IBIS 136: 397-41 1 ~ 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 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.