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.     

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.     

Redshank Tringa totanus flocking behaviour, distance from cover and vulnerability to sparrowhawk Accipiter nisus predation

Over 11 winters I examined the interactions between sparrowhawk Accipiter nisus attack behaviour, the gregariousness of redshanks Tringa totanus and local geography to test hypotheses that suggest birds should flock to reduce their risk of predation and that predation risk should decline with the prey's distance from cover. Sparrowhawk attacks on redshanks feeding on beaches around the high tide mark (the strandline zone) were more frequent and more successful than attacks on redshanks feeding seaward of the strandline zone (in the intertidal zone). The results therefore confirmed hypothetical expectations that predation risk should decline with distance from cover. Flocking only appeared to influence the outcome of hawk attacks at shorter distances from cover on the strandline, with attacks on singletons and small flocks being more successful than attacks on larger flocks. Distance from cover had a stronger influence on the likelihood of attack success than did flock size. Mid-range flock sizes (6–45 birds) were attacked more frequently than expected, but singletons and large flocks were attacked less than expected. Despite these differences an individual redshank's likelihood of predation by a sparrowhawk declined with increasing flock size, thereby confirming the 'dilution effect' and 'vigilance' hypotheses for the evolution of flocking in birds. Food intake rates of redshanks declined with increasing flock size, further indicating that redshanks flocked to avoid predation rather than to increase their food intake rates. The strong interaction between two influences on predation risk revealed by the present study suggests other studies should take great care when considering a single influence on predation risk in isolation from others.     

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.     

Response to Predation Risk in Urban and Rural House Sparrows

Habitat urbanization may change the density of predators, and it is often assumed that such changes lead to altered predation risk for urban populations of their prey. Although it is difficult to study predation hazard directly, behavior responses of prey species may be informative in inferring such habitat differences. In this study, we compared the risk‐taking behavior of urban and rural house sparrows (Passer domesticus) after simulated attacks by two of their important predators (sparrowhawk Accipiter nisus and domestic cat Felis catus). The birds were startled by moving dummies of these predators and respective control objects, and their risk taking was estimated as their latency to feed after the startle. We found that sparrows responded more strongly (had longer post‐startle feeding latencies) to sparrowhawk attacks than to the control object, and their responses differed between the habitats. First, risk taking of urban birds strongly decreased with age (older birds had longer latencies than young birds), while there was no such age difference in rural birds. Second, young urban birds responded less strongly, while older urban birds responded more strongly to the sparrowhawk than the same age groups of rural birds, respectively. We did not succeed in evoking antipredatory response by simulated cat attacks, because birds responded similarly to the dummy and the control object. Our results support that predation risk, posed at least by avian predators, is different in urban and rural habitats of house sparrows. The increased wariness of older, hence presumably more experienced, urban birds implies that sparrows may be more exposed to predation in cities.     

Daily accumulation of body reserves under increased predation risk in captive Greenfinches Carduelis chloris

The effect of increased perceived risk of predation on the trajectory describing the daily gain in body mass of captive Greenfinches Carduelis chloris was tested. Theoretically, increased risk of predation is expected to shift the gain in body mass towards the latter part of the day and reduce body mass. The perceived risk of predation was increased with a stuffed flying hawk three times per day. Following each presentation of the predator, foraging stopped and the birds lost mass. When feeding resumed, the birds compensated for the mass loss by increasing the rate of body mass gain, in line with theoretical predictions. In the presence of the predator, the daily accumulation of body reserves was lower compared with risk-free situations. However, on the days following presentation of the hawk, when the birds were presumably aware of an increased risk of predation, Greenfinches did not exhibit the predicted change in reserve accumulation, but rather maintained their usual pattern of body mass gain.     

Mass-dependent predation risk and lethal dolphin-porpoise interactions

In small birds, mass-dependent predation risk (MDPR) is known to make the trade-off between avoiding starvation and avoiding predation dependent on individual mass. This occurs because carrying increased fat reserves not only 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, the theory of MDPR could also apply to any animal capable of storing energy reserves to reduce starvation and whose escape performance decreases with increasing mass. We used a unique situation along certain parts of coastal Britain, where harbour porpoises (Phocoena phocoena) are pursued and killed but crucially not eaten by bottlenose dolphins (Tursiops truncatus), to investigate whether a MDPR effect can occur in non-avian species. We show that where high levels of dolphin 'predation' occur, porpoises carry significantly less energy reserves than would otherwise be expected and this equates to reducing by approximately 37% the length of time that a porpoise could survive without feeding. These results provide the first evidence that a mass-dependent starvation-predation risk trade-off may be a general ecological principle that can apply to widely different animal types rather than, as is currently thought, only to birds.     

