Optimal diving under the risk of predation

Many air-breathing aquatic foragers may be killed by aerial or subsurface predators while recovering oxygen at the surface; yet the influence of predation risk on time allocation during dive cycles is little known in spite of numerous studies on optimal diving. We modeled diving behavior under the risk of predation at the surface. The relationship between time spent at the surface and the risk of death is predicted to influence the optimal surface interval, regardless of whether foragers accumulate energy at a constant rate while at the food patch, deplete food resources over the course of the dive, or must search for food during the dive. When instantaneous predation risk during a single surface interval decreases with time spent at the surface, a diver should increase its surface interval relative to that which maximizes energy intake, thereby increasing dive durations and reducing the number of surfacings per foraging bout. When instantaneous risk over a single surface interval does not change or increases with increasing time at the surface, divers should decrease their surface interval (and consequently their dive duration) relative to that which maximizes energy intake resulting in more dives per foraging bout. The fitness consequences of selecting a suboptimal surface interval vary with the risk function and the way divers harvest energy when at depth. Finally, predation risk during surface intervals should have important consequences for habitat selection and other aspects of the behavioral ecology of air-breathing aquatic organisms.     

Energy,predators and the behavior of feeding hummingbirds

Summary Current evidence suggests that many animals trade off energy gain against the risk of predation while feeding. In contrast, energetic considerations alone have proven successful in explaining and predicting the behaviour of feeding hummingbirds. This success may reflect the relative lack of natural predation on hummingbirds, but this study suggests that it may additionally reflect the lack of studies taking a predation perspective. In particular, when Anna's hummingbirds (Calypte anna) are faced with an obstructed view of their surroundings, they engage in behaviour suggestive of anti-predatory vigilance. In doing so, they voluntarily reduce their rate of energy intake. These birds also forgo better feeding opportunities that occur close to the ground, where observations suggest they are wary of opportunistic predators such as roadrunners (Geococcys californianus). While energy-based concepts will remain useful in the study of hummingbird feeding behaviour, the lack of predation on these birds should not be equated with an insensitivity to the risk of predation. This realization may lead to further insights into hummingbird-plant interactions, and hummingbird biology in general.     

Predator‐induced modifications to diving behavior vary with foraging mode

Breath‐hold divers are strongly interacting species whose top–down influence on aquatic communities is shaped by factors governing their diving decisions. Although some of these factors (e.g. physiological constraints, energetic needs) have been scrutinized, the possibility that predation risk influences diving behavior has been largely overlooked, and no study to date has asked if anti‐predator responses by divers depend on foraging mode. We contrasted dive cycle changes by herbivorous dugongs Dugong dugon using two foraging tactics – cropping, which always permits anti‐predator vigilance, and excavation, which limits surveillance at depth – in response to temporal variation in tiger shark Galeocerdo cuvier abundance. Dugongs responded to increasing shark abundance (one component of predation risk) by diving more frequently without changing their surface times and thereby spending a greater proportion of time at the surface, but only while excavating. When threatened, in other words, excavating dugongs sacrificed foraging time at depth to facilitate shark detection. In contrast, cropping dugongs at risk from sharks were able to continue diving and foraging normally. By implication, future studies should consider the influence of predation risk on diving decisions, even by large‐bodied species, and the possibility that behavioral responses by divers to predators may vary with foraging mode.     

The influence of temperature on diving behaviour in the alpine newt, Triturus alpestris

An aquatic lifestyle poses serious restriction to air-breathing animals in terms of time and energy spent during a dive cycle. The diving frequency increases with water temperature, therefore an ectotherm's time budget greatly depends on the thermal characteristics of the aquatic environment. Available data suggests that time costs caused by temperature-dependent dive frequency can be partially compensated for by adjusting the swimming speed and diving angle during dive cycle. We tested this prediction by examining the influence of temperature on the diving behaviour of the alpine newt, Triturus alpestris. The ascending speed and angle showed disparate patterns of temperature dependency, with a minor influence on travel duration. Surprisingly, at higher temperatures, the diving newts saved most of their time by restricting swimming activity in the water column during their return to the bottom and not by adjusting their ascending duration. Hence, aquatic newts have the capacity to reduce temperature-dependent time costs of aerial breathing primarily by behavioural modifications during the descending phase of the dive cycle.     

