tit Japan Second-growth forest Higuchi 1978 Parus varius Blue Tit Britain Deciduous woodland, East & Perrins 1988 Parus cueruleus* unmanaged Pied flycatcher Britain Deciduous woodland, Currie & Bamford 1982 Ficedula hypoleuca managed Pied Flycatcher Finland Birch forest, Jarvinen 1978 lightly managed Pied Flycatcher* Northern Sweden Subalpine Birch Enemar & Sjostrand 1972 forest, natural Pied Flycatcher Southern Sweden Broad-leaved Enemar & Sjostrand 1972 woodland, managed Pied Flycatcher Southern Sweden Broad-leaved Enemar & Sjostrand 1972 woodland, managed Collared Flycatcher Sweden Deciduous woodland. Gustafsson 1988 Ficedula albicollis** managed Violet-green Swallow Arizona Pine forest, lightly Brawn & Balda 1988 Tachycineta thalassina** managed Tree Swallow Ontario Mixed. rural Holroyd 1975 Iridoprocne bicolor Purplc Martin Ontario Mixed, rural Holroyd 1975 Progne subis Ash-throated Flycatcher Arizona Riparian, lightly Brush 1983 Myiarchus cineraseens* managed Green-mmped Parrotlet Venezuela Farmland Beissinger & Bucher 1992 Forpus passerinus' European Kestrel Netherlands Grassland Cavk 1968 Falco tinnunculus European Kestrel Britain Grassland Village 1983 1994 LIMITATION OF BIRD BREEDING DENSITIES 401

Table 2. Continued

Species Area Habitat Reference

~ ~ ~~ American Kestrel Wisconsin Farmland Hamerstrom et al. 1973 Ealco sparverius Goldeneye Scotland Forest and lakes, Dennis & Dow 1984 Bucephala clangula managed Goldeneye Sweden Forest and lakes Sibn 1951 Goldeneye Finland Forest and lakes Eriksson 1982 Goldeneye Canada Forest and lakes Johnson 1967 Barrow’s Goldeneye British Columbia Forest and lakes Savard 1988 Bucephala islandica Wood duck Massachusetts Forest and lakes McLaughIin & Grice 1952 Aix sponsa Wood Duck New York Forest and lakes Haramis & Thompson 1985 Wood Duck California Marsh Jones & Leopold 1967 Nestboxes removed or natural holes blocked. leading to a decline in breeding density Mountain Bluebird California Pine-fir forest, Raphael & White 1984 lightly managed Great Tit* Britain Deciduous woodland. East & Penins 1988 unman aged Ash-throated Flycatcher Arizona Riparian, lightly Brush 1983 managed

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 The most substantial feeding experiment, which covered study species resulted from the treatment and not from some several successive winters, was that by van Balen (1980) in other features peculiar to the area or time period. Statisti- the Netherlands. It was based in two areas of similar wood- cally, the more the experiment is replicated, the stronger land 7 km apart, in one of which food was provided while the conclusions. 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, Predators Predators or from one place to another, often correlate with temporal preserved removed and spatial changes in food supplies (Newton 1980). Not all Productivity bird species are amenable to food provision experiments. Brood size in August 3.3 0.1 5.5 0.1 Ideally, they should live at high density in the same locality * f % of hens with broods 59% 77% year round, so that the effects of feeding on their subsequent Young per hen 1.9 4.2 numbers can be assessed readily, and they must eat foods which can be provided readily. These three constraints elim- Under predator removal, inate most species as easy subjects for experiment, and in Yo increase in counts of any case care must be taken to ensure than any food pro- Numbers in Capercaillie Black Grouse vided is nutritionally appropriate and adequate. Most - breeding season Tetrao urogallus Tetrao tetriz lished experiments concern tits (Paridae) which were given seeds in winter, and their subsequent breeding numbers in Lek counts 174 168 the same area were then measured from the number of nests Transect counts 56 80 in nest boxes, supplied in excess. 402 I. NEWTON IBIS 136

Table 4. Efects on avian prey of various predator-removal studies: a summary of experimental findings (B = birds, M = mammals, ? = not measured)

Experimental findings for prey

In- creased In- post- creased Pred- Grade In- breed- breed- ators of creased ing ing re- experi- nest num- num- Prey species Location moved ment’ success bers bers Reference

Ruffed Grouse Connecticut MB 3 Yes No No Bump et a/. 1947 Bonasa umbellus Hill, New York Ruffed Grouse Valcour Island. New York MB 1 Yes No No Bump et al. 1947 Crissey & Darrow 1949 King-necked Pheasant Southern Minnesota MBz 2 Yes’ No No Chesness et al. 1968 Phasianus colchicus Ring-necked Pheasant South Dakota M 3 ? Yes > Trautman et al. 1974 Wild Turkey Texas M 2 Yes Yes Y es Beasom 1974 Meleagris gallapavo & Northern Bobwhite Colinus virginianus Grey Partridge England MBL 3 Yes Yes Yes Tapper et a!. 1990. 1991 Per& perdir Black Grouse Sweden M 3 Yes’ Yes3 Yes’ Marcstrom et al. 1988 Tetrao tetrix & Capercaillie Tetrao urogallus Ptarmigan Sweden B4 2 Yes’ No No Parker 1984 Lagopus lagopus & Black Grouse Various ducks Minnesota MB 3 Yes ? No Baker et al. 1968 Various ducks South Dakota M 2 Yes’ ? Yes Duebbert & Kantrud 1974 Various ducks South Dakota M 2 Yes ? Yes Duebbert & Lokemoen 1980 Various ducks North Dakota M6 3 Yes’ > ? Greenwood 1986 Simulated ground nests Manitoba M 2 Yes’ - __ Lynch 1972 Simulated ground nests North Dakota M 2 Yes’ - - Schrank 1972 White-winged Dove Texas B’ 2 Yes ? Yes Blankenship 1966 Zenaida asiatica

’ Sce ‘I’able 5. ’ Excludes raptors, which were left unharmed. ‘ 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 years before and after food provision indicated that the extra were similar and fluctuated more or less in parallel from feeding doubled the population in poor Beech years but year to year (Fig. 2). After feeding began, breeding densities made little difference in good Beech years (Fig. 2). The fact in the two areas diverged and no longer fluctuated in par- that the effects of food provision were most marked in years allel. Over several years, breeding numbers in the experi- when natural food was scarce provided further evidence that mental area averaged 40% higher than those in the control winter food supplies influenced local breeding densities. On area. The impact of artificial feeding varied between years this evidence. the Great Tits in this experiment fitted the depending on the Beech Fagus silvatica seed crop, which was lower curve (1) in Figure 1. in that variation in winter con- the most variable major component in the natural food sup- ditions were mainly responsible for variations in breeding ply. Comparison of numbers in the experimental area in the density. 1994 LIMITATION OF BIRD BREEDIYG DENSITIES 403

