The effect of time and digestion constraints in Common Eiders while feeding and diving over Blue Mussel beds

1. To maintain energy intake Common Eiders ( Somateria mollissima ) in winter should compensate for reduced day-length by increasing both the proportion of time spent feeding and diving efficiency, defined as the proportional duration of a dive bout within a dive cycle. Common Eiders swallowed Blue Mussel ( Mytilus edulis ) whole with their shells where any behavioural compensation in relation to short days may be limited by digestive processes.
2. Based on time budget studies conducted from mid-December to the end of April in the Gulf of St. Lawrence, Québec, Canada, diving and feeding efficiency were compared for three seasonal periods varying in day-length (from 557 to 890 min).
3. Results showed that eiders were compensating for short days by feeding 56% of the time in mid-winter compared with 33% in spring. However, diving efficiency remained constant through the season and apparently no compensation occurred at this level of their foraging behaviour. Despite this, the daily rate of prey ingestion was much higher in mid-winter than in spring.
4. Ingestion rate values for mid-winter individuals approached or even exceeded the rate at which prey items are defecated and it was concluded that shell crushing performed by the muscular gizzard is physiologically more demanding during that period. On this basis, gizzard mass should be larger in winter when ingestion rates are higher. Data presented support that hypothesis and suggest that compensation in relation to short days can be both behavioural and physiological.     

Lunar cycles in diel prey migrations exert a stronger effect on the diving of juveniles than adult Galápagos fur seals.

In our study of the development of diving in Galápagos fur seals, we analysed changes in diving activity and body mass trends over the lunar cycle. Based on previously observed lunar cycles in colony attendance patterns, we hypothesized a greater impact of prey migrations of deep scattering layer organisms on younger fur seals. Using electronic dive recorders, we determined that seals dived less and deeper on moonlit nights than at new moon, and incurred body mass losses. These changes in foraging over the lunar cycle correlate with the suppression of the vertical migration of prey by lunar light. All effects were more pronounced in juveniles than adult females, with greater relative mass loss during full moon, which must (i) negatively affect long-term juvenile growth rates, (ii) lengthen periods of maternal dependence, and (iii) contribute to the lowest reproductive rate reported for seals. This underlines the importance of studying ontogeny in order to understand life histories, and for determining the susceptibility of animal populations to fluctuations in food availability.     

Evolutionary models of metabolism, behaviour and personality

I explore the relationship between metabolism and personality by establishing how selection acts on metabolic rate and risk-taking in the context of a trade-off between energy and predation. Using a simple time budget model, I show that a high resting metabolic rate is not necessarily associated with a high daily energy expenditure. The metabolic rate that minimizes the time spent foraging does not maximize the net gain rate while foraging, and it is not always advantageous for animals to have a higher metabolic rate when food availability is high. A model based on minimizing the ratio of mortality rate to net gain rate is used to determine how a willingness to take risks should be correlated with metabolic rate. My results establish that it is not always advantageous for animals to take greater risks when metabolic rate is high. When foraging intensity and metabolic rate coevolve, I show that in a particular case different combinations of foraging intensity and metabolic rate can have equal fitness.     

Pushed for time or saving on fuel: fine-scale energy budgets shed light on currencies in a diving bird

Animals may forage using different currencies depending on whether time minimization or energy maximization is more pertinent at the time. Assessment of net energy acquisition requires detailed information on instantaneous activity-specific power use, which varies according to animal performance, being influenced, for example, by speed and prey loading, and which has not been measured before in wild animals. We used a new proxy for instantaneous energy expenditure (overall dynamic body acceleration), to quantify foraging effort in a model species, the imperial shag Phalacrocorax atriceps, during diving. Power costs varied nonlinearly with depth exploited owing to depth-related buoyancy. Consequently, solutions for maximizing the gross rate of gain and energetic efficiency differed for dives to any given depth. Dive effort in free-ranging imperial shags measured during the breeding season was consistent with a strategy to maximize the gross rate of energy gain. We suggest that the divergence of time and energy costs with dive depth has implications for the measurement of dive efficiency across diverse diving taxa.     

Effects of Chemical Cues on Foraging in Damselfly Larvae, <Emphasis Type="Italic">Enallagma antennatum</Emphasis>

Animals experiencing a trade-off between predation risk and resource acquisition must accurately predict ambient levels of predation risk to maximize fitness. We measure this trade-off explicitly in larvae of the damselfly Enallagma antennatum, comparing consumption rates in the presence of chemical cues from predators and injured prey. Damselflies distinguished among types of chemical cues based on species of prey injured or eaten. Injured coexisting heterospecific and unknown heterospecific chemical cues did not reduce foraging relative to starved predator cues, while cues arising from predators eating a coexisting heterospecific did decrease foraging. This study shows a cost in terms of reduced foraging in response to chemical cues and further defines the ability of prey to respond discerningly to chemical cues.     

