The Role of Energy Intake Rate in Prey and Habitat Selection of Common Eiders Somateriamollissima in Winter: A Risk-Sensitive InterpretationAuthor(s): Magella Guillemette, Ronald C. Ydenberg and John H. HimmelmanSource: Journal of Animal Ecology, Vol. 61, No. 3 (Oct., 1992), pp. 599-610Published by: British Ecological SocietyStable URL: http://www.jstor.org/stable/5615 .

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Journal of Animal Ecology 1992, 61, 599-610

The role of energy intake rate in prey and habitat selection of common eiders Somateria mollissima in winter: a risk-sensitive interpretation

MAGELLA GUILLEMETTE*t, RONALD C. YDENBERGt and JOHN H. HIMMELMAN* * GIROQ (Groupe Interuniversitaire de Recherches Oceanographiques du Quebec) and Department de Biologie, Universite Laval Quebec, Quebec, Canada, GI K 7P4; and tBehavioural Ecology Research Group, Department of Biological Sciences, Simon Fraser University, Burnaby, B.C. Canada, V5A IS6

Summary

1. We measured prey selection and habitat profitability of common eiders Somateria

mollissima L. wintering in the Gulf of St. Lawrence, Quebec, Canada. Prey selection was evaluated by comparing the frequency of prey in stomachs of shot

eiders with their frequency in the sublittoral zone. Habitat profitability was

estimated using information on time spent feeding, foraging success, diving dur-

ations and energy content of the prey. 2. In this region, eiders forage on a variety of prey types from several distinct

habitats, kelp beds, urchin barrens and beds of the phaeophyte Agarum cribrosum

(Mert.). In kelp beds eiders feed mostly on small blue mussels Mytilus edulis L.

Over barrens they capture green sea urchins Strongylocentrotus droebachiensis (Muller), and over Agarum beds they feed on both spider crabs Hyas araneus (L.)

and urchins.

3. Flock size also varies with habitat type: all sizes of flocks feed in the kelp beds,

whereas mostly small flocks feed in the barrens and Agarum beds. Small-flock

individuals strongly select mussels and crabs whereas urchins are non-preferred prey.

4. Dive and foraging cycles differ significantly according to the above three habitats. Although, the size, density and energy content of prey differ markedly

between kelp and Agarum beds, these two habitats offer an even energy return.

However, the variance in energy return in these two habitats differs strikingly,

being greater in the latter. We hypothesized, in the context of risk foraging theory,

that this was related to flock sizes and body condition. As predicted, individuals

feeding in small flocks were in bad condition compared to individuals feeding in

large flocks. This suggests that small-flock individuals are seeking the habitat

offering a variable intake to improve their survival probability.

Key-words: common eider, energy intake, prey selection, risk-sensitivity, body condition.

Journal of Animal Ecology (1992), 61, 599-610

Introduction

Many investigations indicate that the maximization of energy intake could be a major driving force of habitat and food selection in animals (reviewed by Schoener 1987). Habitat profitability alone, defined as the gain of energy per unit of time spent handling

* Present address: Departement de Biologie, Universit6 du Quebec a Rimouski, 300 allee des Ursulines, Rimouski (Quebec), Canada, G5L 3A1.

and searching for food in a particular habitat, can be seen as a good correlate of habitat suitability when predation is uniform over the habitat. Under these conditions, an animal should select feeding habitats where average energy intake is maximized (Pulliam 1976). Although this hypothesis has been tested in laboratory and field situations (Schoener 1987), most studies deal with predators feeding on different sizes of the same prey species or prey found in a simple homogeneous habitat structure (Schluter 1981; Werner, Mittelbach & Hall 1981). The goal of 599

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600 Energy intake in wintering common eiders

this paper is to examine the relevance of energy maximization for the common eider Somateria mollissima, a predator that forages in a complex environment where the selection of a particular habitat, and the prey therein, may have important consequences with respect to the strategies we would expect efficient predators to follow.

Experimental studies indicate that foraging de- cisions could be influenced not only by the average intake rate achieved in a habitat (or a patch of food) but also by its associated variance (Caraco, Martindale & Whitham 1980; Caraco et al. 1990; Ha, Lehner & Farley 1990; Cartar 1991). The sen- sitivity to the variability of food intake is referred to as risk-sensitivity and indicates that prey or habitat selection could be based on the probability of an energy shortfall, which would lead to starvation. The rationale behind this theory, called the energy budget rule (Krebs, Stephens & Sutherland 1983), stipulates that, when a predator expects to have a positive daily energy budget, it should behave as a risk-averse forager and choose prey or habitats with low variance. When a predator expects to have a negative energy budget, it should behave as a risk-prone forager and choose habitats with a high variance, because the chances of survival increase with a more variable intake (Caraco 1980; Stephens & Charnov 1982). Risk-proneness should be as- sociated with poor physiological condition. This is because when an animal is in bad condition, the extra energy needed to recover increases its energy requirements relative to an animal in good condition.

