The starvation–predation risk trade-off, body mass and population status in the Common Starling Sturnus vulgaris

It is theoretically and empirically well established that body mass variation in small birds reflects a trade-off between starvation risk and predation risk. This occurs because carrying increased fat reserves reduces starvation risk but also results in a higher predation risk due to reduced escape flight performance and/or the increased foraging exposure needed to maintain a higher body mass. In principle, therefore, the theory of mass-dependent predation risk could be used to understand how a bird perceives and responds to the risks in its environment, because its mass will reflect the predictability of foraging opportunities and predation risk. Mass in birds may then provide a relatively straightforward way of assessing the foraging environment of birds and so the potential conservation problems a species faces. This study tests, for the first time for any species, how body mass changes in response to changing starvation risk, changing predation risk and changing population status. Common Starling Sturnus vulgaris mass varies as predicted by starvation–predation risk trade-off theory: mass is lower when foraging conditions are more favourable and when predation risk is increased. The populations that are declining the most strongly have higher mass, which is most likely indicative of a poor foraging environment, leading to lower relative survival. The results suggest that increased mass in Starlings, and possibly in other species, may provide an indication of the poor quality of the foraging environment and/or rapidly declining populations.     

Fat reserves and perceived predation risk in the great tit, Parus major

The fat reserves of small birds are built up daily as insurance against starvation. They are believed to reflect a trade-off between the risks of starvation and predation such that in situations of high predation risk birds are expected either to reduce their fat reserves in response to mass-dependent predation risk or to increase them in response to foraging interruptions. We assessed the effect on fat reserves of experimentally altering the perceived (but not the actual) risk of predation of wild great tits at a winter feeding site. The perceived predation risk was alternated between 'safe' and 'risky'. Increasing the perceived risk of predation involved 'swooping' a model sparrowhawk over the feeder at four unpredictable times each day using a remote mechanism We produce evidence that the experiment was suceessfull in altering the perceived risk of predation. As predicted from the hypothesis of mass-dependent predation risk, great tits (Parus major) carried significantly reduced fat reserves during the 'risky' treatment. Furthermore, dominant individuals were able to reduce their reserves more than subordinates. As birds returned to feeders within seconds after a predator 'attack', the reduction in fat reserves cannot be attributed to an interruption in feeding.     

Body mass variations in disturbed mallards Anas platyrhynchos fit to the mass‐dependent starvation‐predation risk trade‐off

For passerines the starvation‐predation risk theory predicts that birds should decrease their body mass to improve escape flight performance, when predation pressure increases. To investigate whether this theory may apply to large birds, which manage body reserves differently from small passerines, we experimentally increased the predation risk in mallards Anas platyrhynchos. Two groups were disturbed at different frequencies during experimental sessions lasting one week, while a control group was left undisturbed. We found that body mass loss and final wing loading were similar in both disturbed groups and significantly differed from the control group. Food intake in disturbed groups was reduced up to day four of the disturbance session and was lower than in the control group. Altogether our results suggest that disturbed mallards may adjust their body mass to reach a more favorable wing loading, supposedly to improve escape flight performance. Nevertheless, body mass loss in our mallards was double than what has been observed in passerines. This greater mass decrease might be explained by different strategies concerning energy storage. Furthermore, in large birds the predation component of the starvation‐predation trade‐off might be of greater importance. Hence, the observed relevance of this trade‐off over a large size range suggests that the starvation‐predation risk theory is of major ecological significance for many animal species.     