Effects of prey abundance on the foraging behaviour, diving efficiency and time allocation of breeding Guillemots Uria aalge

The foraging behaviour of Guillemots Uria aalge at sea was compared between 2 years of radically different food abundance. Radio telemetry was used to determine foraging locations and diving patterns. In the poor compared with the good food year, foraging trips were much longer, the birds foraged more than six times further from their breeding sites, they spent over five times as much time diving when at sea and their estimated energy expenditure was twice as great. Time spent foraging in the poor food year was at the expense of time spent sitting at the colony. The duration of a foraging trip was a poor indicator of distance travelled but a good indicator of the amount of time spent diving. Mean dive durations, surface pause durations and interbout periods did not differ between years, but individuals made more than four times as many dives per diving bout in the poor food year. Surface pause lengths did not vary with water depth in either year. In the poor food year, birds made shorter surface pauses for a dive of a gi^ven duration than in the good food year, possibly accepting a lactic acid debt in order to maximize searching time, The duration of the interbout period was positively related to the number of dives in the previous bout, and dives tended to get shorter in long diving sequences, suggesting possible exhaustion effects. These data demonstrate that breeding Guillemots have the capacity to adjust their foraging behaviour and time budgets in response to changes in food abundance, but this flexibility was not sufficient to compensate fully for the very low food abundance experienced by birds in this study.     

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.     

Behavioural context of multi-scale species distribution models assessed by radio-tracking

Incorporating ecological processes and animal behaviour into Species Distribution Models (SDMs) is difficult. In species with a central resting or breeding place, there can be conflict between the environmental requirements of the ‘central place’ and foraging habitat. We apply a multi-scale SDM to examine habitat trade-offs between the central place, roost sites, and foraging habitat in Myotis nattereri. We validate these derived associations using habitat selection from behavioural observations of radio-tracked bats. A Generalised Linear Model (GLM) of roost occurrence using land cover variables with mixed spatial scales indicated roost occurrence was positively associated with woodland on a fine scale and pasture on a broad scale. Habitat selection of radio-tracked bats mirrored the SDM with bats selecting for woodland in the immediate vicinity of individual roosts but avoiding this habitat in foraging areas, whilst pasture was significantly positively selected for in foraging areas. Using habitat selection derived from radio-tracking enables a multi-scale SDM to be interpreted in a behavioural context. We suggest that the multi-scale SDM of M. nattereri describes a trade-off between the central place and foraging habitat. Multi-scale methods provide a greater understanding of the ecological processes which determine where species occur and allow integration of behavioural processes into SDMs. The findings have implications when assessing the resource use of a species at a single point in time. Doing so could lead to misinterpretation of habitat requirements as these can change within a short time period depending on specific behaviour, particularly if detectability changes depending on behaviour.     

Corticosterone alone does not trigger a short term behavioural shift in incubating female common eiders Somateria mollissima, but does modify long term reproductive success

The trade-off between reproductive effort and adult survival in birds is modulated by several factors. Corticosterone and prolactin have additive effects on reproductive behaviour by stimulating foraging and parental behaviours, respectively. When incubation is associated with fasting, nest desertion is supposed to be activated by an unknown refeeding signal when body condition becomes critically deteriorated. The concomitant rise in corticosterone levels has been suggested to be the triggering factor. We tested the role of corticosterone on reproductive success by observing the effect of corticosterone implants on reproductive success and on plasma prolactin concentration in female common eiders Somateria mollissima . Implanted females showed a significant increase in corticosterone and a decrease in prolactin levels. Despite their enhanced daily body mass loss, females did not abandon incubation nor did they start to refeed in the four days following implantation. These data show that the experimentally induced rise in plasma corticosterone concentration alone does not trigger nest desertion. However, after 25 days of incubation, implanted females displayed a higher rate of egg loss, suggesting lower nest attentiveness towards the end of incubation. We suggest that the short-term effects of corticosterone may be dependent on the energy state of the bird. However, the late-induced change in reproductive success is indirectly linked to corticosterone, and we suggest that either a prolactin decrease, or a depletion in protein body reserves, may participate in the long-term adjustment of incubation behaviour in female eiders.     