Common eiders are large sea ducks feeding on a wide variety of rocky subtidal prey, including molluscs, echinoderms and crustaceans. Eiders wintering in the Gulf of St. Lawrence feed preferen- tially in shallow water (0-6 m) where the main prey eaten are found in three different habitats, kelp beds, urchin barrens and Agarum beds (Guillemette 1991). Each of the three habitats are composed of different prey. The blue mussel Mytilus edulis L. and the spider crab Hyas araneus (L.) are found only in kelp and Agarum beds, respectively, whereas the green sea urchin Strongylocentrotus droebachiensis (Muller) is ubiquitous in the subtidal environment and particularly abundant in the grazed areas called barrens. These are by far the most important prey although a variety of other prey are present. Prey species differ in density, size, energy content and in their distribution in the environment. Parameters such as diving frequency, the number of prey cap- tured per dive and the time spent foraging all vary with the type of prey and habitat selected. Thus, for a predator such as the eider foraging in a complex environment, prey and habitat selection are likely to have important consequences for energy intake. This may be especially true for birds in mid-winter at high latitudes where low temperatures coincide with the shortest days of the year. Therefore, we

expect that during winter, when the energy balance should be more difficult to achieve, energy shortfalls are more likely to happen.

In this study, we examine food selection and feeding profitability by common eiders in winter. We base our analysis on observations of eiders foraging over the three habitat types and on deter- minations of the percentage time spend feeding, foraging success, diving durations and energy con- tent of the prey. We show that diet and habitat selection in eiders differ in relation to flock size. We also furnish evidence that although the preferred habitat-prey types differ in many respects, they offer a similar energy intake but differ greatly in their associated variances. Finally, we consider how food selection and flock size are related to body condition and discuss this in the context of risk- sensitivity theory.

Materials and methods

DIETS OF EIDERS

Our study was conducted during the winters of 1985-86, 1986-87 and 1989 on the south-east portion of Ile a la Chasse (50?40'N, 63?07'W), Mingan Archipelago, in the northern part of the Gulf of St. Lawrence, Quebec, Canada. To deter- mine diets and body mass of wintering eiders, 257 individuals were shot in the study area between mid- December and late April in 1985-86 and 1986-87. Of these, 234 birds contained food in their stomachs and were retained for analysis. We collected eiders using two methods. The first consisted of shooting individuals which had been attracted to decoys (n = 171). They came from small (<30) flocks flying from unknown locations. The second method (n =

86) consisted of shooting eiders that were feeding at depths of 0-6m at known sites within our study area. They included birds from both large (>300) and small (<30) flocks. The sample from small flocks consisted of 144 adults (81 males and 63 females) and 60 juveniles or subadults (34 males and 26 females) and the sample from large flocks of 49 adults (29 males and 20 females) and 4 juveniles (2 males and 2 females). We analysed the contents of the gizzard and oesophagus of each bird. In- dividuals shot over decoys contained prey only in the gizzard, whereas feeding individuals contained food in both organs. The relative wet mass of each prey in the gizzard and oesophagus was determined for each bird.

PREY SELECTION

Only eiders actually feeding in our study area (second method) were considered in our analysis of prey selection. The frequency of prey in the stomachs of shot birds was compared to their frequency in the

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601 M. Guillemette, R. C. Ydenberg & J.H. Himmelman

sublittoral zone. The frequency of prey inside each community was evaluated using 0-25-m2 quadrats placed at 10--m intervals along transects using SCUBA during the summer and autumn of 1985. No attempt was made to follow prey frequency and distribution over a complete annual cycle but diving observations in spring 1987 indicated that prey distribution was the same as in 1985. We used the product of the frequency of a prey inside a community times the relative surface area of the same community as the estimate of prey availability. The relative surface area of a community was determined from aerial photographs (1:15000) and was similar for three different years, 1973, 1985 and 1988, indicating that the distribution of these communities is stable. Finally, the distribution of the communities followed a depth gradient, kelp beds being mostly found between 0 and 3 m, urchin barrens on bedrock between 0 and 6 m and Agarum beds between 0 and 18 m in depth (Guillemette 1991).

ENERGETIC CONTENT OF THE PREY

Caloric determinations were made for the three main prey items eaten by eiders: blue mussels, green sea urchins and spider crabs. Prey were collected by divers using SCUBA in March 1987 at two feeding sites. Prey size was measured with vernier callipers to the nearest 0.1 cm. The total body mass (skeleton + water + flesh) was weighed to the nearest milli- gram, first fresh and then after being dried in an oven at 60 ?C until a constant mass was reached. We used logarithmic functions to describe the relation of prey size (L = length in cm) to total body mass and to water content and flesh mass (in g). Then, dry mass of flesh was estimated using linear regression equations relating the dry mass (DM) to water content and flesh mass. The relations for mussels were as follows:

BODY MASS = 0-155 x Lp2845 (R2 = 0-97, n = 200) SHELL MASS = 0.103 x L2681 (R2 = 0-95, n = 100) WATER + FLESH MASS = 0-051 x L3 83

(R2 = 0.95, n= 100) FLESH DM = 0.002 + 0 121 WATER + FLESH (R2 = 0.94, n = 100).

