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Abstract

  1. Top of page
  2. Abstract
  3. Evidence for predation effects
  4. Evidence for habitat effects
  5. INTERACTION MECHANISMS
  6. DISCUSSION
  7. Acknowledgments
  8. REFERENCES

Population declines are often attributed to either habitat change or increased predation rates, without a full consideration of the potential for these two factors to interact. This may lead to an inaccurate diagnosis of the causes of population decline and thus the selection of inappropriate management solutions. Here mechanisms through which habitat change and predation could interact are reviewed. Examples of how these may have contributed to population declines are provided, focusing on European farmland birds. However, very few appropriate studies have been conducted that allow the role of such interactions to be assessed accurately. To remedy this situation experimental designs that could detect the presence of interactive mechanisms are described. When habitat change and predation interact, conservation managers are provided with the opportunity to control predation impacts through habitat management rather than predator removal, which may provide a more cost-effective management strategy.

Populations of many farmland bird species have declined in Britain and throughout north-west Europe in recent decades (Tucker & Heath 1994, Krebs et al. 1999, Donald et al. 2001). Despite an earlier suggestion that environmental change may have increased predator impacts (Reynolds & Tapper 1996), studies of these declines have focused on either habitat change or increased predation rates as causal factors. The question of whether predation rates may have increased as a result of habitat change, i.e. the presence of interactions between predation impact and habitat change, is rarely addressed. This paper provides the first comprehensive review of the mechanisms through which habitat change and predation impact may interact and outlines experimental designs to test for the presence of such interactions. Whilst the review is written mainly from the perspective of European farmland bird conservation, the principles are relevant to any study investigating population declines for which both predation and habitat change are plausible causal factors.

Evidence for predation effects

  1. Top of page
  2. Abstract
  3. Evidence for predation effects
  4. Evidence for habitat effects
  5. INTERACTION MECHANISMS
  6. DISCUSSION
  7. Acknowledgments
  8. REFERENCES

Many avian predators of farmland birds (e.g. corvids, Northern Goshawk Accipiter gentilis, Common Buzzard Buteo buteo, Eurasian Sparrowhawk Accipiter nisus) have increased during the period of population declines (Marchant et al. 1990, Baillie et al. 2002). The same probably applies to most mammalian predators (e.g. Badgers Meles meles, Red Fox Vulpes vulpes, Weasel Mustela nivalis, Stoat Mustela ermina, American Mink Mustela vison, Rat species Rattus spp., Grey Squirrel Sciurus carolinensis and Hedgehog Erinaceus europaeus). However, except that for Badgers, much of the evidence that these predators have increased is either circumstantial or based on bag records; these may be unreliable and some data suggest that Weasels and Stoats are declining (Yalden 1992, 1999, Harris et al. 1995, Reynolds & Tapper 1995, Wilson et al. 1997a, MacDonald & Harris 1999, Macdonald & Tattersall 2002). All of these predators are generalists (Cramp 1980, Corbet & Harris 1991, Cramp & Perrins 1994), and thus predation rates on a particular species are likely to be independent of prey density and could thus cause population declines.

The best evidence that predators can regulate farmland bird populations is provided by Tapper et al. (1996). Through a predator control experiment, with treatment reversal, they showed that the Grey Partridge's Perdix perdix population density and breeding success were reduced by the combined effects of predation by Red Foxes, Weasels, Stoats, Brown Rat Rattus norvegicus, Black-billed Magpies Pica pica and Carrion Crows Corvus corone. Other studies provide some evidence that predation may have contributed to farmland bird declines. Corvid density is positively correlated with nest failure rates of Common Blackbirds Turdus merula and Song Thrushes Turdus philomelos (Paradis et al. 2000); however, corvid density may be confounded with habitat type, and the pattern of nest failure rates may be explained by variation in habitat type. Stoate and Szczur (2001) show that increased breeding success and population density of Song Thrush and Common Blackbird were associated with predator control (of Magpies, Carrion Crows, Red Foxes, Brown Rats, Weasels and Stoats). However, because habitat management occurred simultaneously, the causal link was unproven. Outside the context of farmland bird declines there is good evidence that predation has contributed to population declines of Red Grouse Lagopus lagopus (Thirgood et al. 2000), Golden Plover Pluvialis apricaria (Parr 1992) and Eurasian Curlew Numenius arquata (Grant et al. 1999).