Higher nest predation risk in association with a top predator: mesopredator attraction?

Breeding close to top predators is a widespread reproductive strategy. Breeding animals may gain indirect benefits if proximity to top predators results in a reduction of predation due to suppression of mesopredators. We tested if passerine birds gain protection from mesopredators by nesting within territories of a top predator, the Ural owl (Strix uralensis). We placed nest boxes for pied flycatchers (Ficedula hypoleuca) in Ural owl nest sites and in control sites (currently unoccupied by owls). The nest boxes were designed so that nest predation risk could be altered (experimentally increased) after flycatcher settlement; we considered predation rate as a proxy of mesopredator abundance. Overall, we found higher nest predation rates in treatment than in control sites. Flycatcher laying date did not differ between sites, but smaller clutches were laid in treatment sites compared to controls, suggesting a response to perceived predation risk. Relative nest predation rate varied between years, being higher in owl nest sites in 2 years but similar in another; this variation might be indirectly influenced by vole abundance. Proximity to Ural owl nests might represent a risky habitat for passerines. High predation rates within owl territories could be because small mesopredators that do not directly threaten owl nests are attracted to owl nest sites. This could be explained if some mesopredators use owl territories to gain protection from their own predators, or if top predators and mesopredators independently seek similar habitats.     

A thorough and quantified method for classifying seabird diving behaviour

Time-depth recorders are commonly deployed on diving animals to obtain information on their aquatic behaviour. The recorded data provide a 2D profile of diving activity. As analyses of diving behaviour from such profiles have become more complex, these analyses have often suffered from a lack of consistency and rigour. There is a growing need for a simple, comparative method to classify diving behaviour thoroughly and quantitatively. Here, a new approach to the classification of the dive profiles of penguins is described, which probably has applicability for many other diving predators as well. This simple approach uses a small, coherent set of criteria to classify behaviours in a detailed and quantified manner, and with relative objectivity. Classification of diving behaviour is possible from the temporal scale of a wiggle within a dive to the scale of a bout of dives. The new method will make comparisons between species easier and clearer because these comparisons will be undertaken within a consistent, more objective framework.     

Sex differences in the diving behaviour of a size-dimorphic capital breeder: the grey seal

Both body size dimorphism and sex differences in the relative costs and benefits associated with acquiring energy for reproduction have been advanced to explain the evolution of sex differences in foraging behaviour. We examined the extent to which these factors influenced sex differences in the diving behaviour of a size-dimorphic, capital breeder, the grey seal, Halichoerus grypus. Using time-depth data loggers, we examined the diving behaviour of 46 male and 49 female grey seals for 7 months before parturition and mating. Males and females showed significantly different seasonal patterns in the characteristics of individual dives and dive effort. Compared with males, females showed significantly higher levels of dive effort immediately following moult and in the 3 months before parturition. Females also had longer dives (5.5 versus 4.9 min) and spent more time at depth (3.4 versus 2.7 min), whereas males dived deeper (57 versus 49 m). Males dived consistently throughout the day, whereas females showed strong diurnal patterns in dive depth, duration and frequency. The diving behaviour and rates of mass gain by females suggested a pattern of foraging consistent with early accumulation of body energy to support pregnancy and the subsequent lactation period during which females fast. Males, on the other hand, showed diving behaviour and rates of mass gain consistent with a more gradual accumulation of energy stores. Our results suggest that sex differences in the seasonal patterns of diving behaviour reflect sex differences in the costs and benefits of stored energy for reproduction rather than the influence of body size dimorphism alone.     

The optimal allocation of time and respiratory metabolism over the dive cycle

Because anaerobic metabolism is much less efficient than aerobicmetabolism in supplying energy, it is widely believed that diversrely predominantly on aerobic metabolism for diving. In thispaper, a time budget model, which assumes that the diver canuse either completely aerobic or partially aerobic metabolismwith additional anaerobic metabolism for diving, is developedand is used to make predictions about patterns in optimal allocationof time and respiratory metabolism during the dive cycle. Theresults derived from the model are (1) a diver that can varythe ratio of energy supplied anaerobically to total energy spentduring dive time is favored by natural selection, but the patternsof time allocation over the dive cycle by the diver do not differ fromthose of a diver that cannot vary the ratio. (2) Even if itis assumed that divers switch their metabolism for diving, anobvious upturn in the surface time with respect to dive timedoes not occur at the aerobic dive limit (ADL) but occurs beyondthe ADL. (3) Use of additional anaerobic metabolism can be favoredfor dives shorter than the ADL. These findings provide a usefulguide to understanding the factors that limit diving behavior.     