For urchins the relations were:

BODY MASS = 0*560 x L 2837 (R2 = 0.99. n = 123) TEST MASS = 0-524 x L2 477 (R2 = 0.99, 1 = 104)

For urchins, the mass of fluids and tissues was ob- tained from the difference between total body mass and test mass. We used the values of Keats, Steele & South (1984) for percentage gonad mass to body mass (14.88% at 0-3m in depth) as an estimate of gonad mass in urchins. From a subsample of urchins in which we measured separately the mass of gonad tissue and non-gonad tissue we obtained the fol- lowing relationships:

GONAD DM = 0-013 + 0O160 GONAD WM (R2 = 0-98, n=50) NON-GONAD DM = 0.020 + 0-057 NON-GONAD WM (R 2= 0-97, n = 30).

Shells of molluscs and tests of urchins were removed before drying. The carapace of crabs was not re- moved as the sclerotized exoskeleton has energetic value. For the crabs we used the relations:

BODY MASS = 0.066 x L3688 (R2 =0-92, n = 24) DM = 0.111 + 0*237 WM (R2 = 0*71, n = 12)

Caloric determinations were made using a Parr model 1243 adiabatic bomb calorimeter following the method of Atkinson & Wacasey (1976). A minimum of 10 determinations were made for each prey, and for urchins 10 separate determinations were made for gonad and non-gonad tissues. Tripli- cate ashing determinations were made of each tissue in a muffle furnace at 500?C for 12 h.

FEEDING BEHAVIOUR AND FORAGING

SUCCESS

We studied feeding behaviour in relation to the prey and habitat being used. Foraging cycles in common eiders involve alternating feeding and resting bouts (Fig. 1). Feeding bouts are composed of successive dive-cycles, each of which has three components, diving (completely submerged), handling the prey at the surface and pausing before the next dive. Each dive has either a successful or unsuccessful outcome. When the prey is large, eiders handle it at the surface before swallowing it whole. Then follows pausing which involves resting or swimming at the surface until the next dive. After a certain amount of prey is ingested (= a meal), eiders stop feeding and enter a resting bout during which they undertake comfort activities (preening, bathing, etc.) in addition to resting.

To determine the different parameters of a dive cycle, we used focal-animal sampling (Altman 1974). Individuals were distinguished using plumage criteria and could be recognized before and following dives. Each focal-bird was chosen at random (with a die) from a 'population' of eiders which could easily be identified (usually 5-30 such individuals were present at a time). To determine the diving depth and the community in which they were feeding, the position of each focal-bird was localized using a compass and a range-finder at the beginning of each observation period. The position of each focal-bird was recorded on a bathymetric map, at the scale of 1:10 000, upon which the position of kelp beds, urchin barrens and Agarum beds were superim- posed. When the localization at the end of the observation period differed markedly from the initial one (as whenl there was a shift in type of habitat used), an unknown habitat was assigned to the

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602 Energy intake in wintering common eiders

Foraging cycle

1~ ~~~~ in ALs Dive cycle

Meal size (g) Paus~Die drtime (s)

Fig. 1.Shi no uccessaulnd aSuccessfult

bou Pas tie 3 s

FHandlI ng time (s )|

\ | ~~~~~~~Prey energy (kJ )|

Fig. 1. Schematic representation of a dive and a foraging cycle in the common eider.

bird. Each focal period lasted until the observer voluntarily stopped at 30min or until the bird was lost. No focal bird was followed more than once during any particular day. Only the mean values for each focal bird were used as independent data points for statistical analysis. Throughout this study, mussel, crab and urchin feeding bouts are used as synonyms for eiders foraging over kelp beds, Agarum beds and urchin barrens, respectively.

All our observations of feeding behaviour and foraging success were made on eiders foraging alone or in small flocks (<30). Eiders retrieve a single prey when foraging on urchins and crabs, as these prey are large and require handling at the surface before being swallowed. Thus, the outcome of each dive could be determined by the presence or absence of prey held in the bill of eiders. By contrast, when feeding on mussels, eiders collected many small prey during each dive. Mussels require no handling at the surface and were virtually always swallowed underwater. We inferred that eiders were feeding on mussels when their position on the community map indicated that they were over mussel beds. To estimate the meal size for eiders feeding on mussels, we examined the stomach contents of feeding birds (second sample). We reasoned that the stomach content of an eider would be at a maximum at the end of an ingestion period, the last portion of a cumulative distribution curve of the mass of oeso- phagus and gizzard contents for shot birds was therefore used to estimate meal size.

METABOLIC COSTS OF FEEDING AND

RESTING

Metabolic costs were taken from literature estimates and calculated for a standard individual, an adult female weighing 1825 g (M. Guillemette, unpub-

lished). We used data on a similar diving duck, the tufted duck Aythya fuligula (L.), to obtain an esti- mate of the costs of resting, diving, handling and pausing as multiples of the basal metabolic rate (BMR). Woakes & Butler (1983) estimated that, for an individual tufted duck weighing 0-597 kg, the costs of diving and pausing were 0 566 and 0-444 ml 02 s-1, respectively. Since Woakes & Butler (1983) did not determine the basal metabolic rate (BMR) of tufted ducks, we used the equation from Aschoff & Pohl (1970) for basal metabolic rate during the activity phase in non-passerine birds (BMR = 91-0 Mb0-729 where BMR = energy in kcal day-' and Mb = body mass in kg) to estimate the foraging costs of the tufted duck. Diving increases the BMR by 3*8 times and pausing by 3-0 times. Since handling prey at the surface involves swimming as well as intensive prey processing, we estimated that the approximate cost of handling is 3-3 x BMR.