Reviews of predator control experiments, across a range of habitats, draw different conclusions. Newton (1998) found that in 23 out of 27 experiments nest success increased, in 12 out of 17 experiments this caused increased post-breeding numbers and in 10 out of these 17 experiments this led to increased breeding numbers. By contrast, Cote and Sutherland (1997) argued that although there is good evidence that predation control increases autumn population sizes, through increased nest success, the evidence that this translates into increased breeding densities is much less consistent.

In combination, the reviews suggest that nest predation rates can have a large effect on population dynamics. However, most of the studies focused on ground-nesting gamebird or duck populations and the evidence that nest predation can reduce passerine populations is much weaker. Indeed, the decline in UK bunting populations is not associated with increased nest-predation rates (Crick et al. 1994) and songbird population trends are not correlated with the densities of either Sparrowhawks or Magpies (Thomson et al. 1998). However, such studies may underestimate the effect of predation as predator behaviour may weaken any positive correlation between predator density and predation impact. For example, if predation on birds is opportunistic (i.e. the result of fortuitous encounters with unexpected prey items, whilst looking for the main prey item) then predation rates on the secondary prey item are positively correlated with the density of the predators’ primary food item and may thus be unrelated to predator densities (Vickery et al. 1992, Yanes & Suarez 1996, Schmidt et al. 2001). The essential point is that evidence suggests that predation can have a role in bird population declines.

Evidence for habitat effects

  1. Top of page
  2. Abstract
  3. Evidence for predation effects
  4. Evidence for habitat effects
  5. INTERACTION MECHANISMS
  6. DISCUSSION
  7. Acknowledgments
  8. REFERENCES

In recent years, numerous studies have identified habitat loss as a causal factor in farmland bird population declines (see Table 1). However, it has been demonstrated that habitat loss could fully explain the observed population decline in only one species, the Corncrake Crex crex (Green et al. 1997). Therefore, it is plausible that predation has contributed to the declines of many farmland bird species, perhaps because anthropogenic alterations to the farmland ecosystem have created an environment in which population dynamics are more sensitive to predation, i.e. habitat change may interact with predation rates. Mechanisms through which such interactions may arise were identified by searching the literature and are discussed below.

Table 1.  Examples of how habitat changes have reduced farmland bird populations.
Habitat changeCausal mechanismSpeciesSource
Loss of winter stubblesReduces food supply and thus survival ratesCorn Bunting Miliaria calandra Cirl Bunting Emberiza cirlusDonald and Forrest (1995) Evans and Smith (1994)
Switch from spring to winter sown cerealsReduces availability of summer food and nest-sitesSkylark Alauda arvensisWilson et al. (1997b)
Pesticide applicationsReduces food abundance and thus breeding success, through reduced chick survivalGrey Partridge Perdix perdixPotts (1986)
Polarization (concentration of arable land in eastern UK and pasture in western UK)Reduces the availability of high-quality foraging habitat, i.e. pasture, to birds breeding in arable areas resulting in reduced breeding successLapwing Vanellus vanellusHudson et al. (1994)
Increased cutting rates and frequency of crops due to mechanization and fertilizersIncreases adult and chick mortality and destroysnestsCorncrake Crex crexStowe et al. (1993)

INTERACTION MECHANISMS

  1. Top of page
  2. Abstract
  3. Evidence for predation effects
  4. Evidence for habitat effects
  5. INTERACTION MECHANISMS
  6. DISCUSSION
  7. Acknowledgments
  8. REFERENCES

In reviewing the evidence for interactions between habitat change and predation rates it is inappropriate to give equal weight to evidence gained from observational and experimental studies. Conclusions drawn from observational data are usually less certain as confounding factors may influence the results. Therefore, for each cited work, information is provided on the type of study; this is usually provided alongside the reference using the following code: obs – observational data; exp – experimental data; model – theoretical modelling using simulated data.

