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.     

Plasticity of parental care under the risk of predation: how much should parents reduce care?

Predation can be an important agent of natural selection shaping parental care behaviours, and can also favour behavioural plasticity. Parent birds often decrease the rate that they visit the nest to provision offspring when perceived risk is high. Yet, the plasticity of such responses may differ among species as a function of either their relative risk of predation, or the mean rate of provisioning. Here, we report parental provisioning responses to experimental increases in the perceived risk of predation. We tested responses of 10 species of bird in north temperate Arizona and subtropical Argentina that differed in their ambient risk of predation. All species decreased provisioning rates in response to the nest predator but not to a control. However, provisioning rates decreased more in species that had greater ambient risk of predation on natural nests. These results support theoretical predictions that the extent of plasticity of a trait that is sensitive to nest predation risk should vary among species in accordance with predation risk.     

Strategic Regulation of Body Mass and Singing Behavior in New Zealand Robins

The ‘small bird in winter’ paradigm states that body mass is a balance between the conflicting demands of carrying enough energy to survive nightly fasts while minimizing the risk of predation associated with carrying additional fat reserves. We conducted a short‐term food‐supplementation experiment during which New Zealand robins (Petroica australis) were provided with food on the second day of a 3‐d trial. This allowed us to test two predictions from models of strategic mass regulation in small birds: (1) individual birds reach the same end‐of‐day mass despite differences in their initial morning mass while, (2) using surplus energy for increased singing. As expected, robins gained mass at a higher rate early in the morning on the fed day than they did on either of the two control days, but there was no significant difference in their evening masses across the 3 d of the experiment despite birds on day 3 starting at higher initial masses than birds on day 1. Robins displayed a significantly higher rate of singing when receiving food supplements on day 2, supporting a link between energetic reserves and behavior. Our results suggest that potentially energetically costly behaviors, such as song production, are sensitive to short‐term changes in energy reserves, and that both state and behavioral predictions can be successfully integrated to provide tests of state‐based models of behavior.     

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.     

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.     

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.     

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.     

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.     

Effects of predation risk on diurnal mass dynamics and foraging routines of yellowhammers (Emberiza citrinella)

Theoretical models predict that when having fat reserves iscostly in terms of predation risk, birds should decrease theirlevels of fat reserves in response to increased predation risk.I performed an experiment in which yellowhammers were exposedto a control treatment, where a curtain was moved several timesa day, 5 days in a row, and then to a predator treatment, where aperched, stuffed sparrowhawk appeared when the curtain was moved,5 days in a row. Between the two treatments were 2 days withoutany experimental treatment. The birds were expected to decreasein mass, and/or to change the daily trajectory of mass increasein response to increased predation risk. Yellowhammers decreasedin morning mass and evening mass in response to both the movingcurtain and the sparrowhawk compared to an untreated day beforethe start of the experiment. However, the response to both treatmentswas not the same; in the sparrowhawk treatment the birds waitedlonger before resuming feeding and lost more weight after eachexposure as compared to the curtain treatment. This loss wasregained, and yellowhammers increased their intake rate. Dueto that, they reduced, although not significantly, the timespent feeding under predation risk. A reduction in the timespent feeding under predation risk reduces the time exposedto predators. However, if an increase in intake rate also incursa decrease in vigilance, this might increase predation risk.The results of this study, together with other studies, indicatethat for yellowhammers a reduction in time exposed to predatorsmight be more important for survival than a reduction in bodymass.     

A dynamic model of hypothermia as an adaptive response by small birds to winter conditions

We present a dynamic programming model which is used to investigate hypothermia as an adaptive response by small passerine birds in winter. The model predicts that there is a threshold function of reserves during the night, below which it is optimal to enter hypothermia, and above which it is optimal to rest. This threshold function decreases during the night, with a particularly sharp drop at the end of the night, representing the time and energy costs associated with returning to normal body temperature. The results of the model emphasise the trade-off between energy and predation, not just between foraging options, but also between foraging during the day and entering hypothermia at night. The value of being able to use hypothermia represents not just energy savings, but also reduced predation risk due to changes in the optimal foraging strategy. Conditions which give a high value of hypothermia are short photoperiod, variable food supply, low temperatures, poor and scarce food supplies.     

Climate change and the optimal arrival of migratory birds

Recent climate change has sparked an interest in the timing of biological events, which is a general problem in life-history evolution. Reproduction in many organisms breeding in seasonal environments, e.g. migratory birds, is dependent on the exploitation of a short but rich food supply. If the seasonal timing of the food peak advances owing to climate change, then one would expect the bird to track those changes, hence, initiate migration and breeding earlier. However, when there is competition for territories and a risk of pre-breeding mortality, the optimal response to a shifting food distribution is no longer obvious. We develop a theoretical model to study how the optimal arrival time depends on the mean and variance of the food distribution, the degree of competition for territories and the risk of mortality. In general, the optimal shift in arrival date should never be as extreme as the shift in food peak date. Our results also show that we should expect the high variation of trends in arrival date observed among migratory birds, even if migration and information about climate change were unconstrained.     