Jenssen, Ekker & Bech (1989) report that the basal metabolic rate of common eiders on water in a postabsorptive state during the activity phase is 6039 kJ day-' at thermoneutrality. We used this value and the BMR multiples as determined for the tufted duck in our calculations of energy expenditure of foraging eiders. We assumed that the heat pro- duced as a by-product of foraging was substitutive for the increased thermoregulatory demand below thermoneutrality (i.e. an increase in thermoregula- tory requirements is not additive to the energy spent foraging; see Bevan & Butler 1989; Webster & Weathers 1990). To calculate energy requirements of resting eiders, we used the equation BMR =

5 48 - 009 Tw relating the metabolism of eiders below thermoneutrality (lower critical temperature in water = 15?C) to water temperature (BMR in watts kg-, T, in ?C; Jenssen, Ekker & Bech 1989). All our estimates of foraging and resting costs were

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603 M. Guillemette, R. C. Ydenberg & J.H. Himmelman

made for the mid-winter period (December-January) and we used the freezing point of sea water (-2 ?C) as the water temperature. For the time available for foraging we used the 8 h daylight period plus 1 h for the twilight periods (total = 9 h), Using these pro- cedures, the costs of resting, diving, handling and pausing were calculated to be 13-4, 26-6, 23*1 and 21-OJ s-1, respectively, and were assumed to be constant.

VARIANCE ESTIMATES OF PROFITABILITIES

To assess the variance associated with our estimates of habitat and prey profitability, we used Monte Carlo simulations to 'resample' our original data set randomly (Sokal & Rohlf 1981). To do this, a subset of 2000 simulations were run for each habitat-prey type, for which observed feeding and resting bouts and dive-cycles were chosen randomly. For eiders feeding on urchins and crabs, we assumed that the average handling time at the surface corresponded to the average prey size found in eiders collected for the stomach analyses. For mussels, we assumed that prey size (=number of mussels) was proportional to diving time (as there was no handling component at the surface for this prey). Dive cycles were cumulated until the duration of a feeding bout was reached. A resting bout was then chosen. Each simulation was run until the cumulative foraging time reached 9 h (it excluded roosting time). The estimate of net energy gain obtained in these simulations was for daylight hours and did not include the costs of flying and overnight costs. We used the F distribution and the F ratio (Sokal & Rohlf 1981) to test if the variances of two samples were similar with ni - 1 and n2 - 1 degrees of freedom. We used the smallest sample size of our original data set as a conservative

estimate of the degrees of freedom associated with the F test.

Results

FOOD SELECTION

Although the diet of common eiders consisted of a wide spectrum of prey species, blue mussels and green sea urchins were the most frequent prey. Spider crabs were only eaten by eiders feeding in small flocks (Table 1). Other differences related to flock size were that individuals in large flocks con- sumed more frequently mussels than those in small flocks (G = 11-16, df = 1, P < 0-001) whereas urchins were more frequently eaten by small-flock indi- viduals (G = 4-02, df = 1, P < 0.05) where they could form the bulk of a meal (Table 1). Prey size varied mainly with the species being eaten. Blue mussels were the smallest of the common prey and ranged from 1 to 25 mm in shell length with a mode at 7- 8mm (n = 5600), and urchins ranged from 10 to 46 mm in diameter (n = 46). The spider crab was the largest prey and measured from 30 to 51 mm in carapace length (n = 24). When the frequency of occurrence of a prey in the diet was compared to its frequency in the environment (Table 2), it was apparent that mussels and crabs were highly preferred over other potential prey. Thus, these two prey were actively sought by eiders feeding in small flocks.

ENERGY CONTENT OF PREY

The energy content of the three main prey differed markedly because of differences in the content of organic matter. The shells of mussels and tests of

Table 1. The proportion (wet mass) of the principal dietary components found in the stomachs (gizzard + oesophagus) of common eiders. Each row indicates the mean proportion of the prey categories (above) for the stomachs containing the item on the left (in bold values). The number of stomachs containing the item is shown in parentheses. When proportions in bold values equal or exceed any proportion of a row, we concluded that this prey formed the bulk of a meal

Stomachs' proportional contents

Stomachs containing Mussels Urchins Crabs Others

For 33 small-flock eiders (<30) feeding in the 0-6m depth range Mussels (25) 0-444 0-451 0 007 0-098 Urchins (21) 0-211 0-728 0-044 0-017 Crabs (5) 0-423 0-105 0-424 0-048

For 53 large-flock eiders (>300) feeding in the 0-6m depth range Mussels (52) 0-838 0-126 0 0-036 Urchins (22) 0-600 0-343 0 0-057 Crabs (0) 0 0 0 0