Environmental change and predator encounter rate

Environmental change may have increased predator densities, leading to an increase in the probability of meeting a predator, i.e. predator encounter rate, and thus predation rates in two ways. First, human control of top-level predators can cause population levels of medium-sized predators and thus overall predation rates to increase; this is termed the meso-predator release effect. Modelling demonstrates that Feral Cat Felis catus control can cause rat densities and predation rates to increase and thus cause extinctions of island bird populations (Courchamp et al. 1999 model). Similarly, control of lynx Lynx populations can increase the predation rates of Egyptian Mongooses Herpestes ichneumon on Rabbits Oryctolagus cuniculus, leading to lowered rabbit densities (Palomares et al. 1995 obs), and Red Fox control may result in higher mustelid densities and predation rates (Bright 2000 review).

Secondly, habitat change may cause an increase in predator numbers. Fuller and Gough (1999) suggested that increased livestock densities may increase alternative food supplies for predators such as Red Fox (increased carrion) and corvids (increased carrion and soil invertebrates) leading to increased predator densities. In France, harrier Circus densities are positively correlated with field size, and thus Grey Partridges (which are limited by harrier predation rates) suffer higher predation rates and occur at lower densities in areas with large fields (Bro et al. 2001 obs). Field size increases during agricultural intensification (Sturrock & Cathie 1980 obs), which thus may have indirectly increased predation rates and contributed to the decline in Grey Partridges. Similarly, in North America human activity has increased densities of jays Cyanocitta, leading to increased nest predation rates (Melampy et al. 1999 obs, de Santo & Willson 2001 obs). Anthropogenic influences may have increased the abundance of introduced predators, although more research is needed. Otter Lutra lutra and American Mink compete (Clode & Macdonald 1995 obs) and thus the decline of the otter population may have facilitated the spread of American Mink. Summer densities of Grey Squirrel populations are correlated with food availability (Gurnell 1996 obs), and thus their unintentional feeding at bird tables may maintain populations at higher densities than would otherwise occur.

Even when predator numbers remain constant, three mechanisms can lead to increased predator encounter rates. First, increased nest densities, e.g. owing to a loss of suitable nest-site habitat, can result in higher predation rates (Potts 1986 obs, Chamberlain et al. 1995 exp, Schmidt 1999 model). Such decoupling of habitat attractiveness from suitability may lead to the development of an ‘ecological trap’ (Misenhelter & Rotenberry 2000 obs). For example, in Spain most farmland birds favour fallow fields for nesting; however, this is a rare habitat type so nest densities in fallow fields are high, attracting predators, and thus exposing nests to very high predation rates (Pescador & Peris 2001 exp). A similar situation occurs in Skylarks Alauda arvensis, which preferentially nest in set-aside fields, but suffer high nest predation rates owing to high nest densities in this habitat type (Donald 1999 obs).

Secondly, habitat change may force birds to nest in more dangerous habitat types. For example, the switch from spring to winter sown cereals has increased sward height and density in spring, reducing the availability of the bare ground on which Skylarks prefer to nest (Wilson et al. 1997b obs). Consequently, more Skylark nests are located along ‘tram-lines’ (linear strips of bare ground created by machinery) but these nests experience higher predation rates, probably because they are easier for visually orientated predators to locate (Donald 1999 obs).

Thirdly, reduction in the availability of alternative food sources may cause generalist predators to change their diets. This hypothesis is supported by Schmidt (1999 model) and numerous field studies. For example, nest predation by Blue Jays Cyanocitta cristata and Racoons Procyon lotor is negatively correlated with cicada Magicicala sp. and mulberry Morus spp. abundance (Schmidt & Whelan 1999a obs). Similarly, Black Grouse Tetrao tetrix nests suffer higher predation rates when voles Microtus are scarce, owing to increased predation by Red Foxes (Angelstam et al. 1984 obs). It is possible that agricultural intensification has caused changes in predator diets and thus contributed to declines in farmland birds. For example, Weasel predation on passerines increases when their preferred prey, voles, are at low density (Dunn 1977 obs). Voles are probably currently declining owing to agricultural change (Harris et al. 1995 review) and thus Weasel predation rates on farmland passerines may have increased.