Long‐term declines in winter body mass of tits throughout Britain and Ireland correlate with climate change

The optimum body mass of passerine birds typically represents a trade‐off between starvation risk, which promotes fat gain, and predation pressure, which promotes fat loss to maintain maneuvrability. Changes in ecological factors that affect either of these variables will therefore change the optimum body masses of populations of passerine birds. This study sought to identify and quantify the effects of changing temperatures and predation pressures on the body masses and wing lengths of populations of passerine birds throughout Britain and Ireland over the last 50 years. We analyzed over 900,000 individual measurements of body mass and wing length of blue tits Cyanistes caeruleus, coal tits Periparus ater, and great tits Parus major collected by licenced bird ringers throughout Britain and Ireland from 1965 to 2017 and correlated these with publicly available temperature data and published, UK‐wide data on the abundance of a key predator, the sparrowhawk Accipiter nisus. We found highly significant, long‐term, UK‐wide decreases in winter body masses of adults and juveniles of all three species. We also found highly significant negative correlations between winter body mass and winter temperature, and between winter body mass and sparrowhawk abundance. Independent of these effects, body mass further correlated negatively with calendar year, suggesting that less well understood dynamic factors, such as supplementary feeding levels, may play a major role in determining population optimum body masses. Wing lengths of these birds also decreased, suggesting a hitherto unobserved large‐scale evolutionary adjustment of wing loading to the lower body mass. These findings provide crucial evidence of the ways in which species are adapting to climate change and other anthropogenic factors throughout Britain and Ireland. Such processes are likely to have widespread implications as the equilibria controlling evolutionary optima in species worldwide are upset by rapid, anthropogenic ecological changes.     

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.     

Dominance, competition, and energetic reserves in the European starling, Sturnus vulgaris

We investigated the relationships between social dominance,competition for food, and strategies of body mass and fat regulationin the European starling (Sturnus vulgaris). In birds housedin groups of three, subdominant birds stored more fat than dominants.A removal experiment established a causal link between socialdominance and fat reserves; in groups that had the dominantindividual removed, the remaining birds reduced body mass andfat, relative to control groups that had the subordinate removed.In a second experiment, we investigated the influences of degreeof competition for food and dominance on body mass and fat reserves.Birds under high competition increased fat reserves and tendedto have higher body mass than birds under low competition. Theincrease in fat reserves was higher in the subdominants thanin the dominants. These results are consistent with hypothesesconcerning dominance-dependent access to food; subdominant birds,or birds under increased competition, may store more fat asan insurance against periods when food cannot be obtained. However,relations between dominance, body mass, and fat reserves mayalso arise through other proximate factors relating to dominance-dependentcosts and benefits of fat storage, such as predation risk andenergetic expenditure.     

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.     

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.     

Vulnerability to severe weather and regulation of body mass of Icelandic and British Redshank Tringa totanus

During severe weather, Redshanks suffer the heaviest mortality amongst all the shorebird species wintering around the North Sea coasts of the British Isles. An earlier study had suggested that this resulted from a failure to accumulate sufficient body fat reserves before mid-winter. Detailed field studies in northeast England between 1993 and 1995 of seasonal changes in body mass, and in estimated lean and fat masses, of two races of Redshank, both of which winter in the same estuary, were accompanied by similar studies of small numbers held in captivity with unlimited food. After differences in body size were allowed for, there were no differences in body composition and its seasonal pattern of change in birds of the Icelandic and British races. Body mass changes in wild birds paralleled those in captives between November and March, and mid-winter levels were not limited by food supply; indeed they were slightly higher in a winter with lower prey densities. It is concluded that Redshanks regulate body mass and, indirectly, fat reserves at levels set by a trade-off between the risks of predation and starvation. Unlike most other shorebird species, they take very small prey in relation to their body size and hence must feed for long periods during each tidal cycle to achieve their daily energy intake needs. Thus they have little scope to extend their feeding time during severe weather, which also forces them to feed on ice-free exposed coastal habitats where wind chill cannot be avoided. Both factors lead to more rapid depletion of fat reserves than in other species which have higher energy intake rates or lower total daily requirements.     