For 148 small-flock eiders (<30) flying from unknown locations Mussels (92) 0-612 0-186 0-022 0-180 Urchins (66) 0-204 0-636 0 049 0-111 Crabs (33) 0-048 0-274 0-486 0-192

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604 Energy intake in wintering common eiders

Table 2. Frequency of occurrence (%) of potential prey in the sublittoral zone (based on 292 quadrats of 0-25 m2),

frequency of occurrence (%) in the diet of common eiders and forage ratio for large (n = 53) and small (n = 33) flocks feeding in the 0-6m depth range. Large flocks are >300 individuals and small flocks are <30 individuals. Percentage occurrence values sharing the same superscript were not significantly different (G test, P> 0.05) between flock sizes, otherwise they were (P < 0.05)

Percentage Percentage occurrence in the diet occurrence in Forage ratio*

the sublittoral Prey Large flocks Small flocks zone (0-6m) Large flocks Small flocks

Mussels 98 la 75-7b 13.1 7.5 5 8 Whelks 15 la 6 la 18 1 0-8 0-3 Snails 33_9a 15 2b 62-8 0 5 0 2 Urchins 41.5a 63-6b 99.4 0-4 0-6 Ophiurids 0 3 0 83 2 0 0 0 Crabs 0 15-2 3.7 0 41

* Frequency in the diet/frequency in the 0-6m depth range.

urchins averaged 67% and 62% of total body mass and the inorganic content of dry flesh averaged 16% and 52%, respectively. The inorganic content of the dry flesh and the carapace of the crab represented 36-3% of the total dry mass (no attempt was made to measure the carapace separately). The available energy from mussels per gram live mass was about twice as great as from urchins and the available energy from crabs was five times that of urchins and three times that of mussels (Table 3).

Table 3. Mean size, wet mass (WM), and available energy of the three main prey species eaten by common eiders

Available Available Prey Total wet energy energy per g size mass per prey live mass

Prey (mm)* (gWM) (kJ)t (kJ g1 WM)t

Mussels 9 7 0-175 0 169 0-966 Urchins 29-8 15-360 8-908 0 580 Crabst 39 9 12 070 38-177 3-163

* Length for mussels and crabs, and diameter for urchins. Assuming that the skeletons of mussels and urchins

have negligible energetic value. * Includes the carapace for all the values.

FEEDING BEHAVIOUR

A foraging cycle consisted of alternating feeding and resting bouts. When feeding on mussels in kelp beds, a foraging cycle lasted c. 1300s, with a meal duration of c. 800s and a resting period of c. 500s (Table 4). When feeding in both barrens and Agarum habitats, the foraging cycles were of similar duration (c. 2000 s). When feeding in urchin barrens, feeding and resting bouts were of similar duration, whereas when feeding on crabs in the Agarum beds feeding bouts (1356s) were 2*3 times longer than resting bouts (588s). Feeding bouts tended to be shorter for eiders feeding in kelp beds than for those feeding in Agarum beds (Kruskal-Wallis test, H= 5 91, P = 0-052). Further, the duration of resting bouts differed significantly with habitat type (H = 9-87, P < 0.01). Thus, in a crab foraging cycle, eiders spent 70% of their time feeding compared to 61 and 50% when foraging on mussels and urchins, respec- tively (Table 4).

Successful dive cycle durations differed signifi- cantly for the three types of feeding bouts (P < 0-001, Table 5). This difference cannot be attributed to the average depth of the different habitats. This is

Table 4. Average duration in seconds (? SD) of feeding and resting bouts in common eiders in three different habitats during winter. All observations were made inside the 0-6m depth range. Durations of feeding bouts in the different habitats do not differ significantly (Kruskal-Wallis test, H = 591, P = 0.052) whereas duration of resting bouts do (H= 9-87, P= 0-007)

% feeding in Foraging cycle a foraging

Habitat/feeding bout Feeding time (s) Resting time (s) (s)* cyclet

Kelp beds/mussels 794-2 ? 643-3 498-6 405 6 1292 7 61 4 (n) (26) (27)

Urchin barrens/urchins 1004-7 ? 760-4 1021-7 ? 487-9 2026-4 49 6 (n) (14) (8)

Agarum beds/crabs 1355-8+670-4 587-9?319-3 1943-7 69-8 (n) (10) (7)

* Sum of the average feeding and resting times. t Feeding time/foraging cycle x 100.