Escape flights of yellowhammers and greenfinches: more than just physics

Wintering birds increase their fat reserves throughout the day, and impaired escape performance is often considered to be an important cost of fat reserves. Since lifting a larger mass requires more energy, if birds escape at maximum power output, an increase in mass will impair the escape flight. In this study we did not find support for mass-dependent escape performance for yellowhammers, Emberiza citrinella, and greenfinches, Carduelis chloris, with natural daily mass increases of 7-8%. This suggests either that the birds were not performing at maximum output at dawn, when light, or that maximum power output was higher at dusk, when heavy. Either way, the birds seemed to be able to put more effort into their escape flight when heavier. In both species, when alarmed, birds took off significantly faster and at a steeper angle than when not alarmed. Yellowhammers escaped at a higher speed and angle than greenfinches, and reacted faster to the predator model. This suggests that predator escape is more than just Newtonian physics, and may be influenced by behavioural, as well as morphological, adjustments. Different species may have evolved different responses to predation risk. Our results seem to be in disagreement with recent ideas about mass-dependent predation risk. However, to build up reserves, birds have to increase exposure time, which increases predation risk. This cost may be more important than impaired escape performance when relatively small, daily, changes in body mass are considered. Copyright 2000 The Association for the Study of Animal Behaviour.     

Why do hoarding birds gain fat in winter in the wrong way? Suggestions from a dynamic model

In winter, small birds should be fat to avoid starvation andlean and agile to escape predators. This means that they facea trade-off between the costs and benefits of carrying fat reserves.Every day they must gain enough fat to survive the coming night.Food-hoarding species can afford to carry less fat than nonhoardersbecause they can store energy outside the body. Furthermore, hoardersshould avoid carrying excessive fat during the day because theycan gain fat fast by retrieving food late in the afternoon.With no stored supplies, nonhoarders face more unpredictableaccess to food, and they should start gaining fat earlier inthe day. The predicted pattern is then that nonhoarders gainfat early and that hoarders gain fat late in the day. Recent fielddata show the opposite pattern: hoarders gain relatively morefat reserves in the morning than nonhoarders do. Using a dynamicmodel that mimics the conditions in a boreal winter forest,I investigated under which conditions this pattern will arise.The only assumption of those investigated that produced thispattern was to relax the effect of mass-dependent predation risk.I did this by introducing a limit under which fat reserves didnot affect predation risk. Hoarders then started the day bygaining fat in the morning. Later, when they had reached a safer(but still not risky) level, they switched to hoarding. Thepattern I searched would only occur if either not all food waspossible to store, or if retrieval gave less energy than foragingin good weather conditions. If I assumed that low levels ofbody fat also increased predation risk, hoarders would cachein the morning when they carried least fat. I discuss empiricalevidence for how body fat affects predation risk. In summary,the factors that produced the pattern I searched were a changein the predation-mortality function combined with restrictions onhoarding.     

Mass-dependence in the predation risk of unequal competitors; some models

Foragers can monitor their survival through the size of body reserves in a starvation/predation risk trade-off. Energy reserves reduce the risk of energetic shortfall, while survival will be maximised at intermediate reserve levels when there is a cost of carrying mass loads. The size of reserves that will maximise survival may not be identical for unequal competitors, when unequal access to resources will affect the costs and benefits of energy reserves. Here, I evaluate the effect of competitive ability (dominance) for the mass-dependence in predation risk and how it is affected by (1) attack rate (attack rate effect), (2) distance to the emergence of an unconcealed predator attack (attack distance effect) and (3) distance to cover (cover distance effect). This general model is illustrated by empirical data for parameters specific for birds. The effect of competitive ability for the mass-dependence in predation risk is ambiguous and depends on how rank is mediated into mass-dependent predation risk. Dominants pay a lower cost in predation risk for mass loads than sub-ordinates when competitive ability entails that they feed closer to cover (cover distance effect) and when the exposure to attacks and attack rate is lower than for sub-ordinates (attack rate effect) . In contrast, a shorter distance to the emergence of an unconcealed attack (attack distance effect) implies a lower increase in predation risk with mass for sub-ordinates. As a consequence of how the cost of mass load varies with conditions there is no unambiguous relationship for how predation risk can be traded off for starvation risk for individuals with different competitive ability.     