Separating the effects of predation risk and interrupted foraging upon mass changes in the blue tit Parus caeruleus

The optimal amount of reserves that a small bird should carry depends upon a number of factors, including the availability of food and environmental predation risk levels. Theory predicts that, if predation risk increases, then a bird should maintain a lower level of reserves. Previous experiments have given mixed results: some have shown reduced reserves and some, increased reserves. However, the birds in these studies may have been interpreting a staged predation event as a period when they were unable to feed rather than a change in predation risk: theory predicts that, if the food supply within the environment is variable, then reserves should be increased. In the present study, we presented blue tits (Parus caeruleus) with a potential predator and compared this response (which could have been potentially confounded by perceived interruption effects) with a response to an actual interruption in the environment during both long and short daytime lengths. During long (but not short) days, the birds responded in line with theoretical predictions by increasing their reserves in response to interruption and reducing them in response to predation. These results are examined in the light of other experimental manipulations and we discuss how well experimental tests have tested the predictions made by theoretical models.     

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.     

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.     

Daily body mass regulation in dominance-structured coal tit (Parus ater) flocks in response to variable food access: a laboratory study

In a dominance-structured flock, social status may determinepriority of access to food. Birds of low social status mayperceive present and future access to food as less predictable,and so have a higher risk of starvation, than birds of highsocial rank. Theoretical models predict that subordinate birdsshould carry larger fat reserves and incur higher mass-dependentcosts than dominants. However, empirical tests of the assumptionsof these models are still scarce and controversial. We investigatedthe effect of dominance rank on daily mass gain under conditionsof fluctuating food availability in a laboratory experimentusing four flocks of four coal tits (Parus ater) each. Thesame amount of food was delivered in two treatments, but inone treatment the food was offered at a constant rate betweendays (fixed treatment), while in the other treatment the dailyfood supply varied in an unpredictable sequence between days(variable treatment). All birds showed greater variance inbody mass in the variable treatment than in the fixed treatment.Body mass within birds showed the same variability at dawn thanat dusk in the fixed treatment, but less variability at dawnthan at dusk in the variable treatment. This may be a mechanismto reduce the immediate risk of starvation at the beginningof the day, when fat reserves are at their lowest and the aggressionbetween flock members when feeding highest. Subordinate birdswere excluded from the feeders by dominants more often in theearly morning than in the rest of the day, and they showedmore variability in daily mass gain and body mass at dawn thandominant birds. These results support the hypothesis that subordinatebirds have a reduced probability of surviving when food availabilitychanges unexpectedly compared to dominants.     

Avian daily foraging patterns: Effects of digestive constraints and variability

Summary Birds show a typical daily pattern of heavy morning and secondary afternoon feeding. We investigate the pattern of foraging by a bird that results in the lowest long-term rate of mortality. We assume the following: mortality is the sum of starvation and predation. The bird is characterized by two state variables, its energy reserves and the amount of food in its stomach. Starvation occurs during the day if the bird's reserves fall to zero. The bird starves during the night if the total energy stored in reserves and the stomach is less than a critical amount. The probability that the bird is killed by a predator is higher if the bird is foraging than if it is resting. Furthermore, the predation risk while foraging increases with the bird's mass. From these assumptions, we use dynamic programming techniques to find the daily foraging routine that minimizes mortality. The principal results are (1) Variability in food finding leads to routines with feeding concentrated early in the day, (2) digestive constraints cause feeding to be spread more evenly through the day, (3) even under fairly severe digestive constraints, the stomach is generally not full and (4) optimal fat reserve levels are higher in more variable environments and under digestive constraints. This model suggests that the characteristic daily feeding pattern of small birds is not due to digestive constraints but is greatly influenced by environmental variability.     

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.     

Great tits take greater risk toward humans and sparrowhawks in urban habitats than in forests

Urban animals often take more risk toward humans than their non‐urban conspecifics do, but it is unclear how urbanization affects behavior toward non‐human predators. Responses to humans and non‐human predators may covary due to common mechanisms enforcing a phenotypic correlation. However, while increased tolerance toward humans may be advantageous for urban animals, reduced vigilance toward non‐human predators that can pose actual threat may be costly. Therefore, urban animals may benefit from showing specific responses to different threat levels, such as humans versus non‐human predators, or hostile versus non‐hostile humans. To test these alternatives, we compared responses (latencies to return to nest) of urban and forest‐breeding great tits (Parus major) to familiar hostile and unfamiliar humans as well as one of their common predators, the sparrowhawk (Accipiter nisus). We found that urban birds were more risk‐taking toward both humans and sparrowhawk than forest birds. However, responses to sparrowhawk did not correlate with responses to humans either within or across habitats. This suggests that higher risk‐taking of urban compared to forest‐dwelling great tits toward sparrowhawk may be threat‐specific response to lower predation risk rather than a spillover effect of increased tolerance to humans. Furthermore, birds responded similarly to unfamiliar and familiar (potentially dangerous) humans in both habitats, suggesting that great tits may not adjust their risk‐taking to the threat represented by individual humans. These findings indicate that urban birds may flexibly adjust their risk‐taking to certain, but not all, types of threat.