Water temperature sampling by foraging Brünnich's Guillemots with bird-borne data loggers

We describe the features of waters where seabirds were feeding by sampling vertical water temperature profiles with data loggers mounted on five Brünnich's Guillemots in Svalbard, Norway. The guillemots foraged in a cold water (−0.5–0.5°C SST (sea surface temperature)) by making 1.8 dive bouts in short trips (32–257 min duration) as well as in moderate (0.5–2.0°C SST) and warm waters (2.5–4.0°C SST) by making 6.0 dive bouts during long trips (411–688 min duration). Judging from outbound flying time (15.7–24.4 min), time between dive bouts (23.9–43.3 min) and water types, the birds probably fed in fjord or coastal waters during short trips and in both coastal and offshore waters during long trips. Water temperature and diving behaviour can be simultaneously recorded by small data loggers, which therefore will provide useful information on marine features and foraging activity of top predators.     

Alternative Responses to Predation in Two Headwater Stream Minnows Is Reflected in Their Contrasting Diel Activity Patterns

Animals exhibit diel periodicity in their activity in part to meet energy requirements whilst evading predation. A competing hypothesis suggests that partitioning of diel activities is less important because animals capitalise on opportunity. To test these hypotheses we examined the diel activity patterns for two cyprinid minnows, chubbyhead barb Barbus anoplus and the Eastern Cape redfin minnow Pseudobarbus afer that both occur within headwater streams in the Eastern Cape, South Africa. Chubbyhead barbs exhibited consistent nocturnal activity based on both field and laboratory observations. Due to the absence of fish predators within its habitat, its nocturnal behaviour suggests a response to the cost associated with diurnal activity, such as predation risk by diving and wading birds. In contrast, redfin minnows showed high diurnal activity and a shoaling behaviour in the wild, whereas, in the laboratory, they showed high refuge use during the diel cycle. Despite their preference for refuge in the laboratory, they were diurnally active, a behaviour that was consistent with observations in the wild. The diurnal activity of this species suggests a response to the cost associated with nocturnal activity. Such a cost could be inferred from the presence of the longfin eel, a native predator that was active at night, whereas the daytime shoaling behaviour suggests an anti-predator mechanism to diurnal visual predators. The implications of these findings relate to the impacts associated with the potential invasions by non-native piscivores that occur in the mainstem sections. Diurnal activity patterns for redfin minnows, that are IUCN-listed as endangered, may, in part, explain their susceptibility to high predation by visual non-native piscivores, such as bass and trout. In contrast, the nocturnal habits of chubbyhead barbs suggest a probable pre-adaptation to visual predation. The likelihood of invasion by nocturnally-active sharptooth catfish Clarias gariepinus, however, may compromise this prior advantage.     

Optimal diving behaviour for foraging in relation to body size

Overall, large animals dive longer and deeper than small animals; however, after the difference in body size is taken into account, smaller divers often tend to make relatively longer dives. Neither physiological nor theoretical explanations have been provided for this paradox. This paper develops an optimal foraging diving model to demonstrate the effect of body size on diving behaviour, and discusses optimal diving behaviour in relation to body size. The general features of the results are: (1) smaller divers should rely more heavily on anaerobic respiration, (2) larger divers should not always make longer dives than smaller divers, and (3) an optimal body size exists for each diving depth. These results explain the relatively greater diving ability observed in smaller divers, and suggest that if the vertical distribution of prey in the water column is patchy, there is opportunity for a population of diving animals to occupy habitat niches related to body size.     

