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Density-dependent mortality arising directly or indirectly through starvation can be caused by two kinds of competition. In exploitation competition, the food supply is increasingly depleted as the number of competitors increases so that an increasing proportion of poor competitors cannot feed fast enough to survive. In interference competition, an increasing proportion starves because intensifying interference reduces the intake rate of an increasing proportion of poor competitors, even if the food supplies remain abundant. These two mechanisms are not incompatible but it is difficult in empirical studies to quantify their separate contribution to the starvation of poor competitors. Yet we seem to suppose that, in vertebrates, food depletion is usually a necessary condition for density-dependent starvation to occur (Sinclair 1989). This paper describes a case in which density-dependent starvation arises without food depletion having a significant effect on intake rate. Rather, field and modelling studies show that it occurs because intensifying interference as competitor densities rise causes more poor competitors to starve.
The study was on overwintering oystercatchers Haematopus ostralegus L. on the Exe estuary, UK, where the main prey are mussels Mytilus edulis L. supplemented by other bivalve molluscs, Cerastoderma edule L. and Scrobicularia plana da Costa, and by earthworms Lumbricidae over high water. Most oystercatchers arrive in September and remain until spring, when they leave to breed. Most birds that disappear in winter appear to have starved, especially in severe weather when increased bird energy demands coincide with reduced prey availability and quality (Goss-Custard et al. 1996). Over 15 study winters, oystercatcher numbers on the 10 main mussel beds varied between 1181 and 1883 and mortality from starvation was density-dependent (Durell et al. 2000), with above-trend rates occurring in unusually cold and/or windy winters (Durell et al. 2001).
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Exe oystercatchers removed by spring 12% of > 30-mm mussels present in autumn, but up to 25% of the most preferred large mussels, a rate similar to that in the Oosterschelde (Meire 1996). However, their functional responses were flat across a wide range of prey biomass density, and depletion had little effect on intake rate. However, model results showed that this conclusion only applies at present-day population sizes. Exploitation competition would begin to affect intake rate at two–three times present population levels. The greater depletion rates would then approach the average of 50% (SD = 19·3) found by Dolman & Sutherland (1997) across 24 vertebrates, although whether rates in that sample are typical of vertebrates, or only of cases where depletion was considered large enough to study, is unclear.
Depletion did reduce the mean length of mussels but the effect on intake rate would have been so small (< 3%) that the birds would probably not have detected any decrease (Stillman et al. 2000). Nor is there any evidence that depletion much affected the mean shell thickness of mussels, confirming Meire’s (1996) finding for Oosterschelde ventral hammerers. While many more exclosures might have detected the small net increase in shell thickness (1–3·5%) expected from depletion, the very large samples of autumn–spring comparisons from all mussel beds over 8 years provided no evidence of this. If depletion did cause mussel shells on the main feeding areas to be thicker by the winter’s end, it was undetectably small.
The expectation that the shells of surviving mussels would thicken as oystercatchers removed the thin-shelled ones was based on the assumption that shell thickness does not change from autumn to spring. This assumption may be false because recent data indicate that the shell thickness of individual mussels does vary during winter (R. Nagarajan, unpublished information). In response, hammering oystercatchers take thicker-shelled mussels when these predominate and thinner-shelled ones when they are abundant (R. Nagarajan, unpublished information), as do captive oystercatchers (Sutherland & Ens 1987). Present evidence therefore suggests that, within limits, hammerers raise or lower the threshold thickness of the shells they attack according to what is on offer, although presumably with consequences for the risk of bill breakage and energetic costs (Meire 1996). But at present population sizes, there is no evidence that depletion affected intake rate in hammering oystercatchers by changing shell thickness. The similarity in the overwinter change in intake rate in hammerers and in stabbing birds, which select mussels independently of shell thickness (Durell & Goss-Custard 1984), is consistent with this conclusion.