Mass regulation in response to predation risk can indicate population declines

In theory, survival rates and consequent population status might be predictable from instantaneous behavioural measures of how animals prioritize foraging vs. avoiding predation. We show, for the 30 most common small bird species ringed in the UK, that one quarter respond to higher predation risk as if it is mass-dependent and lose mass. Half respond to predation risk as if it only interrupts their foraging and gain mass thus avoiding consequent increased starvation risk from reduced foraging time. These mass responses to higher predation risk are correlated with population and conservation status both within and between species (and independently of foraging habitat, foraging guild, sociality index and size) over the last 30 years in Britain, with mass loss being associated with declining populations and mass gain with increasing populations. If individuals show an interrupted foraging response to higher predation risk, they are likely to be experiencing a high quality foraging environment that should lead to higher survival. Whereas individuals that show a mass-dependent foraging response are likely to be in lower quality foraging environments, leading to relatively lower survival.     

Evidence of the trade-off between starvation and predation risks in ducks

The theory of trade-off between starvation and predation risks predicts a decrease in body mass in order to improve flight performance when facing high predation risk. To date, this trade-off has mainly been validated in passerines, birds that store limited body reserves for short-term use. In the largest avian species in which the trade-off has been investigated (the mallard, Anas platyrhynchos), the slope of the relationship between mass and flight performance was steeper in proportion to lean body mass than in passerines. In order to verify whether the same case can be applied to other birds with large body reserves, we analyzed the response to this trade-off in two other duck species, the common teal (Anas crecca) and the tufted duck (Aythya fuligula). Predation risk was simulated by disturbing birds. Ducks within disturbed groups were compared to non-disturbed control birds. In disturbed groups, both species showed a much greater decrease in food intake and body mass during the period of simulated high risk than those observed in the control group. This loss of body mass allows reaching a more favourable wing loading and increases power for flight, hence enhancing flight performances and reducing predation risk. Moreover, body mass loss and power margin gain in both species were higher than in passerines, as observed in mallards. Our results suggest that the starvation-predation risk trade-off is one of the major life history traits underlying body mass adjustments, and these findings can be generalized to all birds facing predation. Additionally, the response magnitude seems to be influenced by the strategy of body reserve management.     

Testing the mass-dependent predation hypothesis: in European blackbirds poor foragers have higher overwinter body reserves

As foraging becomes more unpredictable animals should increase their body reserves to reduce the risk of starvation. However, any increases in reserves may increase the risk of predation because extra mass probably compromises escape ability. Because of differences in foraging ability not all individuals will be affected in the same way by changes in foraging conditions. Relatively poor foragers will have more unpredictable foraging success for any given availability of food and therefore should carry larger body reserves. The mass-dependent predation hypothesis then predicts a negative correlation between levels of body reserves and foraging ability, although this may be modified by state-dependent compensation. I measured foraging rates and body masses of wintering European blackbirds, Turdus merula. Individuals with the lowest foraging rates had the largest gain in mass for the winter and had relatively high mass overall, independently of age and sex. That foraging rate determined mass rather than the reverse was demonstrated because foraging rate was independent of daily and seasonal mass change. Foraging rate within the experimental system was also independent of predation risk (as measured by distance from protective cover) and so the relation between mass and foraging rate was unlikely to have been confounded by any changes in vigilance to compensate for increased mass-dependent predation risk. The results suggest that blackbirds with high relative foraging rates have lower body reserves during the winter. Therefore there is probably a direct link between overwinter condition and fitness at least in blackbirds. Copyright 2003 Published by Elsevier Science Ltd on behalf of The Association for the Study of Animal Behaviour.      

How climate change might influence the starvation–predation risk trade-off response

Climate change within the UK will affect winter starvation risk because higher temperatures reduce energy budgets and are likely to increase the quality of the foraging environment. Mass regulation in birds is a consequence of the starvation–predation risk trade-off: decreasing starvation risk because of climate change should decrease mass, but this will be countered by the effects of predation risk, because high predation risk has a negative effect on mass when foraging conditions are poor and a positive effect on mass when foraging conditions are good. We tested whether mass regulation in great tits (Parus major) across the UK was related to temporal changes in starvation risk (winter temperature 1995–2005) and spatial changes in predation risk (sparrowhawk Accipiter nisus abundance). As predicted, great tits carried less mass during later, warmer, winters, demonstrating that starvation risk overall has decreased. Also, the effects of predation risk interacted with the effects of temperature (as an index of foraging conditions), so that in colder winters higher sparrowhawk abundance led to lower mass, whereas in warmer, later, winters higher sparrowhawk abundance led to higher mass. Mass regulation in a small bird species may therefore provide an index of how environmental change is affecting the foraging environment.     