Theory and method in studies of vigilance and aggregation

Predation is considered one of the most important selective pressures on free-ranging animals. Our understanding of it derives mainly from studies of individual vigilance (visual scanning of the surroundings beyond the immediate vicinity) and aggregation in prey. Vigilance bears a direct relationship to aggregation, because animals in groups may rely on associates for early warning of danger. This review addresses the relationship between vigilance and aggregation with particular attention to the prediction that individual vigilance declines with increasing group size. Contrary to most other animals studied, primates do not support the prediction. Exploring this, I examined the assumptions underlying vigilance theory in the light of primate behaviour. First I tested whether manual harvesting and upright processing of food as seen among primates might permit them to feed and scan simultaneously. I found no support for this idea. Next I examined the targets of primate vigilance and found that one component (within-group vigilance) might explain the differences between primates and other animals. Finally, I evaluated whether individual primates in large groups face a lower risk of predation than those in small groups. A conclusion was impossible, but by separating group-level from individual-level risk, I was able to identify several common circumstances in which group size would not predict individual risk or vigilance. These circumstances arose for primates and nonprimates alike. I concluded that the relationship of vigilance to aggregation is not straightforward. The absence of a group-size effect on vigilance among primates is probably due to functional differences in vigilance behaviour or safety in groups, not to methodological differences. Furthermore, future work on animal vigilance and aggregation must fully consider both the targets of glances, and the assumption that larger groups are safer from predators. I predict that animals will not relax vigilance in larger groups if conspecific threat increases with group size. Group size will not predict individual risk of predation nor individual vigilance rates when predators do not rely on surprise, or when predators select a small subset of highly vulnerable group members. Copyright 2000 The Association for the Study of Animal Behaviour.     

Characterization of postdive recovery using sound recordings and its relationship to dive duration,exertion, and foraging effort of southern elephant seals (Mirounga leonina)

It is notoriously difficult to measure physiological parameters in cryptic free‐ranging marine mammals. However, it is critical to understand how marine mammals manage their energy expenditure and their diving behavior in environments where the predation risks are low and where survival is mainly linked to capacities to maintain physiological homeostasis and energy budget balance. Elephant seals are top marine predators that dive deeply and continuously when at sea. Using acoustic recorders deployed on two postbreeding southern elephant seals (SES) females, we developed methods to automatically estimate breathing frequency at the surface. Using this method, we found that seals took successive identical breaths at high frequency (0.29 Hz) when recovering at the surface and that breath count was strongly related to postdive surfacing time. In addition, dive depth was the main factor explaining surfacing time through the effects of dive duration and total underwater swimming effort exerted. Finally, we found that recovery does not only occur over one dive timescale, but over a multidive time scale for one individual. The way these predators manage their recovery will determine how they respond to the change in oceanic water column structure in the future.     

No shallow talk: Cryptic strategy in the vocal communication of Blainville's beaked whales

Communicating animals must balance fitness benefits against the costs of signaling, such as increased predation risk. Cetaceans communicate mainly with sound and near‐surface vocalizations can place signalers at risk from shallow‐diving top‐predators with acute hearing such as killer whales. Beaked whales are deep divers living in small cohesive groups with little social defense from predation. Little if anything is known about their acoustic communication. Here, eight Blainville's beaked whales were studied with suction cup attached DTags to provide the first report on social communication as a function of diving behavior for any of the 21 ziphiid species. Tagged whales produced two previously unrecorded signals with apparent communicative functions: (1) fast series of ultrasonic frequency modulated clicks (rasps) were recorded from six individuals, and (2) harmonically rich short whistles with a mean fundamental frequency of 12 kHz were recorded from one whale at up to 900 m depth, the deepest whistles recorded from a marine mammal. Blainville's were silent 80% of the time, whenever shallower than 170 m depth and during the prolonged (19 min) silent ascents from vocal dives. This behavior limits the ability of shallow‐diving predators to track Blainville's acoustically and may provide a striking example of the evolutionary influence of the risk of predation on animal communication.     