Rather, intake rates decreased because the flesh content of individual mussels declined by 40–50%. Model simulations showed that, without this, mortality rates would have been much lower, although still density-dependent. As mussels lose flesh over the winter because of reduced phytoplankton food supply (Bayne & Worrall 1960), the rate of decline in mussel flesh content, and thus in oystercatcher intake rate, was presumably independent of bird density.
It is nonetheless surprising that intake rate did decline over the winter because birds did appear to have spare foraging time in which to raise their intake rates. Across all sites and independently of the stage in the winter, stabbing and hammering oystercatchers spent only 56·3% (SE = 2·2) and 67·4% (SE = 2·2), respectively, of their foraging time ‘handling’ mussels (i.e. pecking at and attacking mussels, either successfully or unsuccessfully). The remaining time was spent walking with head aloft, the birds apparently searching visually for prey to attack. Contrary to the assumption made in the ‘disc’ equation for the type II functional response (Holling 1959), the asymptotes were clearly not limited by all the foraging time being used in handling mussels, a conclusion also reached for a captive oystercatcher eating Scrobicularia (Wanink & Zwarts 1985). Holling (1959) recognized that factors other than handling time can determine the asymptote, one alternative being a digestive constraint. But although gut processing rate in oystercatchers does limit consumption over a tidal cycle (Kersten & Visser 1996), it is most unlikely to have limited the instantaneous intake rate over the 5-min observation periods. First, oystercatchers eating shellfish elsewhere have intake rates up to twice those on the Exe (Zwarts et al. 1996; Norris & Johnstone 1998). Secondly, Exe oystercatchers did not increase their volumetric intake rates by the end of winter, despite the rates then being considerably below autumn rates; they could presumably have ingested flesh at a higher rate in spring, but did not do so. Thirdly, the consistently lower asymptote in stabbing birds compared with hammerers implies that gut constraints did not limit their intake rate at most stages of the winter.
The factors determining the functional response asymptote in Exe oystercatchers remain to be discovered, as in some other birds (Caldow & Furness 2001). One possibility is that oystercatchers may have traded-off the risks of ingesting parasites against the energetic gains of increasing their intake rate, as argued for oystercatchers selecting cockles of different sizes (Norris & Johnstone 1998). Thus, if the numbers of parasites per mussel remained constant, or even increased, over the winter as the flesh content declined, oystercatchers may have become increasingly selective against the increasing density of parasites in the flesh, and thus rejected an increasing proportion of mussels. However, this is unlikely as the probability of an Exe oystercatcher rejecting an encountered mussel (as defined in Stillman et al. 2000) did not increase over the winter (J.D. Goss-Custard, unpublished information), as would be expected if they had become increasingly selective. Furthermore, the low intake rate on mussel beds in late winter caused large numbers to eat earthworms Lumbricidae above high water (Caldow et al. 1999), where their chance of ingesting damaging nematode worms was probably high (Goss-Custard et al. 1996). Restraining intake rate over low water would merely have resulted in increased exposure to risk of infection from other parasites at high water. As an alternative speculation, we propose a hidden component of searching that adds a time expenditure, x, to every mussel that is attacked, so that the asymptote was limited not by handling time alone but by handling time + x. Research is now testing this hypothesis.
Our interpretation of how density-dependent starvation occurred in mussel-eating Exe oystercatchers is as follows. As population density increased, average intake rate was reduced through increased rates of interference, this leading to starvation towards the end of winter when the mussel condition was poor. However, it was not just the subdominant birds that were most susceptible to interference that starved, but the least efficient ones as well. A bird of low efficiency, by definition, had a relatively low intake rate even when competitors were scarce. They therefore started from a low base, especially towards the end of winter after the mussels had lost nearly half their flesh. Interference reduced the intake rate of the most susceptible animals at a proportionate rate as competitor density increased (Stillman et al. 1996). Thus, with two competitors of equal susceptibility to interference but differing foraging efficiency, the less efficient one starved first as population density increased, even though the density dependence was due almost entirely to interference rather than to exploitation competition.