Table 5. Summary of experiments on the limitation of breeding 8 71 density in birds

Appro- 8 69 priate 0 change in 0 Grade of breeding 70 experiment' density 00 occurred 800 1 2 3 Total (Yo)

00 0 Food provision (winter) 4 6 8 18 ll(61) 0 Nest-site provision 23 5 4 32 30(95) .AT I . . I . , , , , , - Predator reductionz 1 6 4 11 6(55) 0 -1 -2 -3 -4 -5 -6 -7 -8 -9 -10 -11 Parasite reduction 0 0 1 1 l(100) Temperature ("C) Totals 28 17 17 62 48(77) Figure 3. Numbers of breeding Great Tits in a study area near Turku, Finland, in relation to winter temperature (the average tem- Grade 1 = simple before-and-after comparison in the same area: perature in the months December-February). Open circles denote grade 2 = simultaneous comparison between experimental and con- normal winters and solid circles, winters when much artificial food trol area; grade 3 = reversal of treatments between experimental was provided. From Haartman (1973). 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 area and year, sometimes one species responded while the effects of predator removal on breeding density. other did not (e.g. Krebs 1971). Where a response to food provision occurred, breeding density increased by up to around 100°/o compared with that in control areas, and where Further north in Europe, Great Tit breeding densities were the birds were ringed, the increase in breeding density re- greatly influenced by the severity of winter, with the lowest sulted from some combination of increased local survival densities following the coldest winters (Fig. 3). When food and increased immigration, affecting mainly first-year birds was provided artificially in three winters, the same relation- (Krebs 1971. vanBalen 1980, Janssonet al. 1981).Similarly, ship held with weather but breeding densities were corre- in the Song Sparrow Melospiza melodia on Mandarte Island, spondingly higher (Haartman 1973). Other experiments on western Canada, seed provision in one winter led to im- tits, covering one or two winters, gave variable results. In proved survival, especially of juveniles, and to increased some areas, two species had access to the supplementary breeding density (38%) (Smith et al. 1980). food, and if each of these is counted as a separate experiment, In an experiment with Carrion Crows Corvus corone. extra then, compared with control areas, 8 out of 13winter feeding food (hen eggs and chicks) was put out throughout one win- experiments led to obvious increases in the subsequent ter and spring to investigate whether territories would shrink breeding density (Table 1). The same species responded to and extra pairs would settle (Yom-Tov 1974). This did not food provision in one area but not another, and in the same happen, although the food was taken and nest sites were

180- 180-

160

120 U g 100- nL 0 / 80- 80- Figure 2. Left: Numbers of Great Tit pairs aL n in two woodland areas in the Netherlands, 5 40- 40 before and after the provision of extra food 'supplementary in one area (from winter 1966-1967). Right: = 20- feedlng . 20- Numbers in the experimental area in years