Increased sensitivity of population dynamics to nest predation

Habitat changes can lead to shortened breeding seasons and thus less opportunity to replace predated nests, thus increasing the sensitivity of breeding success to nest predation rates. The ability of prey to re-nest may have a strong influence on the impacts of predation (Schmidt & Whelan 1999b model, Donovan & Thompson 2001 model). For example, the widespread drying out of lowland wet grasslands in the UK (e.g. Green & Robins 1993 obs) has reduced the number of nesting opportunities for Common Snipe Gallinago gallinago and contributed to a population decline (Green 1988 obs). A similar situation may affect Song Thrushes, as declining populations are associated with more intensively managed land and have fewer nesting attempts than stable populations (Thomson & Cotton 2000 obs), and Skylarks, as the switch from spring to winter sown cereals has shortened their breeding season (Chamberlain et al. 1999 obs).

Increased nest predation rates nest visibility

Increased vegetation density and heterogeneity may reduce nest predation rates as they increase nest crypsis (Newton 1998 review, Willson et al. 2001 review). However, predation rates are not always related to the degree of nest concealment (Howlett & Stutchbury 1996 exp, Burhans & Thompson 1998 obs, Braden 1999 obs). This may occur when predators use non-visual stimuli for nest detection (e.g. Rangen et al. 1999 obs) and/or because a trade-off exists between nest crypsis and the ability of parents at the nest to detect predators and thus take mitigating action (Gotmark et al. 1995 exp, Cresswell 1997 exp, King et al. 1999 exp).

Ground-nesting birds that rely solely on nest crypsis for defence against nest predators may experience increased predation rates owing to habitat change. For example, Sage Grouse Centrocercus urophasianus nest-predation rates are related negatively to the availability of tall grass cover and shrub cover, the removal of which may explain the long-term decline in grouse abundance and productivity (Gregg et al. 1994 obs, de Long et al. 1995 obs). Fuller and Gough (1999) suggested that increasing livestock densities may reduce the availability of nest cover for some species and/or simplify the sward structure, resulting in poorer camouflage. Many ground-nesting farmland birds select sparsely vegetated nest-sites as they can detect predators sooner and reduce predation rates by adopting mitigating action. Examples include Skylark (Wilson et al. 1997b obs), Northern Lapwing (Galbraith 1988 obs) and Stone Curlew Burhinus oedicnemus (Green et al. 2000 obs). All three species have undergone long-term population declines that may be explained partly by increased nest predation rates resulting from agricultural intensification increasing vegetation density.

Many declining farmland birds prefer to nest in hedgerows, e.g. thrushes and Common Linnet Carduelis cannabina, in which vegetation density and heterogeneity have been reduced through changes in hedgerow management (O’Connor & Shrubb 1986 obs, Joyce et al. 1988 obs). This may have increased nest detectability and thus predation rates. Although few studies have investigated this hypothesis, it is supported by Hatchwell et al. (1996 obs) who found that successful Common Blackbird nests were less conspicuous than nests that were predated.

Nest detectability owing to increased begging

Predators also use auditory stimuli, e.g. nestling begging calls, to detect active nests. This creates a positive correlation between begging intensity and predation rates (Redondo & Castro 1992 obs, Haskell 1994 exp, Leech & Leonard 1997 exp, Briskie et al. 1999 obs, Dearborn 1999 exp). Begging intensity is increased by chick hunger and reduced chick condition (e.g. Cotton et al. 1996 exp, Lotem 1998 exp), and begging frequency in the absence of a parent, when predation is more likely, is positively correlated with hunger (Budden & Wright 2001 obs). Therefore, more frequent or more intense food shortages, as a result of habitat change, could increase begging rates and thus nest predation. Whilst the links between hunger, begging intensity and predation are well established, no studies have yet investigated this relationship with respect to agricultural intensification reducing food availability.