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605 M. Guillemette, R. C. Ydenberg & J.H. Himmelman

Table 5. Average durations in seconds (? SD) of diving, handling, pausing and cycle times for successful dives and diving intensity (dive cycles h-1) for eiders feeding in three different habitats during winter. Number of individuals observed (N) and number of observations (n) are given respectively for each activity and habitat. Kruskal-Wallis tests were made using mean values for each individual and diving (H = 153-9), pausing (H = 52-9) and dive cycle (H = 98.3) durations differ significantly among habitat (P < 0-001). Superscripts denote a posteriori comparisons and activities with same letters do not differ significantly (P> 0.05) among habitats, otherwise they do (P< 0-001). Handling did not differ significantly between habitats (Mann-Whitney U= 1-86, P = 0-063)

Habitat/feeding bout (N)

Kelp beds/ Urchin barrens/ Agarum beds/ Activity mussels (46) urchins (152) crabs (83)

Diving 17.9 ? 5.6a 14-5 + 6-3b 35.0 ? 9.3c (n) (652) (688) (184)

Handling - 39-3 + 29.4a 49.3 ? 40-5a

(n) (673) (180) Pausing 24-8 ? 12.2a 58-3 + 32-8bo 52-0 ? 30.5c

(n) (612) (525) (143) Dive cycle 42-7 ? 13-9a 103-9 + 43-8b 123-1 ? 46.7c

(n) (654) (570) (157) Diving intensity

(dive cycles h-1) 84-3 34-6 29-2

because most dives executed in urchin barrens were made at the same depth as in kelp beds (0-3m, Table 6) and also because, as reported previously (Beauchamp, Guillemette & Ydenberg, in press), the duration of successful dive cycles do not vary significantly between depths of 0 to 12 m in the Agarum habitat. Nevertheless, dive cycles were shortest when feeding on mussels, indicating that feeding on this prey was associated with the highest diving intensity (dives h-1). Diving intensity de- creased with the inclusion of larger prey such as urchins and crabs (Table 5). This was mainly because large prey need to be handled at the surface (dis- articulating crabs and breaking spines from urchins before swallowing them). Moreover, the handling component was not the sole factor explaining the longer dive cycles, as crab feeding bouts also had the longest diving durations (Table 5). This was expected as crabs were sparsely scattered on the bottom (0.5 crabs m-2; Guillemette 1991). Searching was probably an important part of diving time when feeding on crabs. In contrast, diving time was the shortest when feeding on urchins (Table 5) indicating short searching times. This was not surprising given

that urchins were ubiquitous in the subtidal zone (density of c. 90 individuals m-2). In the case of mussels, the situation differed markedly as they were small prey (<10mm) which occurred in high densities (16 000 individuals m-2). We thus conclude that the longer duration of dives for mussels, com- pared to those for urchins, was because a high number of prey was collected during each dive, whereas only a single urchin could be captured per dive.

We assumed that dives were always successful when feeding on mussels in kelp beds (0-3m). We calculated the number of mussels captured per dive, based on the mass of a meal and the duration of feeding bouts (Table 4) and dive cycles (Table 5). We first plotted the cumulative frequency of the mass of the oesophagus contents as a percentage of body mass of shot eiders, and calculated that about 20% of shot birds were at their maximum stomach content. This maximum corresponded to 3 5-5 0% of body mass which was equivalent to 64-93 g of mussels. We used 80 g (or 460 mussels) as an average estimate in our computations. The average number of dives per feeding bout was obtained by dividing

Table 6. Percentage of successful dives in Agarum and urchin barrens habitats. No significant differences in percentage of success were found among depth ranges in both habitats (Agarum, G = 6-20, df = 4, P > 0*05; urchin barrens, G = 0-18, df = 2, P > 0.05), n = number of dives observed

Agarum habitat Urchin barrens habitat

Depth (m) (n) Crabs Urchins None (n) Urchins None

0-3 (219) 21-0 11 0 68-0 (639) 79-8 20-2 3-6 (83) 32*5 8-4 59 1 (24) 83-3 16-7 6-12 (143) 26-6 14-0 59-4 (46) 80*4 19-6 Unknown (298) 24-5 8-4 67-1 (166) 72-9 27-1

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606 Energy intake in wintering common eiders

the average duration of a feeding bout (794 s) by the average duration of a dive cycle (43 s). This gave 19 dives during the meal associated with an average feeding bout. We therefore estimated that an average of 24 mussels were captured during each dive.

When feeding on crabs in the Agarum beds, the percentage success averaged only 25%. It did not vary significantly with depth (0-12 m, G = 6-20, P>0-05, Table 6) indicating that the difficulty in finding crabs was similar for the three depths con- sidered. The percentage success for eiders feeding on urchins in barrens also did not vary significantly with depth (G = 0-18, P> 0.05), although the great majority of dives were done in shallow water (0- 3m, Table 6). The proportion of successful dives was 79%, three times greater than when feeding on crabs in Agarum beds (Table 6).

HABITAT PROFITABILITY

We calculated the daily net energy intake for eiders feeding in the three habitats. The net gain during a foraging cycle was obtained by multiplying the net gain for an average dive cycle (energy in average prey-energetic costs of diving, handling and pausing) by the number of dive cycles in a feeding bout and then subtracting the energy spent during the resting bout. Multiplying this by the number of foraging cycles possible in a 9-h foraging day yielded an estimate of the net daily energy gain. The average rate of energy gain was 1353 kJ day-' when feeding in kelp beds and 1547 kJ day-1 when feeding in Agarum beds. In contrast, the energy gain in urchin barrens was only 590kJ day-1 (Fig. 2). Thus, these calculations indicate that eiders had similar net energy intake when feeding in kelp and Agarum beds, and a much lower intake when feeding in urchin barrens.