Loss of body mass under predation risk: cost of antipredatory behaviour or adaptive fit-for-escape?

Predation risk may compromise the ability of animals to acquire and maintain body reserves by hindering foraging efficiency and increasing physiological stress. Locomotor performance may depend on body mass, so losing mass under predation risk could be an adaptive response of prey to improve escape ability. We studied individual variation in antipredatory behaviour, feeding rate, body mass and escape performance in the lacertid lizard Psammodromus algirus. Individuals were experimentally exposed to different levels of food availability (limited or abundant) and predation risk, represented by reduced refuge availability and simulated predator attacks. Predation risk induced lizards to reduce conspicuousness behaviourally and to avoid feeding in the presence of predators. If food was abundant, alarmed lizards reduced feeding rate, losing mass. Lizards supplied with limited food fed at near-maximum rates independently of predation risk but lost more mass when alarmed; thus, mass losses experienced under predation risk were higher than those expected from feeding interruption alone. Although body mass of lizards varied between treatments, no component of escape performance measured during predator attacks (endurance, speed, escape strategy) was affected by treatments or by variations in body mass. Thus, the body mass changes were consistent with a trade-off between gaining resources and avoiding predators, mediated by hampered foraging efficiency and physiological stress. However, improved escape efficiency is not required to explain mass reduction upon predator encounters beyond that expected from feeding interruption or predation-related stress. Therefore, the idea that animals may regulate body reserves in relation to performance demands should be reconsidered.     

Subtle cues of predation risk: starlings respond to a predator's direction of eye-gaze

For prey animals to negotiate successfully the fundamental trade-off between predation and starvation, a realistic assessment of predation risk is vital. Prey responses to conspicuous indicators of risk (such as looming predators or fleeing conspecifics) are well documented, but there should also be strong selection for the detection of more subtle cues. A predator's head orientation and eye-gaze direction are good candidates for subtle but useful indicators of risk, since many predators orient their head and eyes towards their prey as they attack. We describe the first explicit demonstration of a bird responding to a live predator's eye-gaze direction. We present wild-caught European starlings (Sturnus vulgaris) with human 'predators' whose frontal appearance and gaze direction are manipulated independently, and show that starlings are sensitive to the predator's orientation, the presence of eyes and the direction of eye-gaze. Starlings respond in a functionally significant manner: when the predator's gaze was averted, starlings resumed feeding earlier, at a higher rate and consumed more food overall. By correctly assessing lower risk and returning to feeding activity earlier (as in this study), the animal gains a competitive advantage over conspecifics that do not respond to the subtle predator cue in this way.     

What determines probability of surviving predator attacks in bird migration?: the relative importance of vigilance and fuel load

Migrating birds must accumulate fuel during their journeys and this fuel load should incur an increased risk of predation. Migratory fuelling should increase individual mass-dependent predation risk for two reasons. First, acquisition costs are connected to the increased time a bird must spend foraging to accumulate the fuel loads and the reduced predator detection that accompanies foraging. Second, birds with large fuel loads have been shown to suffer from impaired predator evasion which makes them more vulnerable when actually attacked. Here, I investigate the relative importance of these two aspects of mass-dependent predation risk and I have used published data and a hypothetical situation for a foraging bird to investigate how much migratory fuelling in terms of escape performance and natural variation in predator detection contribute to individual risk during foraging. Results suggest that for birds foraging close to protective cover the negative impact of fuel load on flight performance is very small, whereas variation in time to predator detection is of great importance for a bird's survival. However, the importance of flight performance for predation risk increases as the distance to cover increases. Hence, variation in predator detection (and vigilance) probably influences individual survival much more than migratory fuel load and consequently, to understand risk management during migration studies that focus on vigilance and predator detection during fuelling are much needed.     