Food availability may also be linked to predation rates in precocial species such as gamebirds. Hungry chicks may increase their mobility and thus their visibility to predators, leading to a reduction in survival rates. Survival of Grey Partridge broods is negatively correlated with the distance moved between nocturnal roost sites, which is greater in areas sprayed with pesticides (Rands 1986 exp), which reduces food abundance (Potts 1986 exp). Similarly, the mortality of Common Pheasant Phasianus colchicus chicks increased with the distance moved during the day (Warner 1984 obs). Also, precocial chicks that are weakened by hunger are less likely to respond appropriately to parental alarm calls, leading to increased predation rates (Swennen 1989 obs).

Reduced nest defence

Food shortages may also lead to increased predation rates by altering adult behaviour patterns. Optimal foraging theory suggests that parental foraging distances will increase when food is in short supply (Orians & Pearson 1979). This can lead to parents spending less time nest-guarding and thus increase the vulnerability of nests to predation. Modelling supports this hypothesis (Schmidt 1999 model) and it has been demonstrated by supplementary feeding of Black-billed Magpies (Hogstedt 1981 exp), Carrion Crows (Yom-Tov 1974 exp) and Eurasian Jackdaws Corvus monedula (Soler & Soler 1996 exp). In these studies extra food resulted in parents spending more time near the nest and thus higher breeding success as a result of a reduction in predation rates. In Common Starlings Sturnus vulgaris increased foraging costs, imposed by experimentally manipulating brood size, are associated with parents spending more time away from the nest-site (Wright et al. 1998 exp).

Anthropogenic influences on species interactions may indirectly reduce nest defence and thus increase predation rates. Breeding Lapwings attack and deter predators, thus offering a ‘protective umbrella’ to neighbouring Yellow Wagtails Motacilla flava (Erikson & Gotmark 1982 obs) and other passerines (Elliot 1985 obs). The decline in the Northern Lapwing population, which is partly caused by habitat alteration (Wilson et al. 2001 obs), could have thus contributed to the decline in some farmland bird populations through increased nest predation. In Poland, Common Snipe and Common Redshank Tringa totanus gain from a protective ‘umbrella’ provided by Black-tailed Godwits Limosa limosa (Dyrcz et al. 1981 obs); the extreme rarity of Black-tailed Godwits in the UK, as a result of intensification, may have resulted in Snipe and Redshank experiencing elevated nest predation rates.

Levels of parental nest-defence are positively correlated with female body condition in the Great Skua Catharacta skua (Hamer & Furness 1993 obs), Red Grouse (Martin & Horn 1993 obs) and Fieldfare Turdus pilaris (Hogstad 1993 obs). Habitat changes that cause food shortages and lead to reduced parental body condition may thus indirectly cause increased predation rates as a result of reduced nest defence behaviour. However, parental body condition did not influence nest defence in Great Tits Parus major (Radford & Blakey 2000 obs) and no studies have yet been carried out on farmland birds.

Parental investment theory (Williams 1966) suggests that parents should be less willing to defend broods of low reproductive value, e.g. those with poor body condition. This has been demonstrated in the Willow Tit Parus montanus (Rytkonen et al. 1995 obs) and Pied Flycatcher Ficedula hypoleuca (Listoen et al. 2000 exp), but not the Great Tit (Radford & Blakey 2000 obs). Food abundance and chick condition are usually positively correlated (e.g. Saino et al. 1997 exp, Hoi-Leitner et al. 2001 obs). Therefore, a lowering of brood condition owing to habitat-induced food shortages may reduce the levels of parental nest defence, resulting in increased predation rates, but no studies have been done on farmland birds.

Fragmentation and edge effects

Agricultural land is the dominant habitat type throughout Europe and is not usually considered to be fragmented. However, specific components (e.g. hay meadows and extensive pasture) have become more isolated and hedgerows may be viewed as extensively fragmented linear strips of woodland.