0 1111111° 1111 11 , 1 before and after the provision of extra food, 80 62 84 86 68 70 72 10 20 30 40 50 80 70 80 shown in relation to the Beech crop. Re- Year Beech crop index drawn from van Balen (1980). 404 I. NEWTON IBIS 136 present in excess. So this experiment went against the idea Experiments involving reduction of food supplies caused that food limited breeding density in Carrion Crows in a by the use of insecticides have been tried in summer, as an direct and simple way. However, one might not expect a adjunct to forest-insect control programmes. The chemicals sudden increase in a bird such as this, in which individuals most often used in these programmes include DDT. carbaryl are long lived and territories normally remain stable for and fenitrothion, applied in a wide range of dosages and years, despite some fluctuation in natural food supply. The spraying regimes. In some studies, no effects of spraying result might have been different if food had been provided were apparent on local bird breeding densities. while in over a longer period (and not just in one winter and spring) others the reported declines may have been due more to or if the existing birds had been removed to enable different direct poisoning of birds by the pesticide than to reductions ones to settle. That food could act at the level of the individual in their food supplies (Pearce & Peakall 1977, Peakall & Bart territory in shorter-lived species was shown in an experi- 1983, Spray et al. 1987). However, in the study by Cooper ment in which Sunflower Helianthus sparsijolius seeds were et al. (1990) in West Virginia, the chemical used was diflu- provided in winter to Wood Nuthatches Sitta europaea, which benzuron, a growth regulator which kills insect larvae but then took smaller territories than in another winter, so that is nontoxic to birds. These authors counted the songbirds density was increased (Enoksson & Nilsson 1983). present in three sprayed 59-ha plots for comparison with In Red Grouse Lagopus 1. scoticus, burning or fertilizing those in three similar-sized unsprayed plots. Plots were sep- areas of heather (the food plant) promoted an increase in arated by at least 150 m to minimize spray drift. Spraying breeding density 1year later over the previous year, as well was done in early May, and bird counts followed from late as over that in control areas nearby (Miller et al. 1970). This May to mid-July. No significant differences in the numbers occurred when the experiment was started in years with of 21 common species. or in their combined numbers, were low or moderate densities, but in a later trial, fertilizing an found between treated and untreated plots. Many species area failed to halt a big decline (Watson & Moss 1979). The were shown to turn to alternative foods on the sprayed plots, Red Grouse in the area concerned underwent marked fluc- and one species (Red-eyed Vireo Vireo olivaceous) studied in tuations, and these experiments suggested that the birds detail was found to forage over larger areas than in un- could respond to an improved food supply during a period sprayed plots. The findings suggested that breeding density of increase but not during a period of decline. was not affected in the same year by reduced summer food Artificial feeding of Black Grouse Tetrao tetrix in winter supply, but the birds had settled by then and alternative started in Finland as a widespread management procedure food sources were available. Similar results were obtained in an attempt to stop their decline in numbers. The birds in other studies involving the same chemical (Richmond et were provided with oats at lekking sites throughout the win- al. 1979. DeReede 1982. Stribling & Smith 1987). The gen- ter. Although the birds took the food, long-term population eral conclusion from studies involving diflubenzuron was decline continued, as did shorter-term cycles in numbers. that breeding densities of insectivorous species. after the The only obvious effect of the feeding was change in the time of settlement, were not affected by reductions in the local distribution of the grouse, which were attracted from larval insect component of the diet. wide areas to leks where food was provided (Majakangas To summarize, some species in feeding experiments showed 1987). The procedure also was evaluated experimentally in clear evidence that breeding numbers were influenced by Sweden, where Black Grouse were fed at two leks for 4 years, winter food supplies, at least in some years or areas. Others while those at three other leks in the same area were left as showed no evidence that they were influenced by food sup- controls. No differences in body-weights or survival were plies in the years and areas concerned, but in some cases noted between birds at the two types of lek (Willebrand the food may have been provided for too short a period or 1988). This last experiment was in an area of abundant at the wrong time of year. Reduction of insectivorous food natural winter food (Birch), but the conclusion from both supplies in summer spray programmes caused no reduction studies was that Black Grouse numbers were not limited by in the breeding densities of local songbirds. winter food. This was in line with other studies which point- ed to habitat deterioration as causing long-term decline and to predation as the main year-by-year limiting factor (An- EXPERIMENTS INVOLVING NEST SITES gelstam et al. 1984, Marcstrom et al. 1988). Turning to manipulation of summer food supplies, a prob- While food supply could potentially limit the numbers of all lem hangs over the experiment of Franzblau & Collins (1980), birds, in some species breeding density is often held at a who placed extra food (Tenebrio larvae) in five territories of level lower than food would permit by shortage of some other Rufous-sided Towhees Pipilo erythrophthalmus montanus part resource, notably nest sites. Limitation by nest sites is evi- way through the breeding season. No change was detected dent mainly in species which use special sites, such as cliffs in the sizes of these territories before and after food provision or tree cavities. The evidence is partly correlative, in that or in comparison with five control territories where no food spatial or temporal variations in the breeding density of such was provided. It may have been unreasonable to expect a species often parallel spatial or temporal variations in nest- change in territory size during the course of a breeding sea- site availability, and breeding pairs are absent from areas son, when the adult population is normally static. which lack nest sites but which seem suitable in other re- 1994 LIMITATION OF BIRD BREEDING DENSITIES 405 spects (nonbreeders may live there). Those cliff nesters, such may obtain enough sites, and subordinate ones increasingly as some hirundines, which have taken to nesting on build- obtain nest sites as more become available and the needs of ings have thereby spread over huge areas from which they the dominants are satisfied. The role of competition for nest were formerly absent. sites in limiting the breeding densities of other hole nesters Most experiments on nest-site provision have involved has been shown experimentally by Dhondt & Eyckerman species which normally nest in tree cavities but cannot ex- (1980).van Balen et al. (1982) and Gustafsson (1988). cavate their own holes. Such species readily accept appro- The results from 32 studies on nestbox provision are sum- priately designed nestboxes. In any experiment involving marized in Table 2. Most were simple before-and-after stud- nest sites, one has to be sure that the acceptance of new ies, but some included control areas and replication. They sites has allowed extra pairs to nest and has not merely included a range of 25 species, from songbirds to ducks and entailed shifts of existing pairs from other sites. The process raptors. In 92Yo (30 of 32) of these studies, breeding density of density limitation depends on defence of the nest site, or of one or more species increased after box provision, sug- of the territory containing it, by the pair in occupation, so gesting that limitation by shortage of nest sites is widespread that other pairs are excluded. Experimental demonstrations among hole-nesting birds. However, many experiments were of nest-site shortages provide some of the clearest examples in young managed woods, deficient in old and dead trees, of resource limitation in birds. They also show the action of so may not be typical of all woods. Moreover, studies which successive limiting factors, for once the shortage of nest sites did not lead to increased breeding density were perhaps less has been rectified, numbers usually increase to a new higher likely to be published. It is uncertain, therefore, how typical level, at which they may be assumed to be limited by other of forest in general these findings might be. Nonetheless, factors. increases of two- to four-fold in breeding density were ob- Some studies have examined the response of the entire served commonly and increases of 5-20-fold occasionally. cavity-nesting guild to nest-site provision or removal, en- As expected, the increases were more marked in species that abling species differences in the degree of site limitation to defended little more than the nest site, such as Pied Fly- be assessed. In Ponderosa Pine Pinus ponderosa forest in Ar- catcher Ficedula hypoleuca and Tree Sparrow Passer montan- izona, Brawn & Balda (1988) studied hole-nesting birds on us, than in species such as tits, which held large territories. five 8-ha plots of different structure. On three plots they In Finland, Haartman (1971) recorded that following box counted all hole-nesting birds