The effect of thermoregulatory substitution on optimal energy reserves of small birds in winter

Previous models have predicted the body mass of small birds in winter on the basis of a trade-off between starvation and predation. Many of these models have assumed that energy expenditure while active increases with body mass. The implications of the fact that the metabolic cost of activity can substitute for internal heat production and help keep the bird warm have not been investigated. In this paper we show that if thermoregulatory substitution occurs then there is a critical level of energy reserves above which an active bird is thermoneutral. This critical level increases as temperature decreases. Below this level, substitution of energy results in higher optimal levels of reserves than would be predicted in the absence of substitution. Our model thus predicts that at low temperatures body mass will be higher when thermoregulatory substitution occurs.     

Anti-Predator Behavioral Responses of Mosquito Pupae to Aerial Predation Risk

Aquatic insects have two potential sources of predation risk: aquatic predators and aerial predators. Our goal was to assess anti-predator responses of Culex pipiens to aerial predation. By simulating predator attacks, we assessed (a) the distance fled in relation to depth and group size, (b) the distribution of individuals at different depths, and (c) the duration of surfacing events to obtain air in scenarios with varying predation risk. Pupae located closer to the surface fled deeper into the water, and the number of conspecifics decreased the distance fled. When the risk of predation increased, more individuals were found deeper in the water column, and the interval between two consecutive surfacing events increased. Culex pipiens shows a trade-off between avoiding aerial predation and maintaining oxygen acquisition, which may be regulated by the need to conserve energy reserves.     

Strategic diel regulation of body mass in European robins

Stochastic dynamic programming (SDP) is a computational technique that has been used to model daily routines of foraging in small birds. A diurnal bird must build up its fat reserves towards dusk in order to avoid starvation during the night, when it cannot feed. However, as well as the benefits of avoiding starvation, storing fat imposes costs such as an increased predation risk and higher flight and metabolic costs. There is therefore an optimal level of fat reserves for a bird to reach at dusk in order to survive overnight without being left with excessive fat reserves at dawn. I tested a prediction common to all SDP models of daily foraging routines, that a bird will attempt to reach this level at dusk, regardless of its fat reserves the previous dawn. I provided supplementary food to manipulate the fat reserves at dawn of free-living European robins, Erithacus rubecula. Diurnal changes in body mass (a reliable estimate of fat reserves) were then monitored remotely. Robins provided with an ad libitum food supply reached almost exactly the same body mass at dusk, regardless of their body mass at dawn, supporting the prediction that birds attempt to reach a target level of reserves at dusk. Copyright 2000 The Association for the Study of Animal Behaviour.     

The effects of latitude and day length on fattening strategies of wintering coal tits Periparus ater (L.): a field study and aviary experiment

1. Cyclic daily fattening routines are very common in wintering small wild birds, and are thought to be the consequence of a trade-off between different environmental and state-dependent factors. According to theory, these trajectories should range from accelerated (i.e. mass increases exponentially towards dusk) when mass-dependent predation costs are the most important cause of mortality risk, to decelerated (i.e. the rate of mass gain is highest at dawn and decreases afterward) when starvation is the greater risk. 2. We examine if geographically separate populations of coal tits, wintering in Scotland and central Spain under contrasting photoperiods, show differences in their strategies of daily mass regulation. We describe population differences in wild birds under natural conditions, and experimentally search for interpopulation variation in diurnal body mass increase under common, manipulated, photoperiod conditions (LD 9 : 15 h vs. 7 : 17 h), controlling for temperature, food availability, predator pressure and foraging arena. 3. Winter diurnal mass gain of wild coal tits was more delayed towards the latter part of the daylight period in central Spain (i.e. the locality with longer winter days) than in Scotland. In both localities, the pattern was linked to the average mass at dawn, with mass increasing more rapidly in lighter birds. However, under the controlled photoperiod situation the pattern of daily mass gain was similar in both populations. Diurnal body mass gain was more accelerated at the end of the day, and the increase in body mass in the first hour of the day was considerably lower under the long (9 h) than under the short (7 h) photoperiod in both populations. 4. Wintering coal tits show patterns of mass gain through the day that are compatible with current theories of the costs and benefits of fat storage, with birds at lower latitudes (with longer winter days) having a greater tendency to delay mass gain until late in the day. The experimental study revealed that these patterns are plastic, with birds responding directly to the photoperiod that they experience, suggesting that they are continually making fine-scale adjustments to energy reserves on the basis of both inherent (e.g. state-dependent) and extrinsic cues.     