Populations isolated by fragmentation may be more vulnerable to extinction as a result of predation (Macdonald et al. 1999 model). An increased nest-predation rate, owing to edge effects, is one of the most cited explanations for bird population declines in fragmented landscapes (Carlson & Hartman 2001 review), and many other reviews have concluded that nest predation rates are elevated in edge habitats (Paton 1994, Andren 1995, Major & Kendal 1996, Hartley & Hunter 1998). However, although the most recent review (Lahti 2001) found that the probability of an edge effect occurring did increase with the degree of fragmentation, it did not support the generalization of increased nest-predation in edge habitats. Other recent studies have also failed to find that predation rates are influenced by edge effects (Carlson & Hartman 2001 exp, Howard et al. 2001 exp, Huhta & Jokimaki 2001 obs).

Therefore, the case for fragmentation contributing to farmland bird declines, through elevated predation rates, is weak and no explicit studies have been conducted. However, some support for the hypothesis is provided by Chamberlain et al. (1995 exp), who found that the probability of predation on Common Blackbird nests increased along a transition from woodland to woodland edge to hedgerows.

Increased adult predation rates

Reduced food availability

Many species reduce their fat loads when the perceived risk of predation is high, probably as a consequence of mass-dependent predation risk (e.g. Cresswell 1998 obs, Carrascal & Polo 1999 exp). Recent increases in predator densities may thus cause birds to carry less fat than they did historically, as demonstrated in the Great Tit (Gosler et al. 1995 obs, Gentle & Gosler 2001 exp). The combination of increased predation and reduced food availability may therefore have increased starvation-induced mortality in farmland birds by reducing the difference between the optimum mass, for avoiding predation, and the threshold mass at which starvation occurs.

Increased predation risk may also increase the probability of starvation by reducing the maximum potential daily intake rate. This might occur as a consequence of the costs of predator avoidance behaviour, e.g. the metabolic costs of fleeing or reduced foraging time owing to increased time spent in vigilance behaviour and/or in cover (e.g. Lima & Dill 1990 review, Dall & Witter 1998 exp, Lilliendahl 2000 exp).

Another possibility is that as birds approach the starvation threshold they are obliged to forage in a manner that increases their predation risk (Ward et al. 2000 model), and field studies support this hypothesis (Lima & Dill 1990 review, Hilton et al. 1999 obs). For example, when Yellowhammer Emberiza citrinella maximum daily food intake rates are close to the survival threshold they reduce the time that they invest in vigilance behaviour and continue foraging when predator activity is highest (van der Veen 2000 exp).

The ‘predation-sensitive food hypothesis’ (McNamara & Houston 1987, Abrams 1991) describes the situation that exists when such increased risk-taking results in higher predation rates, which limit the population. Such interactions between food availability and predation risk limit the Serengeti Wildebeast Connochaetes taurinus population (Sinclair & Arcese 1995 obs), influence population density in Snowshoe Hares Lepus americanus (Krebs et al. 1995 exp) and Arctic Ground Squirrels Spermophilus parryii (Karels et al. 2000 exp), and may explain the decline in the UK's Common Bullfinch Pyrrhula pyrrhula population. Foraging Bullfinches may have been restricted to areas near cover because of an increased risk of Sparrowhawk predation following an increase in their population size, and this may have reduced access to food and thus lowered the carrying capacity of the environment, precipitating a population decline (Newton 1967 obs).

DISCUSSION

  1. Top of page
  2. Abstract
  3. Evidence for predation effects
  4. Evidence for habitat effects
  5. INTERACTION MECHANISMS
  6. DISCUSSION
  7. Acknowledgments
  8. REFERENCES

Research implications

Numerous mechanisms exist through which interactions between agricultural intensification and predation could have contributed to farmland bird declines. However, insufficient research has been conducted to assess whether this potential is realized. A fuller understanding of farmland bird declines would arise if experiments were conducted to test for the presence of interactions between habitat change and predation. Whilst it is difficult to design such experiments in a manner that combines scientific rigour and practicality, some suggestions are outlined in Table 2.

Table 2.  Summary of the main mechanisms through which interactions between habitat change and predation rates may arise, and outlines of experiments to test for the presence of such interactions.
Habitat changeInteraction mechanismExperimental test
  • *

    Manipulating perception of predation risk should be done through exposure to predator models, caged predators or flying of tame raptors.