for 4 years, then added nest- provision Pied Flycatchers could increase from virtual ab- boxes and continued the counts for another 4 years. The sence to densities of 2000 pairs per km2, greater than all other two plots were left as controls: no boxes were provided, other species together in those areas. but counts were continued throughout (Fig. 2). As indicated above, nest sites are not always limiting for The degree to which sites were limiting varied between hole-nesting birds, especially in mature forest with abundant species and between plots, depending partly on the number natural sites. In an oak-pine forest in California, Waters et of dead snags present. Overall breeding densities (all hole al. (11990) found 176 cavities on a 37-ha plot, a minimum nesters combined) increased significantly after box provision estimate of the total present. In 1 year they blocked 67 of on the two plots with fewest natural sites. Increases occurred these cavities and in another year 106, yet in neither year progressively for 4 years (when the study ended), giving in did the density of hole-nesting birds (or nests found) decline the fourth year overall densities 230% and 760% higher than more than in a nearby control plot. Evidently cavities were previously. On these plots, more than 90% of the hole nesters surplus to needs in this forest. found were in boxes. Three species responded strongly, so Several studies (notably on Pied Flycatcher) showed that were most clearly limited by nest-site availability before box- numbers increased abruptly the year after boxes were in- es were installed, namely the Violet-green Swallow Tachi- stalled, implying that large numbers of potential occupants cinata thalassina. Pygmy Nuthatch Sitta pygmaea and West- were generally available. Without the boxes, these birds ern Bluebird Sialia rnexicana. The last increased from 20 pairs presumably would not have bred but would have remained per km2 before box provision to 78-88 pairs per km2 after as part of a large nonbreeding contingent unable to breed box provision. Three other hole nesters did not respond sig- because of shortage of sites. In these species, limitation of nificantly. In these same years, no sigruiicant density changes breeding density followed scenario (3) in Figure 1, because occurred on the two control plots where no boxes were in any 1 year more potential breeders had survived the provided. Similarly. in the third experimental plot, which winter than could be supported by the nesting habitat. Other had the most natural sites, densities remained unchanged, studies showed that, following box provision, numbers in- and only 3Oyo of the hole nesters used boxes. On this plot, creased slowly over several years (as in the Brawn & Balda cavities seemed already surplus to needs, and the occurrence [1988] study), implying that no more than a small surplus of some box nests was attributed to birds switching from was present in any 1 year and that reproduction or contin- natural sites. Different responses of species to nestbox pro- ued immigration contributed to the longer-term increase. vision might have depended on the degree to which boxes Whatever the species and its rate of increase, numbers even- were acceptable substitutes for natural sites, as well as re- tually levelled off, regardless of the number of extra boxes flecting different degrees of limitation and competitive abil- provided. The implication was that, once the shortage of ities. In the presence of limited nest sites, dominant species nest sites was rectified, another factor took over to limit 4 0 6 I. NEWTON IBIS 136 numbers at a higher level. Evidence for various tits and predators were removed, more young were produced and raptors showed that this second factor was food supply subsequent breeding numbers were higher than where pred- (Newton 1979, Dhondt & Eyckerman 1980).In such species, ators were left (Table 3). The conclusion was that mam- then, densities in different areas were limited by either nest malian predation limited the breeding density of the game sites or food, whichever was in shortest supply. species concerned. Hole nesters are not the only birds that have responded On these islands, as on the mainland. the mammalian to the experimental provision of nest sites. Population in- predators fed mainly on rodents and only secondarily on creases of other species have been noted following the pro- game birds. It was observed that predation on game birds vision of baskets or artificial stick nests in trees (Viage 1990). was reduced and post-breeding populations were higher in rafts (as island substitutes, Crawford & Shelton [1978]). py- years when voles were numerous. Where predators were lons (as tree substitutes, Steerihoffet at. [1993]) and buildings left alone, grouse breeding success was correlated with vole (as cliff substitutes, Newton 119791). It seems that shortage abundance, as most young grouse were produced in the peak of nest sites can limit the distributions and breeding densities vole years, but no such relationship occurred where pred- of a wide range of bird species. ators 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 EXPERIMENTS INVOLVING PREDATORS suggested by observational data (Angelstam et aI. 1984). However, the removal of Foxes and Martens had no signif- Observational evidence suggests that predators can have the icant effect on vole abundance itself during two 4-year cy- following effects on bird breeding densities. depending on cles, suggesting that these predators did not drive the vole circumstances (Newton 1993): cycle. (1) No obvious reduction in breeding density. This is ap- The findings from a total of 15 predator-removal studies parent in some species which suffer considerable predation involving various avian prey species are summarized in Ta- but are demonstrably limited by other factors (examples ble 4. Eight studies involved gallinaceous birds, six involved include the nestbox species just discussed). It is also apparent ducks (including two with simulated nests) and one involved in some large species (such as certain swans) which, in pres- doves. The parameters that were measured most commonly ent conditions, are virtually immune to predation and often included nest success, post-breeding numbers (or ratio of have a large nonbreeding surplus of mature adults. large young to adults) and subsequent breeding numbers. (2) Hold breeding density at an approximate equilibrium In 14 studies in which nest success was measured. all showed well below the level that resources would permit (as in the an increase under predator removal; in eight stuhes in which Grey Partridge Perdix perdix in some areas, Potts [1980]). post-breeding numbers were measured, four showed an in- (3) Cause marked fluctuations in breeding density, either crease and of 11 studies in which breeding numbers were irregular or regular (cyclic), as suggested for some northern measured, six showed an increase. Improved nest success gallinaceous birds exposed to periodic heavy predation (Lack was not always reflected in increased post-breeding num- 1954, Keith 1963, Angelstam et ul. 1984, Keith & Rusch bers, and. similarly, an increase in post-breeding numbers 1988). was not always reHected in increased subsequent breeding (4) Cause decline to extinction, as in some birds of oceanic numbers. Overall. it seems that, in about half the studies in islands exposed to introduced rats and cats (Atkinson 1985). Table 4, breeding density was limited by predation, even Predator-removal experiments have not been concerned though all species experienced heavy predation at some stage in distinguishing these different types of impact, only in test- of their lives. These studies were discussed in greater detail ing whether an effect was apparent, in other words, in dis- by Newton (1993). They conform to the first (lower line) tinguishing (1)from the rest. Most concerned ground-nest- scenario in Figure 1. ing game birds and ducks, stimulated by the commercial Almost all the species studied were ground nesters, which interest of hunting. as a group may have been more vulnerable to predation One of the best predator-removal studies was conducted than were other birds which nest in safer sites. None of the on two forested islands in the Baltic Sea off northern Sweden species studied formed the main prey of the predators con- (Marcstrom Pt al. 1988). These islands were large enough to cerned, as the predators were generalists which fed mainly sustain populations of several mammalian predators but also on other prey (such as voles or lagomorphs) and therefore were joined to the mainland in winter by sea ice, enabling were sustained mainly by other prey. These are precisely predators to move freely on and off. Mammalian predators the circumstances in which marked effects on vulnerable (mainly Fox Vulpes vulpes and Marten Martes martes) were subsidiary prey species might be expected, because the pred- removed from one island but were left on the other. After ators are buffered against decline in their subsidiary prey. 5 years, the treatments were reversed for four further years, Predation was influenced not only by the numbers and types so that the experimental island then became the control and of predators present but also by the availability of alternative vice versa, giving 9 years of study in all. The effects of pred- prey (such as rodents) and by habitat features such as nesting ator removal were measured on four species of grouse, main- cover. In all the experiments, the effects of predator removal ly Capercaillie Tetruo urogallus and Black Grouse. Where invariably were short lived, and when control stopped, the 1994 LIMITATION OF BIRD BREEDING DENSITIES 407