We expected there would be much higher vari- ations in profitability when feeding in Agarum than when feeding in kelp beds, because of the differences between crabs and mussels in their size and energy content as well in their associated foraging success. However, it was impossible to calculate directly the variance associated with our estimates of pro- fitability. Four main sources of variance were in- volved in our estimate of energy intake: (i) the energy content of the prey which is related mainly to its size, and secondly to its quality (Jg-1 DW); (ii) the percentage success of dives; (iii) the durations of diving, pausing and handling times composing a dive-cycle; and (iv) the duration of the foraging cycle. We used Monte Carlo simulations to estimate the variance associated with our estimates of prey profitabilities, and these in turn were used to test whether the observed profitabilities were similar (Fig. 2). The variance in profitability when feeding on crabs in Agarum beds was 4-6 times higher than when feeding on mussels in kelp beds (df = 7, 26,

600 - Kelp beds / mussels Mean = 1353

I- |Variance 27102

400-

200CLJ 600

Urchin barrens /urchins Mean = 590

400 - Variance = 16664

L 200 L

O 0 . |. _. . . . . . . .

600 - Agarum beds / crabs

Mean = 1547 Variance = 124132

400 -

200 -i I

0 I 200 600 1000 1400 1800 2200

Daylight energy gain (kJ)

Fig. 2. Frequency distribution of net energy gain obtained from simulations of eiders feeding in three different habitats for one day (see Methods). The net energy gains do not include overnight and flying costs and exclude time spent roosting. The F ratio is 4 58 for crabs-mussels (P < 0.001, df = 7, 26), 1 62 for mussels-urchins (P > 0-05, df = 26, 8) and 7-45 for crabs-urchins (P< 0-01, df = 7, 8).

P < 0.001) and 7*5 times higher than when feeding on urchin in barrens (df = 7, 8, P < 0-01).

The differences in eider feeding between kelp and

Agarum beds suggest that feeding on blue mussels can be considered a 'safe' strategy because it results in a steady food intake, whereas feeding on crabs can be considered as 'risky' due to the associated

high variance in intake. Therefore, habitat selection may be influenced by the variance associated with the foraging process and accordingly common eiders

should behave as risk-sensitive foragers. We have

shown above that only small-flock individuals use the Agarum habitat. Thus, we hypothesized that the differences observed in habitat selection between flocks of different sizes is related to their body condition and predicted that large-flock individuals would be in better condition, and thus heavier, than small-flock individuals. To test this hypothesis we compared the body mass (corrected for stomach and faecal content) of adults taken from small and large flocks in different months of the winter (Table 7). In a first step, we tested whether the size of eiders, based on four morphometric measurements (wing, tarsus, bill and keel length), would differ between

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607 M. Guillemette, R. C. Ydenberg & J.H. Himmelman

Table 7. Mean body mass in g ? SD of adult common eiders found in large (>300) and small (<30) flocks for three different months of winter. The P values correspond to Mann-Whitney U tests (one-tailed) of the hypothesis that large-flock individuals are heavier than small-flock individuals

Month Sex Large flock Small flock P value

Jan Male 2123? 122 1965?207 0-017

(n) (19) (11) Female 1884 + 101 1662? 183 0-010

(n) (12) (5) Feb Male 2116 ? 138 1965 ? 132 0-006

(n) (6) (22) Female 1874 ? 86 1715 + 162 0-024

(n) (4) (22) Apr Male 1971 ? 41 1955 + 114 0-450

(n) (4) (25) Female 1902 ? 90 1816 ? 137 0-095

(n) (3) (24)

flock size and lead to differences in body mass. We found no significant differences in any of these measurements (ANOVA, P > 0.05). As predicted, however, large-flock individuals were heavier than small-flock individuals. Adult males and females from large flocks were significantly heavier than those from small flocks, for January and February (P < 0.05), but not in April (P > 0-05). Since there is a good correlation between body mass and body fat in common eiders (Milne 1976; Parker & Holm 1990; M. Guillemette, unpublished), we can con- clude that large-flock eiders were in better condition than small-flock individuals.

SENSITIVITY ANALYSIS

To evaluate to what extent the assumed foraging costs affected our estimates of profitabilities, we conducted a sensitivity analysis. We increased the costs of diving, handling and pausing, respectively, and computed the profitabilities obtained as a per- centage change of the original estimates (Table 8). For each of the prey, these analyses indicated that increases in activity costs by as much as 50%, affected the outcome by < 12%. These small changes indicate that for all of the prey the cost of foraging is small compared to the gains. We also tested the effect of errors in the estimate of prey size (Table 8), because our measures of profitabilities were based on the assumption that the average prey found in the stomach closely corresponded to that which we saw being handled at the surface. This analysis indicated that an error of 10% in the numbers of mussels swallowed underwater would have increased slightly the estimate of energy intake (13%). However, errors in estimating the size of urchins and crabs could have a greater effect on the estimates of profitability (28% to 46%). This is related to the logarithmic relationship of prey size to energy