  • Food availability should be experimentally manipulated through both experimental increases (e.g. with supplementary feeding) and reductions (e.g. with pesticides).

  • These experiments could be done with real or artificial nests. Ideally, real nests should be used owing to problems associated with artificial nest experiments, e.g. they do not mimic parental behaviour and lack olfactory stimuli (e.g. Willebrand & Marcström 1988, Roper 1992, Haskell 1995, Major & Kendal 1996). However, if restricting the study to real nests would yield low sample sizes, then artificial nest experiments should be used as they can provide useful data (Sieving & Willson 1998, Wilson et al. 1998). The problems associated with artificial nest experiments can be reduced by baiting nests with eggs that structurally resemble those of the study species (de Graaf & Maier 1996, Maier & de Graaf 2001) and using real, but abandoned, nests of the focal species (Martin 1987).

Reduced food availability …… increases the probability of the threshold mass at which starvation occurs being reached whilst increased predation risk simultaneously reduces the difference between the optimum mass, for avoiding predation, and the starvation mass. In combination these effects increase starvation rates and reduce over-winter survival*Manipulate perception of predation risk, during the winter, and measure changes in adult condition and subsequent survival
Reduced food availability …… increases risk taking and thus predation rates*Manipulate food availability and record changes in foraging location, vigilance behaviour and the time-lag between exposure to predators and resumption of foraging. Natural adult predation rates should be recorded if possible
Reduced food availability …… reduces primary food sources for generalist predatory leading to increased consumption of secondary food sources, i.e. nests and adult birdsManipulate the availability of predators’ alternative food sources and monitor changes in predator density, which may be a confounding factor, and nest predation rates. For example, alter the availability of corvids’ alternative food supply by changing the availability of household waste
Reduced food availability …… increases begging intensity and thus nest detectability and predation ratesA. Manipulate begging rates by altering food levels or feeding chicks. Record food availability, begging rates (with hidden microphones) and predation rates. Changes in parental nest defence behaviour need to be controlled for statistically or, when chicks do not require brooding, by short-term removal of parents. B. Play begging calls at nests to simulate increased begging levels and monitor changes in predation rates, again controlling for changes in parental behaviour. (Although note that this will not demonstrate the link between increased begging and altered food availability)
Reduced food availability …… lowers parental defence and thus increases nest predation rates through …*All experiments involve recording changes in adult attack behaviour when exposed to predators. Record the following variables: (1) time lag from exposure to response, (2) attack intensity, (3) maximum distance between predator and nest at which attack occurs. All experiments also require statistical control for and thus recording of parental condition (with automatic balances), begging intensity (with hidden microphones) and parental foraging distances (with radio-telemetry)
 1… lowered parental body condition and thus nest defenceManipulate adult body condition by roosting overnight at higher or lower temperatures than ambient, thus providing an energy surplus or deficit (see Spencer 1998)
 2… lowered chick condition, reducing parents’ willingness to defend the nestManipulate brood condition by changing brood size
 3… forcing adults to forage further from the nest, reducing their ability to detect and deter predatorsManipulate food availability
Reduced nest-site quality …… forces birds to nest in less suitable sites and/or at higher densities increasing nest predation ratesAcross sites increase and decrease the availability of suitable nest-sites by manipulating vegetation characteristics (e.g. sward height and density) and record changes in the selection of nesting habitat, nest density and predation rates
NB. All experiments should be conducted with replication, across sites and years, and treatment reversal at each site. Extra information on appropriate techniques could be gained from the studies, cited in the main text, based on experimental manipulations.

Management implications

When interactions between habitat change and predation contribute to population declines, predator impacts could be reduced by killing predators and/or through habitat management. The most appropriate solution will depend on the predators’ overall, or total, response to increasing prey density. The total response is the product of the numerical and functional responses (Solomon 1949). The numerical response describes how the predator population initially increases with prey density, owing to increased immigration and reproduction, and then levels off as a result of limitation by other factors. The functional response represents consumption by a single predator and usually takes one of two forms (Holling 1959, 1965). In the Type II response, consumption increases with prey density, but then reaches an asymptote owing to predator satiation and handling time. The Type III response is described by an S-shaped curve, i.e. consumption is directly density-dependent at low prey densities and inversely density-dependent at high prey densities.