experimental areas were soon recolonized and predation with the best-documented examples involving Hawaiian buds rates reverted to normal. The maximum breeding densities (Warner 1968. van Riper et al. 1986). achieved under predator removal were about twice as high Only recently have attempts been made to remove disease as in areas where predators were left. These effects were organisms from wild populations by using chemicals to re- similar to those found in food-provision experiments but move disease vectors from the local environment (Kissam et were trivial compared with those achieved with inverte- al. 1975) or parasites from individual hosts and host nests brates, in experiments or in biological control programmes, (Brown & Brown 1986. Hudson 1986, M~ller1990, Chap- in which density differences of 100-fold or more followed man & George 1991) and vaccination programmes to reduce from the addition or removal of predators (Sih et al. 1985). disease impacts (Hudson & Dobson 1990). However, almost In several predator-removal studies, experimental and all the published work on birds so far has concerned effects control areas were adjacent to one another, leaving them on individual survival and breeding performance, and few open to the effects of movements. The killing of predators studies have examined the effects of parasite removal on in one area may have affected both predator and prey num- breeding numbers. bers over a wider area, including the control area, and the One such study concerned the effects of the strongyle prey may have redistributed themselves each year, so that worm parasite Trichostrongylus tenuis on Red Grouse. Re- any potential gains from predator removal in one area might moval of this parasite from individual grouse, using an an- have been nullified by dispersal to the adjacent area so as thelminthic drug, led to increases in both the breeding suc- to even out the densities. Only five of the studies were on cess and survival of individual grouse compared with islands or other well-separated areas, which would reduce untreated individuals (Hudson 1986, Hudson et al. 1992). the probIem of movements (Crissey & Darrow 1949, Traut- Treatment of the majority of the grouse in the same way man et al. 1974. Greenwood 1986. Marcstrom et al. 1988, prevented a cyclic decline in numbers on five occasions on Tapper et al. 1990). Another problem in some studies was four different moors compared with trends in control areas that predator numbers were not monitored apart from the (P. Hudson, pers. comm.). The conclusion was that treat- totals killed. It is hard to remove every last predator from ment of this particular parasite at the level of the grouse any area, especially with continuing immigration, so unless population could prevent the periodic crashes in grouse their numbers in both treatment and control areas are mon- numbers previously attributed to this parasite. Red Grouse itored independently, it is impossible to assess the effective- in these areas thus conformed to the first (lower line) sce- ness of the removals. nario in Figure 1, at least in the crash years. Because most experiments were short lived, they could A second study concerned the effects of parasitic Brown- not be expected to show long-term effects nor whether headed Cowbirds Molothrus ater on the rare Kirtland’s War- breeding numbers increased to the maximum level possible. bler Dendroica kirtlandii, now restricted to a small area of Nor could they show whether predation regulated, rather Michigan (Rye1 1981, Mayfield 1983, Probst 1986, Weinrich than merely limited, prey population density. If the exper- 1988). A marked decline in warbler numbers between the iments had been continued longer, it is theoretically possible 1960s and 1970s coincided with a period of heavy cowbird that the prey may have increased to the point at which parasitism, when warbler breeding success was reduced to predators could no longer reduce their numbers to former less than one young per nest. Following a period of cowbird levels (the predator pit hypothesis). This was the outcome removal, warbler breeding success increased three-fold and of a predator-removal study on rabbits, providing evidence the decline in breeding numbers stopped. However, the war- for the existence of two equilibrium densities in the presence bler breeding population did not recover to its former levels. of predators (Pech et al. 1992). It is also possible that, if So while cowbird parasitism clearly affected warbler nest habitat quality (food and cover) had been changed instead success, it remained uncertain whether it also affected of predator numbers, a bigger and more lasting rise in den- breeding numbers. Indeed, other factors were suggested sity might have occurred. (Mayfield 1983). So this particular experiment was incon- clusive 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. EXPERIMENTS INVOLVING PARASITES AND PATHOGENS Empirical and modelling studies have suggested that para- sites could have the same effects on host populations as DISCUSSION predators have on their prey, leading to either (1) no obvious reduction in breeding density, (2) an equilibrium level lower The experiments discussed above are summarized in Table than resources would permit, (3) marked fluctuations in 5. Many were simple before-and-after studies, but 27% in- abundance or (4) decline to extinction. Natural experiments, cluded a control area, and another 27% also involved re- involving the accidental introduction of a disease or disease versal of treatments or replication. Despite their various de- vector to a new area, have occurred from time to time, signs, field experiments have served to confirm that, within sometimes with devastating effects on the local avifauna, areas of suitable habitat, the main potential limiting fac- 408 I. NEWTON IBIS 136 tors-whether resources or natural enemies-have affected of breeding, consisting of breeders and nonbreeders. The the breeding density of