The relationship between foraging behaviour and energy expenditure in Antarctic fur seals

By using time-depth recorders to measure diving activity and the doubly-labelled water method to determine energy expenditure, the relationship between foraging behaviour and energy expenditure was investigated in nine Antarctic fur seal females rearing pups. At-sea metabolic rate (MR) (mean of 6.34 ± 0.4 W. kg^-1; 4.6 times predicted BMR) was positively correlated to foraging trip duration (mean of 4.21 ± 0.54 days; r²= 0.5, P < 0.04). There were no relationships between MR and the total number of dives, the total time spent diving or the total vertical distance travelled during the foraging trip. There was, however, a close negative sigmoidal relationship (r²= 0.93) between at-sea MR and the proportion of time at sea spent diving. This measure of diving behaviour may provide a useful, inexpensive means of estimating foraging energy expenditure in this species and possibly in other otariids. The rate of diving (m.h^-1) was also negatively related to at-sea MR (r²= 0.69, P < 0.005). Body mass gain during a foraging trip had a positive relationship to the time spent at sea (r²= 0.58, P < 0.02) and the total amount of energy expended while at sea (r²= 0.72, P < 0.004) such that, while females undertaking long trips have higher metabolic rates, the energetic efficiency with which females gain mass is independent of the time spent at sea. Therefore, within the range of conditions observed, there is no apparent energetic advantage for females in undertaking foraging trips of any particular duration.     

How group size affects vigilance dynamics and time allocation patterns: the key role of imitation and tempo

In the context of social foraging, predator detection has been the subject of numerous studies, which acknowledge the adaptive response of the individual to the trade-off between feeding and vigilance. Typically, animals gain energy by increasing their feeding time and decreasing their vigilance effort with increasing group size, without increasing their risk of predation ('group size effect'). Research on the biological utility of vigilance has prevailed over considerations of the mechanistic rules that link individual decisions to group behavior. With sheep as a model species, we identified how the behaviors of conspecifics affect the individual decisions to switch activity. We highlight a simple mechanism whereby the group size effect on collective vigilance dynamics is shaped by two key features: the magnitude of social amplification and intrinsic differences between foraging and scanning bout durations. Our results highlight a positive correlation between the duration of scanning and foraging bouts at the level of the group. This finding reveals the existence of groups with high and low rates of transition between activities, suggesting individual variations in the transition rate, or 'tempo'. We present a mathematical model based on behavioral rules derived from experiments. Our theoretical predictions show that the system is robust in respect to variations in the propensity to imitate scanning and foraging, yet flexible in respect to differences in the duration of activity bouts. The model shows how individual decisions contribute to collective behavior patterns and how the group, in turn, facilitates individual-level adaptive responses.     

Behaviour of leatherback sea turtles, Dermochelys coriacea, during the migratory cycle

Leatherback sea turtles, Dermochelys coriacea, undertake broad oceanic movements. While satellite telemetry has been used to investigate the post-nesting behaviour of female turtles tagged on tropical nesting beaches, long-term behavioural patterns of turtles of different sexes and sizes have not been described. Here we investigate behaviour for 25 subadult and adult male and female turtles satellite-tagged in temperate waters off Nova Scotia, Canada. Although sex and reproductive condition contributed to variation in migratory patterns, the migratory cycle of all turtles included movement between temperate and tropical waters. Marked changes in rates of travel, and diving and surfacing behaviour, accompanied southward movement away from northern foraging areas. As turtles approached higher latitudes the following spring and summer, they assumed behaviours consistent with regular foraging activity and eventually settled in coastal areas off Canada and the northeastern USA. Behavioural patterns corresponding to various phases of the migratory cycle were consistent across multiple animals and were repeated within individuals that completed return movements to northern waters. We consider the potential biological significance of these patterns, including how turtle behaviour relates to predator avoidance, thermoregulation and prey distribution.     

Evolution restricts the coexistence of specialists and generalists: the role of trade-off structure

Environmental variability and adaptive foraging behavior have been shown to favor coexistence of specialists and generalists on an ecological timescale. This leaves unaddressed the question of whether such coexistence can also be expected on an evolutionary timescale. In this article, we study the attainability, through gradual evolution, of specialist-generalist coexistence, as well as the evolutionary stability of such communities when allowing for immigration. Our analysis shows that the potential for specialist-generalist coexistence is much more restricted than originally thought and strongly depends on the trade-off structure assumed. We establish that ecological coexistence is less likely for species facing a trade-off between per capita reproduction in different habitats than when the trade-off acts on carrying capacities alone. We also demonstrate that coexistence is evolutionarily stable whenever it is ecologically stable but that in most cases, such coexistence cannot be reached through gradual evolution. We conclude that an evolutionarily stable community of specialists and generalists may be created only through immigration from elsewhere or through mutations of large effect. Our results highlight that trade-offs in fitness-determining traits can have counterintuitive effects on the evolution of specialization.     