Sizing up your enemy: individual predation vulnerability predicts migratory probability

Partial migration, in which a fraction of a population migrate and the rest remain resident, occurs in an extensive range of species and can have powerful ecological consequences. The question of what drives differences in individual migratory tendency is a contentious one. It has been shown that the timing of partial migration is based upon a trade-off between seasonal fluctuations in predation risk and growth potential. Phenotypic variation in either individual predation risk or growth potential should thus mediate the strength of the trade-off and ultimately predict patterns of partial migration at the individual level (i.e. which individuals migrate and which remain resident). We provide cross-population empirical support for the importance of one component of this model--individual predation risk--in predicting partial migration in wild populations of bream Abramis brama, a freshwater fish. Smaller, high-risk individuals migrate with a higher probability than larger, low-risk individuals, and we suggest that predation risk maintains size-dependent partial migration in this system.     

Seasonal changes in the response of oystercatchers Haematopus ostralegus to human disturbance

The response of foraging animals to human disturbance can be considered as a trade-off between the increased perceived predation risk of tolerating disturbance and the increased starvation risk of not feeding and avoiding disturbance. We show how the response of overwintering oystercatchers Haematopus ostralegus to disturbance is related to their starvation risk of avoiding disturbance. As winter progresses, oystercatcher energy requirements increase and their feeding conditions deteriorate. To survive they spend longer feeding and so have less spare time in which to compensate for disturbance. Later in winter, birds approach a disturbance source more closely and return more quickly after a disturbance. Their behavioural response to disturbance is less when they are having more difficulty surviving and hence their starvation risk of avoiding disturbance is greater. These results have implications for studies which assume that a larger behavioural response means that a species is more vulnerable to disturbance. The opposite may be true. To more fully understand the impact of disturbance, studies should measure both behavioural responses and the ease with which animals are meeting their requirements. Conservation effort should be directed towards species which need to spend a high proportion of their time feeding, but still have a large response to disturbance.     

The costs of being cool: a dynamic model of nocturnal hypothermia by small food-caching birds in winter

Many birds could expend substantially less energy at night by using hypothermia, but generally do not. This suggests that the potential savings are offset by costs; one of these costs is presumed to be the risk of predation at night. If this assumption is correct, a bird will face one of two tradeoffs: (1) it can avoid the cost of hypothermia by gaining fat to decrease the risk of starvation, but this increases energetic costs of fat maintenance and risk of diurnal predation, or (2) it can maintain lower fat reserves and use hypothermia at night, but this option increases the risk of nocturnal predation. We used a dynamic model to investigate these trade-offs and how the use of nocturnal hypothermia changes energy management tactics in food-caching birds. Our model predicted that: (i) optimal daily routines of fat reserves, feeding rate, food caching, and cache retrieval should be similar in hypothermic and non-hypothermic birds; (ii) low fat reserves, small cache size, low ambient temperature, and high variability in foraging success favor increased use of hypothermia; (iii) the effect of ambient temperature on the use of hypothermia is especially important at higher levels of variance in foraging success; (iv) hypothermic birds are predicted to have lower mass at dusk than non-hypothermic individuals while their morning mass should be more similar. Many of these predictions have been supported by empirical data. Also, survival rates are predicted to be higher for birds using hypothermia, especially in the most severe environmental conditions. This is the first attempt to evaluate the role of cache maintenance and variance in foraging success in the use of hypothermia. This is also the first discussion of the relationship between behavior hypothermia and diurnal patterns of energy management.