one bird species or another. They main practical problem in most bird species is that, in con- also have confirmed that the same species can be limited in trast to breeders, nonbreeders are often nonterritorial and breeding density by different factors in different areas or in inconspicuous or flocking and range over much larger areas different years. The provision of food or removal of predators than breeders. This behaviour makes them hard to count Icd in extreme cases to a doubling of breeding densities com- accurately and to keep track of during experiments. How- pared with control areas, but provision of nestboxes often ever, whatever limits the numbers of breeders in a popu- led to much bigger increases-5-20-fold in the most ex- lation must also indirectly set a ceiling on the numbers of treme cases. nonbreeders. Thus, once all available breeding habitat is An obvious drawback of experiments is that they are pos- occupied, with no room for further settlers, an upper limit sible only on certain species which have food supplies, nest is set on both the number of breeders and the annual output sites. predators or parasites that lend themselves to manip- of young. In due course, this must eventually limit the num- ulation, are common enough for experiment and remain in bers of nonbreeders, which can increase only up to the point the same area long enough to assess the effect of the ma- where the annual additions (from reproduction and exit from nipulation. For each of the species studied, experiments were the breeding sector) match the annual losses (from mortality done on whatever limiting factor previous observation had and entry to the breeding sector). The numbers of nonbreed- suggested might have been important in the area concerned. ers would then stabilize at that level (Newton 1992). The As a sample, then, the experiments which have been made theoretical maximum ratio of nonbreeders to breeders was were predisposed to give positive results, and they could give calculated by Brown (1969) for a range of bird species with no indication of what would be the effect of manipulating different reproductive and mortality rates. In the most ex- some quite different factor in the species concerned (such treme examples, nonbreeders could outnumber breeders. as predation where breeding density appeared to be limited The existence of a theoretical maximum for the numbers of by nest sites). If species for each type of experiment had been nonbreeders (set by the numbers of breeders) does not of selected from the available avifauna at random, rather than course exclude the possibility that environmental con- 011 the basis of prior knowledge, the number of positive straints might restrict their numbers below this level. The results would probably be much less than the 77% recorded important point, however, is that whatever limits the breed- for the experiments reported here. In addition, all experi- ing numbers of a species can also influence the total spring ments so far have examined particular limiting factors in- population of breeders and nonbreeders, either directly or dividually. None has explored the possible interactions be- indirectly. tween different limiting factors, such as parasitism and food shortage; this is an obvious opening for future work. I am grateful to Professor D. Jenkins for helpful discussion over many Because of thc small areas amenable to experiment, the years and for critical comments on this manuscript. 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 ex- REFERENCES ample. if some local treatment had caused more birds to survive than could be accommodated in local nesting hab- Angelstam. P.. Lindstrom. E.C. &Widen, P. 1984. Role of predation itat, this could (through emigration) have led to increased in short-term population fluctuations of some birds and mammals breeding densities over areas larger than the study site. Con- in Fennoscandia. Oecologia 62: 199-208. versely, if the treatment had favoured immigration, densities Atkinson. I.A.E. 1985. The spread of commensal species of Rattus in surrounding areas might have been unaffected or de- to oceanic islands and their effects on island avifaunas. ICBP Tech. Bull. 3: 35-81. prcsscd as a result of thc experiment. Ralser. D.J.. Dill. H.H. & Nelson, H.K. 1968. Effect of predator The evidence provided by experiments is as good as we reduction on waterfowl nesting success. J. Wildl. Mgmt 32: 669- are likely to get, but even when a positive result was ob- 682. tained. there is still the possibility that some unknown lim- Reasom, S.L. 1974. Intensive short-term predator removals as a iting factor changed in parallel to the one studied and caused game managemcnt tool. Trans. North Am. Wildl. Nat. Resour. thc change in numbers. And even where change in some Conf. 39: 230-240. particular factor did change numbers, it is not safe, of course, Beissinger. S.R. & Bucher, E.H. 1992. Sustainable harvesting of lime that all changes in numbers were due to this same parrots for conservation. In Beissinger. S.R. & Snyder, N.F.R. (eds) factor. A given factor may be sufficient for some changes New World Parrots in Crisis: 73-115. Washington, D.C.: Smith- but not nccessary to explain them all. Despite these caveats, soriian Institution Press. Berndt. R. & Frantzen. M. 1964. Vom Einfluss des strengen Winters cxperiments are an improvement over observing natural 1962/63 auf den Bruthestand der Kohlenbriiter bei Braun- changes because in experiments it is the observer who brings schweig. Om. Mitt. 16: 126-130. a bout the change. Blankinship. D.R. 1966. The relationship of White-winged Dove Experiments on the limitation of breeding density reveal production to control of Great-tailed Grackles in the lower Rio little about the limitation of numbers at other times of year Grande Valley of Texas. Trans. North Am. Wildl. Nat. Resour. or about the limitation of total population size at the start Conf. 31: 45-58. 1994 LIMITATION OF BIRD BREEDING DENSITIES 409