Introduced mammalian predators induce behavioural changes in parental care in an endemic New Zealand bird

The introduction of predatory mammals to oceanic islands has led to the extinction of many endemic birds. Although introduced predators should favour changes that reduce predation risk in surviving bird species, the ability of island birds to respond to such novel changes remains unstudied. We tested whether novel predation risk imposed by introduced mammalian predators has altered the parental behaviour of the endemic New Zealand bellbird (Anthornis melanura). We examined parental behaviour of bellbirds at three woodland sites in New Zealand that differed in predation risk: 1) a mainland site with exotic predators present (high predation risk), 2) a mainland site with exotic predators experimentally removed (low risk recently) and, 3) an off-shore island where exotic predators were never introduced (low risk always). We also compared parental behaviour of bellbirds with two closely related Tasmanian honeyeaters (Phylidonyris spp.) that evolved with native nest predators (high risk always). Increased nest predation risk has been postulated to favour reduced parental activity, and we tested whether island bellbirds responded to variation in predation risk. We found that females spent more time on the nest per incubating bout with increased risk of predation, a strategy that minimised activity at the nest during incubation. Parental activity during the nestling period, measured as number of feeding visits/hr, also decreased with increasing nest predation risk across sites, and was lowest among the honeyeaters in Tasmania that evolved with native predators. These results demonstrate that some island birds are able to respond to increased risk of predation by novel predators in ways that appear adaptive. We suggest that conservation efforts may be more effective if they take advantage of the ability of island birds to respond to novel predators, especially when the elimination of exotic predators is not possible.     

Breeding suppression in the bank vole as antipredatory adaptation in a predictable environment

Summary In northern Fennoscandia, microtine rodent populations fluctuate cyclically. The environment of an individual vole can be considered to be predictable when the risks of predation and intra- and interspecific competition change with the cycle, such that both are high during the population highs of voles. The risk of predation is also high during the vole crash. After the crash, the vole population is characterized by low intra- and interspecific competition and low predation pressure. The main predators affecting voles during the crash are the small mustelids, least weasel and stoat. The density of these specialist predators declines drastically during the winter after the vole crash. We studied experimentally the impact of the perceived presence of stoats on the breeding and mating behaviour of voles. In a series of breeding experiments with bank voles,Clethrionomys glareolus, both old and young females suppressed breeding when exposed to the odour of stoats,Mustela erminea. The weights of females decreased in both experimental and control groups, but more among the voles under odour exposition. It seems that females actively avoided copulations under high predation risk and that breeding suppression is mediated by a change in female mating behaviour. There was no change in male behaviour or physical condition between the experimental and control treatments. An alternative mechanism for the observed breeding suppression could be the one caused by decreased feeding in females mediated with low energy intake which does not allow breeding. Regardless of its mechanism, delay of breeding should increase the probability of non-breeding females to survive to the next breeding season. The females surviving the crash should gain a strong selective advantage in a predator-free environment of the subsequent breeding season, which could explain the adaptive function of this antipredatory strategy.     

REDUCTIONS IN OXYGEN CONSUMPTION DURING DIVES AND ESTIMATED SUBMERGENCE LIMITATIONS OF STELLER SEA LIONS (EUMETOPIAS JUBATUS)

Accurate estimates of diving metabolic rate are central to assessing the energy needs of marine mammals. To circumvent some of the limitations inherent with conducting energy studies in both the wild and captivity, we measured diving oxygen consumption of two trained Steller sea lions ( Eumetopias jubatus ) in the open ocean. The animals dived to predetermined depths (5–30 m) for controlled periods of time (50–200 s). Rates of oxygen consumption were measured using open-circuit respirometry before and after each dive. Mean resting rates of oxygen consumption prior to the dives were 1.34 (±0.18) and 1.95 (±0.19) liter/min for individual sea lions. Mean rates of oxygen consumption during the dives were 0.71 (±0.24) and 1.10 (±0.39) liter/min, respectively. Overall, rates of oxygen consumption during dives were significantly lower (45% and 41%) than the corresponding rates measured before dives. These results provide the first estimates of diving oxygen consumption rate for Steller sea lions and show that this species can exhibit a marked decrease in oxygen consumption relative to surface rates while submerged. This has important consequences in the evaluation of physiological limitations associated with diving such as dive duration and subsequent interpretations of diving behavior in the wild.     