Theoretical models of adaptive energy management in small wintering birds

Many small passerines are resident in forests with very cold winters. Considering their size and the adverse conditions, this is a remarkable feat that requires optimal energy management in several respects, for example regulation of body fat reserves, food hoarding and night-time hypothermia. Besides their beneficial effect on survival, these behaviours also entail various costs. The scenario is complex with many potentially important factors, and this has made 'the little bird in winter' a popular topic for theoretic modellers. Many predictions could have been made intuitively, but models have been especially important when many factors interact. Predictions that hardly could have been made without models include: (i) the minimum mortality occurs at the fat level where the marginal values of starvation risk and predation risk are equal; (ii) starvation risk may also decrease when food requirement increases; (iii) mortality from starvation may correlate positively with fat reserves; (iv) the existence of food stores can increase fitness substantially even if the food is not eaten; (v) environmental changes may induce increases or decreases in the level of reserves depending on whether changes are temporary or permanent; and (vi) hoarding can also evolve under seemingly group-selectionistic conditions.     

Migrants in tropical bird communities: the balanced breeding limitation hypothesis

Explanations for the ecological integration of migratory and non-migratory (resident) insectivorous birds in the tropics have been complicated by the paradox that arthropod abundances are low when bird abundances reach their annual peak. The breeding currency hypothesis and the nest predation hypothesis both account for this paradox by postulating that residents are held below the non-breeding season carrying capacity, which frees resources available for migratory insectivores. The breeding currency hypothesis suggests residents are limited by food suitable for nestlings, whereas the nest predation hypothesis emphasizes the primacy of high rates of nest predation. However, theoretical arguments suggest that food availability and predation risk interact strongly to limit breeding birds. We use graphical analyses to extend the breeding currency hypothesis to incorporate effects of nest predation. This yields a more synthetic and realistic model for the integration of migrant and resident insectivores in the tropics – the balanced breeding limitation hypothesis.     

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.     

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.      

Sex‐Specific Parental Care in Response to Predation Risk in the European Roller,Coracias garrulus

Sublethal effects of predation constitute an important part of predation effects, which may modulate prey population and community dynamics. In birds, the risk of nest predation may cause a reduction in parental activity in the care of offspring to reduce the chance of being detected by predators. In addition, parents may modify their parental food allocation preferences within the brood in response to predation risk. Our aim in this study was to evaluate the effects of risk of nest predation on parental care and within‐nest food allocation in the European Roller (Coracias garrulus), an asynchronously hatching bird. We manipulated brood predation risk by placing a snake model near the nests that simulates the most common nest predator in the Mediterranean region. Our results show that males but not females increased their provisioning rate when they were exposed to the model and that despite this, nestlings’ body mass decreased in response to this temporary increase in predation risk. We did not find evidence that parents changed their food allocation strategy towards senior or junior nestlings in their nests in response to predation risk. These results show that the European roller modifies parental care in response to their perception of predation risk in the nest and a sex‐specific sensitivity to the threat, which suggests a different perception of offspring reproductive value by parents. Finally, our results show that changes in parental behaviour in response to nest predation risk might have consequences for nestling fitness prospects.     

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.     

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.     

Credit or debit? Resource input changes population dynamics of city-slicker birds

The underlying evolutionary mechanisms of urban bird populations have hardly been studied. High food density and low predation risk serve to explain the global pattern of extremely high urban bird population densities. Both these bottom-up and top-down effects are paradoxical since the per capita amount of food is small due to competition, and domestic predator density is high in cities. The bottom-up paradox can be resolved by taking into account the high food resource-predictability in cities. Concerning the top-down effect, recent studies suggest that at least when it comes to nest predation the effect of cats is minor. I suggest that the combination of high food predictability and low predation risk in cities alter bird foraging behaviour, which in turn affects population dynamics. In terms of density, the result is that bird populations exceed the carrying capacity of the urban environment, costing heavily on body condition and/or life span. Under such conditions the population should consist of a few winners and many losers. Only the winners have sufficient access to food resources and the opportunity to reproduce. The highly predictable continuous input of food in the urban environment allows them to "live on their credit". They may trade off between offspring body condition and clutch size. In the lack of predation, the losers among the fledglings may survive for a relatively long period, getting just enough energy to survive. Though they may never become healthy enough to reproduce, they will have a major contribution to the observed population density. Results of several case studies seem to support the credit card hypothesis and suggest that it can serve as a general rule for the evolution of animal populations and communities in highly predictable human managed environments.     

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.