Boyd, A.W. 1932. Notes on the Tree Sparrow. Br. Buds 25: 278- Duebbert, H.F. & Kantrud, H.A. 1974. Upland duck nesting related 285. to land use and predator reduction. J. Wildl. Mgmt 38: 257-265. Brawn, J.D. & Balda, R.P. 1988. Population biology of cavity- Duebbert. H.F. & Lokemoen. J.T. 1980. High duck nesting success nesters in northern Arizona: Do nest sites limit breeding densities? in a predator-reduced environment. J. Wildl. Mgmt 44: 428-437. Condor 90 61-71. East, M.L. & Perrins. C.M. 1988. The effect ofnest-boxes on breed- Brown, C.R. & Brown, M.R. 1986. Ectoparasitism as a cost of ing populations of birds in broadleaved temperate woodlands. Ibis coloniality in CliffSwallows (Hirundopyrrhonata). Ecology 67: 1206- 130: 393-401. 1218. Enemar. A.B. & Sjostrand, B. 1972. Effects of the introduction of Brown, J.L. 1969. Territorial behaviour and population regulation Pied Flycatchers Ficedula hypoleuca on the composition of a pas- in birds. Wilson Bull. 81: 293-329. serine bird community. Ornis Scand. 3: 79-87. Brush, T. 1983. Cavity use by secondary cavity-nesting birds and Enoksson. B. & Nilsson, S.G. 1983. Territory size and population response to manipulations. Condor 85: 461466. density in relation to food supply in the Nuthatch Sitta europaea. Bump, G.. Darrow. R.W.. Edminster. F.G. & Crissey. W.F. 1947. J. Anim. Ecol. 52: 927-935. The Ruffed Grouse. New York: Authority of the New York State Eriksson, M.O.G. 1982. Differences between old and newly estab- Legislature. lished Goldeneye (Bucephala clangula) populations. Ornis Fenn. 59: Cave. A.J. 1968. The breeding of the Kestrel, Falco tinnunculus L., 13-19. in the reclaimed area Oostelijk Flevoland. Neth. J. Zool. 18: 313- Errington, P.L. 1946. Predation and vertebrate populations. Quart. 407. Rev. Biol. 21: 144-177, 221-245. Chapman, B.R. & George, J.E. 1991. The effects of ectoparasites Franzblau. M.A. & Collins, J.P. 1980. Test of a hypothesis of ter- on Cliff swallow growth and survival. In Loye, J.E. & Zuk, M. (eds) ritory regulation in an insectivorous bird by experimentally in- Bird-parasite Interactions: 69-92. Oxford Oxford University Press. creasing prey abundance. Oecologia 46: 164-1 70. Chesness, R.A.. Nelson, M.M. & Longley. W.H. 1968. The effect Gauhl, F. 1984. Ein Beitrage zur Bruthiologie des Feldsperlings of predator control on Pheasant reproductive success. J. Wildl. (Passer montanus). Vogelwelt 105: 176-187. Mgmt. 32: 683-697. Gauthier. G. & Smith, J.N.M. 1987. Territorial behaviour. nest-site Coleman, J.D. 1974. The use of artificial nest sites erected for availability, and breeding density in Buffleheads. J. Anim. Ecol. Starlings in Canterbury. New Zealand. N.Z. J. Zool. 1: 349-354. 56: 171-184. Cooper, R.J.. Dodge, K.M., Martinat, P.J.. Donahoe. S.B. & Whit- Greenwood. R.]. 1986. Influence of Striped Skunk removal on more, R.C. 1990. Effect of diflubenzuron application on eastern upland duck nest success in North Dakota. Wildl. SOC.Bull. 14: deciduous forest birds. J. Wildl. Mgmt 54: 486-493. 6-11. Crawford, R.J.M. & Shelton, P.A. 1978. Pelagic fish and seabird Gustafsson. L. 1988. Inter- and intraspecific competition for nest- inter-relationships off the coasts of South West and South Africa. holes in a population of the Collared Flycatcher Ficedula albicollis. Biol. Conserv. 14: 85-109. Ibis 130 11-16. Creutz. G. 1949. Untersuchungen zur Brutbiologie des Feldsper- Haartman, L. von. 1971. Population dynamics. In Farner. D.S. & lings (Passer m. rnontanus L.). 2001. Jahrb. 78: 133-172. King, J.R. (eds) Avian Biology, Vol. 1: 391-459. : Academic Crissey. W.F. & Darrow, R.W. 1949. A study of predator control Press. on Valcour Island. Res. Ser. No. 1. Albany, N.Y.: New York State Haartman. L. von. 1973. Talgmespopulationen Lemsjoholm. Lin- Conservation Department, Division of Fish and Game. tumies 8: 7-9. Currie. F.A. & Bamford. R. 1982. Songbird nest-box studies in Hamerstrom, F.. Hamerstrom. F.N. & Hart, J. 1973. Nest boxes: forests in north . Q. J. For. 76: 250-255. An effective management tool for Kestrels. J. Wildl. Mgmt 37: Cutforth. B. 1968. Eighth annual report of the Brandon Juniors 400-403. nest box project, 1968. Blue Jay 20 188. Haramis. G.M. & Thompson, D.Q. 1985. Density-production char- Dahlsten, D.C. & Copper. W.A. 1979. The use of nesting boxes to acteristics of box-nesting Wood Ducks in a northern greentree study the biology of the Mountain Chickadee (Parus gambeli) and impoundment. J. Wildl. Mgmt 49: 429-436. the impact on selected forest insects. In Dickson, J.G.. Conner. Higuchi, H. 1978. Use of nest-boxes by birds according to forest R.N., Fleet, R.R., Kroll. J.C. & Jackson, ].A. (eds) The Role of types and the breeding density in forests with and without nest- Insectivorous Birds in Forest Ecosystems: 217-260. London: Ac- boxes. J. Jpn. For. SOC.60 255-261. ademic Press. Holroyd. G.L. 1975. Nest-site availability as a factor limiting pop- Davies. N.B. 1978. Ecological questions about territorial behav- ulation size of swallows. Can. Field-Nat. 89: 60-64. iour. In Krebs, J.R.& Davies. N.B. (eds) Ekhavioural Ecology. An Hudson, P.J. 1986. The effect of a parasitic nematode on the breed- evolutionary approach: 317-350. Oxford: Blackwell Scientific ing production of Red Grouse. J. Anim. Ecol. 55: 85-92. Publications. Hudson, P.J. & Dobson, A.P. 1990. The control of parasites in Dennis. R.H. & Dow. H. 1984. The establishment of a population natural animal populations: Nematode and virus infections of Red of Goldeneyes (Bucephala clangula) breeding in Scotland. Bud Study Grouse. In Perrins. C.M.. Lebreton, J-D. & Hirons, G.J.M. (eds) 31: 217-222. Bird Population Studies: Their relevance to conservation and DeReede, R.H. 1982. A field study on the possible impact of the management: 413-432. Oxford: Oxford University Press. insecticide diflubenzuron on insectivorous buds. Agro-Ecosys- Jansson. C.. Ekman. J. & Briimssen. A. von. 1981. Winter mortality tems 7: 327-342. and food supply in tits (Parus spp.). Oikos 37: 313-322. Dhondt. A.A. & Eyckerman. R. 1980. Competition between the Jarvinen. A. 1978. Nest-box studies in mountain birch forest at Great Tit and the Blue Tit outside the breeding season in field Kilpisjarvi. Finnish Lapland. Anser (Suppl. 3): 107-11 1. experiments. Ecology 61: 1291-1296. Johnson, L.L. 1967. The Common Goldeneye Duck and the role Dornbusch. M. 1973. Zur Siedlungsdichte und Ernarung des of nesting boxes in its management in north central Minnesota. Feldsperlings in Kiefern-Dickungen. Der Falke 20: 193-195. J. Minnesota Acad. Sci. 34: 110-1 13. 4 1 0 I. NEWTON lBIS 136