Utilisation of Intensive Foraging Zones by Female Australian Fur Seals

Within a heterogeneous environment, animals must efficiently locate and utilise foraging patches. One way animals can achieve this is by increasing residency times in areas where foraging success is highest (area-restricted search). For air-breathing diving predators, increased patch residency times can be achieved by altering both surface movements and diving patterns. The current study aimed to spatially identify the areas where female Australian fur seals allocated the most foraging effort, while simultaneously determining the behavioural changes that occur when they increase their foraging intensity. To achieve this, foraging behaviour was successfully recorded with a FastLoc GPS logger and dive behaviour recorder from 29 individual females provisioning pups. Females travelled an average of 118 ± 50 km from their colony during foraging trips that lasted 7.3 ± 3.4 days. Comparison of two methods for calculating foraging intensity (first-passage time and first-passage time modified to include diving behaviour) determined that, due to extended surface intervals where individuals did not travel, inclusion of diving behaviour into foraging analyses was important for this species. Foraging intensity ‘hot spots’ were found to exist in a mosaic of patches within the Bass Basin, primarily to the south-west of the colony. However, the composition of benthic habitat being targeted remains unclear. When increasing their foraging intensity, individuals tended to perform dives around 148 s or greater, with descent/ascent rates of approximately 1.9 m•s^-1 or greater and reduced postdive durations. This suggests individuals were maximising their time within the benthic foraging zone. Furthermore, individuals increased tortuosity and decreased travel speeds while at the surface to maximise their time within a foraging location. These results suggest Australian fur seals will modify both surface movements and diving behaviour to maximise their time within a foraging patch.     

Development of foraging behavior in juvenile northern elephant seals

Rapid development of foraging ability is critical for phocids. In northern elephant seals Mirounga angustirostris , juvenile survivorship is low compared with adults and foraging difficulties are potentially associated with increased mortality. At Año Nuevo, California, foraging behavior of nine juvenile females during their third foraging migration and five juvenile females on their fourth foraging migration were documented using a variety of commercially available and custom time depth recorders. Foraging success, diving ability, time at depth, bouts of behavior and body composition changes were compared between trips to sea. There were no significant differences in foraging success measured as mass gain between the third and fourth trips to sea. There were differences in how energy was deposited between lean and adipose tissue compartments. Diving ability developed between trips to sea, reflected in significant increases in depth, dive duration and bottom time. Development also occurred within trips to sea. Depth, dive duration and bottom time increased with time at sea. Aerobic capacity appears to increase between the third and fourth trip, with a significantly increased percentage of total time submerged and a significantly lower diving rate. All juveniles on the fourth trip and four out of nine juveniles on the third trip followed marked diel patterns, foraging deep during the day and shallow at night. Like adults, juveniles appeared to stay primarily aerobic with surface intervals independent of dive durations. These results confirm that female juvenile northern elephant seals undergo important developmental changes in foraging behavior between the third and fourth trip, but these changes do not significantly impact foraging success.     

Dangerous dive cycles and the proverbial ostrich

Data rarely are available to address the level of predation risk faced by diving animals in different parts of the water column. Consequently, most published research on diving behaviour implicitly assumes – like the proverbial ostrich – that 'unseen' predators are functionally unimportant. We argue that failure to consider diving in a predation risk framework may have precluded many insights into the ecology of aquatic foragers that breathe air. Using existing literature and a simple model, we suggest that fear from submerged predators in several systems might be influencing patch residence time, and therefore the duration of other dive cycle components. These analyses, along with an earlier model of predation risk faced by diving animals at the surface, suggest that dive cycle organisation can be modified to increase safety from predators, but only at the cost of reduced energy gain. Theoretical arguments presented here can seed hypotheses on factors contributing to population declines of diving species. For instance, adjustments to the dive cycle that reduce predation risk might be unaffordable if resources are scarce. Thus, if animals are to avoid imminent starvation or substantial loss of reproductive potential, resource declines might indirectly increase predation rates by limiting the extent to which dive cycles can deviate from those that would maximize energy gain. We hope that ideas presented in this paper stimulate other researchers to further develop theory and test predictions on how predation risk might influence diving behaviour and its ecological consequences.     