When the total response follows a Type III response curve, predators may trap their prey in a locally stable state of low density, i.e. a predation pit. This situation arises as, at low prey densities, the rate of population growth is lower than the rate at which predation-induced mortality increases with increased prey density. Conversely, at high prey densities, the predation rate becomes inversely density-dependent so an increase in the prey population, e.g. as a result of reduced predation, allows the prey to escape to a high population density. Moreover, this density is locally stable even when predation increases to the original rate (Sinclair et al. 1998).

The existence of a predation pit has been demonstrated conclusively for Red Fox predation on Rabbits in Australia (Pech et al. 1992 exp, Banks 2000 exp) and evidence strongly suggests its occurrence in other systems (Krebs 1996 exp, Calvete et al. 1997 obs, Sinclair et al. 1998 obs). When predator–prey dynamics operate according to the predation pit hypothesis, the short-term control of predators may allow the prey species to achieve permanently higher densities, even when predator control is subsequently relaxed. In this situation predator control may be a more cost-effective conservation solution than habitat management, owing to the shorter time period over which it is required.

When dynamics follow the Type II response function, a predation pit cannot arise. This is because population growth rates are never lower than the rate at which predation increases with increased prey density, at least within the range of predator densities that are consistent with viable prey populations (Sinclair et al. 1998 model & obs). Therefore, permanently reducing predator impacts by killing predators will require a permanent reduction in predator density. As immigrants frequently replace exterminated individuals, this usually entails an indefinite, and thus expensive, commitment to predator control; this, however, may only require episodic culling. Therefore, when predator–prey dynamics follow a Type II response curve, and interactions occur between predation rates and habitat change, habitat management may be a more cost-effective management solution than predator control. The use of habitat management to control predators has the additional benefit of removing any conflict between conservation organizations and their membership over animal welfare issues that may arise from killing predators (e.g. Gentile 1987, Minnis 1997).

The presence of interactions between habitat change and predation thus presents conservation managers with a range of options for reversing population declines. The selection of the most appropriate solution will require knowledge of the interaction mechanism, together with an understanding of how the predation rate varies with prey densities, i.e. the functional response. In practice it can be difficult to determine the nature of the functional response from a statistical (Holling & Arditi 1982, Trexler et al. 1988) or practical point of view (Sinclair et al. 1998) and data may fit a particular functional response even when the assumptions underlying the theory of that response are not met (Caldow & Furness 2001). However, guidance can be offered to conservation managers concerning which type of functional response is likely to apply to a particular situation. Type II responses are the commonest type reported in the literature (Caldow & Furness 2001, Skalski & Gilliam 2001). Type III responses are likely to occur when the prey species is relatively inaccessible, as a result of its rarity or occupation of refuges, and when a generalist predator switches to alternative food sources (Hik 1995, Molles 1999, van Baalen et al. 2001, Schenk & Bacher 2002). In considering this guidance it should be remembered that there is no substitute for high-quality research data when determining the nature of a functional response. If conservation managers are to address interactions between habitat change and predation rates, the first and essential step is for researchers to determine the type and frequency of such interactions by conducting experiments such as those outlined in Table 2. It is hoped that this review provides the stimulus for such research.

Acknowledgments

  1. Top of page
  2. Abstract
  3. Evidence for predation effects
  4. Evidence for habitat effects
  5. INTERACTION MECHANISMS
  6. DISCUSSION
  7. Acknowledgments
  8. REFERENCES

This work was conducted whilst funded by a D. Phil. stipend from the Royal Society for the Protection of Birds. Andy Wilson, Richard Bradbury, Will Cresswell, Jeremy Wilson and an anonymous referee all helped to improve the manuscript.

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  1. Top of page
  2. Abstract
  3. Evidence for predation effects
  4. Evidence for habitat effects
  5. INTERACTION MECHANISMS
  6. DISCUSSION
  7. Acknowledgments
  8. REFERENCES
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