An application of optimal diving models to diving behaviour of Brünnich's guillemots

Although theoretical models predict that the quality of foraging patches has little effect on optimal dive time with increasing depth, many empirical studies show that dive time at a given depth may vary. We developed a model that incorporated patch quality as a parameter of energy intake as a nonlinear function of time, and applied it to the diving behaviour of Brünnich's guillemots, Uria lomvia. The model indicated that optimal dive time can vary widely depending on the parameter. It also explained the convergence of observed dive times with travel time. Assuming the birds dived optimally, this parameter can be estimated from travel time and dive time for each dive. Foraging patches with larger estimated parameter values were favoured by the birds, suggesting that the parameter indicated patch quality. We used this parameter to test an optimal patch use model in divers. The results indicate that Brünnich's guillemots adjust their diving behaviour adaptively depending on patch quality, and that the optimal diving model is valid for prediction of observed dive patterns if patch quality is incorporated appropriately. Copyright 2002 The Association for the Study of Animal Behaviour. Published by Elsevier Science Ltd. All rights reserved.     

Deep-diving foraging behaviour of sperm whales (Physeter macrocephalus)

1. Digital tags were used to describe diving and vocal behaviour of sperm whales during 198 complete and partial foraging dives made by 37 individual sperm whales in the Atlantic Ocean, the Gulf of Mexico and the Ligurian Sea. 2. The maximum depth of dive averaged by individual differed across the three regions and was 985 m (SD = 124.3), 644 m (123.4) and 827 m (60.3), respectively. An average dive cycle consisted of a 45 min (6.3) dive with a 9 min (3.0) surface interval, with no significant differences among regions. On average, whales spent greater than 72% of their time in foraging dive cycles. 3. Whales produced regular clicks for 81% (4.1) of a dive and 64% (14.6) of the descent phase. The occurrence of buzz vocalizations (also called 'creaks') as an indicator of the foraging phase of a dive showed no difference in mean prey capture attempts per dive between regions [18 buzzes/dive (7.6)]. Sperm whales descended a mean of 392 m (144) from the start of regular clicking to the first buzz, which supports the hypothesis that regular clicks function as a long-range biosonar. 4. There were no significant differences in the duration of the foraging phase [28 min (6.0)] or percentage of the dive duration in the foraging phase [62% (7.3)] between the three regions, with an overall average proportion of time spent actively encountering prey during dive cycles of 0.53 (0.05). Whales maintained their time in the foraging phase by decreasing transit time for deeper foraging dives. 5. Similarity in foraging behaviour in the three regions and high diving efficiencies suggest that the success of sperm whales as mesopelagic predators is due in part to long-range echolocation of deep prey patches, efficient locomotion and a large aerobic capacity during diving.     

Do shark declines create fear‐released systems?

We illustrate the theoretical plausibility that fishery removal of sharks can indirectly alter predation pressure on different fish species via the behavioural responses of mesoconsumers released from predator intimidation. Our dynamic state variable model of foraging decisions by harbour seals, a mesopredator, predicted indirect effects of the removal of Pacific sleeper sharks on two species consumed by seals, Pacific herring and walleye pollock, as mediated by seal behaviour. Herring, a fatty fish, form near‐surface aggregations that often are ephemeral and widely dispersed. Pollock are found in the deeper strata preferred by sharks and have lower energy density than herring, but also are larger and their more continuous distribution potentially makes them the more predictable resource for seals. During simulations, predation risk from sharks produced an asymmetric trophic cascade mediated by the seal's underutilisation of deeper, riskier strata. Risk management by seals reduced mortality on pollock, which required riskier access in deep strata, while increasing mortality on herring, which could be accessed with less risk in shallow strata. This effect, however, attenuated if herring were scarcer and seal energy state was poor. During shark removal scenarios, seals shifted to deeper strata, increasing pollock consumption and substantially decreasing use of herring; the proportional change was greatest if seals were in good energy state. Prior studies have addressed how shark declines might affect community structure through density responses by species consumed by sharks; earlier models incorporating antipredator behaviour of the mesopredator (i.e. Ecosim/Ecospace) allow for activity reduction but not for the spatial shifts that altered the asymmetric trophic cascade in our simulations. Our results suggest that shark declines might have stronger ecological consequences than previously recognised if we account for spatial and diet shifts by mesoconsumers released from shark intimidation.