Antibacterial and anatomical defenses in an oil contaminated,vulnerable seaduck

Oil spills have killed thousands of birds during the last 100 years, but nonlethal effects of oil spills on birds remain poorly studied. We measured phenotype characters in 819 eiders Somateria mollissima (279 whole birds and 540 wings) of which 13.6% were oiled. We tested the hypotheses that (a) the morphology of eiders does not change due to oil contamination; (b) the anatomy of organs reflects the physiological reaction to contamination, for example, increase in metabolic demand, increase in food intake, and counteracting toxic effects of oil; (c) large locomotion apparatus that facilitates locomotion increases the risk of getting oiled; and (d) individual eiders with a higher production of secretions from the uropygial grand were more likely to have oil on their plumage. We tested whether 19 characters differed between oiled and nonoiled individuals, showing a consistent pattern. The final model retained seven predictor variables showing relationships between eiders contaminated with oil and food consumption, flight, and diving abilities. We tested whether these effects were due to differences in body condition, liver mass, empty gizzard mass, or other characters that could have been affected by impaired flight and diving ability. There was no evidence of such negative impact of oiling on eiders. We found that significant exposure to oil was associated with increased diversity of antibacterial defense. Oiled eiders did not constitute a random sample, and superior diving ability as reflected by large foot area was at a selective disadvantage during oil spills. Thus, specific characteristics predispose eiders to oiling, with an adaptation to swimming, diving, and flying being traded against the costs of oiling. In contrast, individuals with a high degree of physiological plasticity may experience an advantage because their uropygial secretions counteract the effects of oil contamination.     

Eat now,pay later? Evidence of deferred food-processing costs in diving seals

Seals may delay costly physiological processes (e.g. digestion) that are incompatible with the physiological adjustments to diving until after periods of active foraging. We present unusual profiles of metabolic rate (MR) in grey seals measured during long-term simulation of foraging trips (4-5 days) that provide evidence for this. We measured extremely high MRs (up to almost seven times the baseline levels) and high heart rates during extended surface intervals, where the seals were motionless at the surface. These occurred most often during the night and occurred frequently many hours after the end of feeding bouts. The duration and amount of oxygen consumed above baseline levels during these events was correlated with the amount of food eaten, confirming that these metabolic peaks were related to the processing of food eaten during foraging periods earlier in the day. We suggest that these periods of high MR represent a payback of costs deferred during foraging.     

Foraging behavior and success of a mesopelagic predator in the northeast Pacific Ocean: insights from a data-rich species, the northern elephant seal

The mesopelagic zone of the northeast Pacific Ocean is an important foraging habitat for many predators, yet few studies have addressed the factors driving basin-scale predator distributions or inter-annual variability in foraging and breeding success. Understanding these processes is critical to reveal how conditions at sea cascade to population-level effects. To begin addressing these challenging questions, we collected diving, tracking, foraging success, and natality data for 297 adult female northern elephant seal migrations from 2004 to 2010. During the longer post-molting migration, individual energy gain rates were significant predictors of pregnancy. At sea, seals focused their foraging effort along a narrow band corresponding to the boundary between the sub-arctic and sub-tropical gyres. In contrast to shallow-diving predators, elephant seals target the gyre-gyre boundary throughout the year rather than follow the southward winter migration of surface features, such as the Transition Zone Chlorophyll Front. We also assessed the impact of added transit costs by studying seals at a colony near the southern extent of the species' range, 1,150 km to the south. A much larger proportion of seals foraged locally, implying plasticity in foraging strategies and possibly prey type. While these findings are derived from a single species, the results may provide insight to the foraging patterns of many other meso-pelagic predators in the northeast Pacific Ocean.     

Local orientation and the evolution of foraging: changes in decision making can eliminate evolutionary trade-offs

Information processing is a major aspect of the evolution of animal behavior. In foraging, responsiveness to local feeding opportunities can generate patterns of behavior which reflect or "recognize patterns" in the environment beyond the perception of individuals. Theory on the evolution of behavior generally neglects such opportunity-based adaptation. Using a spatial individual-based model we study the role of opportunity-based adaptation in the evolution of foraging, and how it depends on local decision making. We compare two model variants which differ in the individual decision making that can evolve (restricted and extended model), and study the evolution of simple foraging behavior in environments where food is distributed either uniformly or in patches. We find that opportunity-based adaptation and the pattern recognition it generates, plays an important role in foraging success, particularly in patchy environments where one of the main challenges is "staying in patches". In the restricted model this is achieved by genetic adaptation of move and search behavior, in light of a trade-off on within- and between-patch behavior. In the extended model this trade-off does not arise because decision making capabilities allow for differentiated behavioral patterns. As a consequence, it becomes possible for properties of movement to be specialized for detection of patches with more food, a larger scale information processing not present in the restricted model. Our results show that changes in decision making abilities can alter what kinds of pattern recognition are possible, eliminate an evolutionary trade-off and change the adaptive landscape.