Jones. R.E. & Leopold. AS. 1967. Nesting interference in a dense Potts. G.R. 1980. The effects of modern agriculture, nest predation population of Wood Ducks. J. Wildl. Mgmt 31: 221-228. and game management on the population ecology of partridges Kallander, H. 1981. The effects of provision of food in winter on Prrdix prrdix and Alectoris ruJa. Adv. Ecol. Res. 11: 1-79. a population of the Great Tit Parus major and the Blue tit P. caerule- Probst, J.R. 1986. A review of factors limiting Kirtland's Warbler 11s. Ornis Scand. 12: 244-248. on its breeding grounds. Am. Nat. 117: 87-100. Keith. I,.B. 1963. Wildlife's Ten-year Cycle. Madison, Wis.: Uni- Raphael, M.G. & White, M. 1984. 1Jse of snags by cavity-nesting versity of Wisconsin Press. birds in the Sierra Nevada. Wildl. Monogr. 86: 1-66. Keith, L.R. & Rusch. D.H. 1988. Predation's role in the cyclic Richmond, M.L., Henny, C.J.. Floyd. R.L.. Mannan. R.W.. Finch, fluctuations of RuHed Grouse. Proc. Int. Om. Congr. XIX: 699- D.M. & DeWeese, L.R. 1979. Effects of sevin-4-oil. dimilin and 732. orthene on forest birds in northeastern Oregon. US. For. Serv. Kissam. J.B.. Noblet, K.E. & Garris. G.1. 1975. Large scale aerial Res. Pap. PSCO-148. treatment of an endemic area with abate granular larvicide to Ryel, LA. 1981. Population change in the Kirtland's Warbler. control black flies (Diptera: Simulidae) and suppress Leucoc!jtozoon Jack-pine Warbler 59: 76-91. srnithi of turkeys. 1. Med. Entomol. 12: 359-362. Samson. F.R. & Lewis, J.]. 1979. Experiments on population reg- Krcbs, J.K. 1971. Territory and breeding density in the Great Tit, ulation in two North American parids. Wilson Bull. 91: 222-233. l'urus major L. Ecology 52: 2-22. Savard, J.L. 1988. Use of nest boxes by Barrow's Goldeneyes: Nest- lack. D. 1954. 'The Natural Kegulation of Animal Numbers. Ox- ing success and effect on the breeding population. Wildl. Soc. Bull. ford: Oxlord University Press. 16: 125-1 32. Lynch. G.M. 1972. Effect of strychnine control on nest predators Schrank. B.W. 1972. Waterfowl nest cover and some predation of dabbling ducks. J. Wildl. Mgmt 36: 436-440. relationships. J. Wildl. Mgmt 36: 182-186. Marcstriim. V., Kenward. R.E. & Engren, E. 1988. The impact of Sih. A., Crowley. P.. McPeek, M.. Petranka. J. & Stohmeier. K. 1985. predation on boreal tetraonids during vole cycles: An experimen- Predation, competition, and prey communities: A review of field La1 study. J. Anirn. Ecol. 57: 859-872. experiments. Ann. Rev. Ecol. Syst. 16: 269-311. Ilarjakangas, A. 1987. Does the provision of extra food in winter Siren. M. 1951. Increasing the Goldeneye population with nest- affect the abundance of Finnish Black Grouse? In Hudson, P. & boxes. Suomen Riista 6: 189-190. Lovel, T. (eds) Fourth International Grouse Symposium: Paper Smith, J.N.M., Montgomerie. R.D.. Taitt. M.J. & Yom-Tov. Y. 19F3. No. 20. West Germany: World Pheasant Association. A winter feeding experiment on an island Song Sparrow popu- Mayfield, H.F. 1983. Kirtland's Warbler, victim of its own rarity? lation. Oecologia 47: 164-170. Auk 100: 974-976. Spray, C.J., Crick, H.Q.P. & Hart, A.D.M. 1987. EHects of aerial Mc1,aughliri. C.L. & Grice. D. 195.2. The effectiveness of large-scale applications of fenitrothion on bird populations of a Scottish Pine erection of Wood Duck boxes as a management procedure. Trans. plantation. 1. Appl. Ecol. 24 29-47. Worth Am. Wildl. Natur. Resour. Conf. 17: 242-259. Stribling, H.L. & Smith, H.R. 1987. Efkcts of dimilin on diversity Miller. G.R., Watson. A. & Jenkins. D. 1970. Responses of Red and abundance of forest birds. North 1. Appl. For. 4: 37-38. Grouse populations to experimental improvement in their food. Tapper, S.C., Rrockless, M. & Potts. C.R. 1991. The Salisbury Plain In Watson. A. (ed.) Animal Populations in Relation to Their Food experiment: The conclusion. The Game Conservancy Review of Rcsourccs: 323-3 35. Oxford: Blackwell. 1990: 87-91. M01ler, A.P. 1990. Effects of parasitism by a haematophagous mite Tapper. S.C.. Potts. G.K.. Reynolds. J., Stoate, C. & Rrockless. M. on reproduction In the Rarn Swallow Hirundo rustica. Ecology 71: 1990. Salisbury Plain experiment-Year six. The Game Conscr- 2345--2%57. vancy Annual Review of 1989: 42-49. Ucwton, 1. 1979. Population Ecology of Raptors. Berkhamsted: 'I'rautman, C.G.. Fredrtckson. L.F. & Carter. A.V. 1974. Kelation- Poyser. ship of Red Foxes and other predators to populations of Ring- Sewton. I. 1980. The role of food in limiting bird numbers. Ardea necked Pheasants and other prey, South Dakota. Trans. North 68: 11-30. Am. Wildl. Nat. Res. Conf. 39: 241-255. Newton. I. 1992. Experiments on the limitation of bird numbers van Balen. J.H. 1980. Population fluctuations of the Great Tit and by territorial behaviour. Biol. Rev. 67: 129-173. feeding conditions in winter. Ardea 68: 143-164. Newton. I. 1993. Predation and limitation of bird numbers. Cur- van Balen. J.H.. Booy. C.J.H.. van Franeker, J.A. & Osieck, E.R. rent Ornith. 11: 143-198. 1982. Studies on hole nesting birds in natural nest sites. 1. Avail- Parker, H. 1984. Effect of corvid removal on reproduction of Wil- ability and occupation of natural nest sites. Ardea 70: 1-24. low Ptarmigan and Black Grouse. J. Wildl. Mgmt 48: 1197-1205. van Riper, C., van Riper, S.G.. Coff. M.G. & Laird, M. 1986. The Prakall. D.R. & Bart. J.R. 1983. Impacts of aerial application of epizootiology and ecological significance of malaria in Hawaiian insecticides on forest birds. CBC Critical Reviews in Environmental land birds. Ecol. Monogr. 56: 327-344. Control 13: 117-165. Village, A. 1983. The role of nest-site availability and territorial t'earce. P.A. & Peakall, D.B. 1977. The impact of fenitrothion on behaviour in limiting the breeding density of Kestrels. J. Anim. bird populations in New Rrunswick. In Roberts, J.R.. Greenhalgh. Ecol. 52: 635-645. R. & Marshall, W.K. (eds) Fenitrothion: The long-term effects of Village, A. 1990. The Kestrel. Calton: Poyser. its use in forest ecosystems-Current status: 199-306. Publ. No. Warner. R.E. 1968. The role of introduced diseases in the extinc- 1 5 389. Ottawa: National Research Council of Canada. tion of the endemic Hawaiian avifauna. Condor 70: 101-120. I'rch, R.P., Sinclair. A.R.E.. Newsome. A.E. & Catling. P.C. 1992. Waters, J.R.. Noon, B.R. & Verncr. J. 1990. Lack of nest site lim- Limits to predator regulation of rabbits in Australia: Evidence from itation in a cavity-nesting bird community. J. Wildl. Mgmt 54: predator-removal experiments. Oecologia 89: 102-112. 239-245. 1994 LIMITATION OF BIRD BREEDING DENSITIES 41 1

Watson, A. &Moss, R. 1979. Population cycles in the Tetraonidae. (Tetrao tetrix L.) population. Published doctoral thesis, Uppsala Ornis Fenn. 56: 87-109. University. Weinrich, J.A. 1988. Status of Kirtlands Warbler 1987. Jack-pine Yom-Tov, Y. 1974. The effect of food and predation on breeding Warbler 66: 155-158. density and success, clutch size and laying date of the Crow (Corvus Willebrand. T. 1988. Demography and ecology of a Black Grouse corone). J. Anim. Ecol. 43: 479498.