Table 8. Sensitivity of net energy intake to errors associated with the assumed foraging costs and estimated average prey size

Foraging activity Percentage deviation from prey size and original estimate percentage change Mussels Urchins Crabs

Diving + 50% ?7-8 ?4 3 ?6.2 Handling ? 50% - ?6 9 ?1-9 Pausing?50% ?5 8 ?11-5 ?6-2 Prey size + 10%* +13 1 +27-6 +42-8 Prey size- 10% -13 1 -42 3 -45.6

* Prey size for mussels is considered as the number of individuals captured during one dive.

content; at a point the energy content of a prey increases faster that its size. The size of urchins selected by eiders was between 10 and 46 mm, based on 46 urchins found in the oesophagus of shot birds. It is plausible that the smaller urchins in this sample had been swallowed underwater, and it is thus poss- ible the handling times measured would not match the sizes of urchins captured. On the other hand, it is unlikely that crabs would have been swallowed underwater as we did not find crabs measuring <3 cm in carapace length in eider stomachs. An error in our estimate of the size of crabs is therefore unlikely. However, possible errors for urchins would not change our conclusion that urchins are less profitable than mussels and crabs.

Discussion

DIET AND FORAGING BEHAVIOUR

The diet of eiders is characterized by a low energy content per unit live mass as prey are swallowed whole and include shells, tests and carapaces (Table 3). One consequence of this is that eiders must process a large amount of material in order to meet their daily energy requirements (c. 2 kg). Moreover, M. Guillemette (unpublished) calculated that the digestion rate is much slower than the ingestion rate. We suggest that resting after a meal provides time to process a part of the food ingested and to lose mass by defecation and excretion. It follows that resting bouts can be considered as an obligatory part of the foraging behaviour of the eider. Together these considerations stress the importance of measuring the intake rate at the scale of a foraging cycle or a day, as we did in this study, in order to take into account the hidden handling that is occurring within the digestive system (Hixon 1982).

The feeding behaviour of eiders is influenced largely by the type of prey eaten. Dive cycles differ significantly depending on prey type, size and abun- dance. No previous study has examined the effect of prey size on the feeding behaviour of diving birds. The most obvious consequence associated with the

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608 Energy intake in wintering common eiders

capture of large prey is the need to include a handling component at the surface which increases the dur- ation of a dive cycle. Prey density also influences the duration of dive cycles. For example, when prey density is high, as when eiders feed in kelp beds and urchin barrens, diving time is low compared to when eiders feed on the scattered crabs in Agarum beds. Similarly, Draulans (1982) and Tome (1988) de- monstrate experimentally that diving time in benthic diving ducks increases as prey density decreases. In contrast to our study, in these studies prey type was constant.

PREY SELECTION AND THE ENERGY

MAXIMIZATION HYPOTHESIS

Blue mussels and spider crabs are highly selected by common eiders in winter (Table 2). Both these prey are rare in the environment relative to their frequency in the diet. Mussels occur in patches in kelp beds, which cover only 13-1% of the 0-6m depth range. Crabs occur in low numbers scattered through Agarum beds, which represent 44-6% of the 0-6m depth range (Guillemette 1991). In con- trast, urchins occur in high numbers throughout the sublittoral zone. As a result, the selectivity index for the urchin was low in spite of its common occurrence in the eider's diet (Table 2).

We found strong differences in prey selection by eiders in flocks of different sizes. This is consistent with the observation of Guillemette (1991) that flock size in eiders is related to the type of habitat selected. Our data on prey composition and selection (Tables 1, 2) indicate that large-flock eiders specialize on mussels and eat urchins only as an accompanying prey. On some occasions we observed that urchins were the last item of a meal in the stomach of large- flock eiders, suggesting that selectivity decreases during the course of a meal. This observation is supported by theoretical results (Beauchamp, Guillemette & Ydenberg, in press) which indicate that selectivity in eiders decreases with satiation level. In contrast to large-flock eiders, our analysis shows that small-flock eiders use the habitat dif- ferently and at times feed solely in either urchin barrens or Agarum beds during a meal (Table 1).

Our estimates of energy intake for small-flock eiders are consistent with the energy maximization hypothesis even though eiders are foraging in a multifood system, where there is much variation in prey size, density and energy content. Mussels and crabs are actively selected by eiders and correspond to the most profitable prey, whereas urchins are not preferred and permit only a low energy intake. Thus, food and habitat selection can increase the energy intake in wintering eiders. However, urchins are often eaten even though the selectivity index for this prey is low. One possible explanation lies in the consideration of the digestive process. Perhaps

eiders need to keep their stomachs full in winter so that digestive output is maximized: the green sea urchins are ubiquitious prey and not eating them could result in a cost associated with having an empty stomach. Another possible explanation is related to our estimate of the average size of urchins eaten by eiders. It is plausible that a portion of the urchins found in eider stomachs are swallowed underwater and the urchins observed being handled at the surface are the larger ones. This error would result in an underestimation of our measure of the net energy intake by as much as 40%. Although such an error in the estimate of urchin profitability is plausible, the conclusion remains that urchins are unprofitable compared to mussels and crabs.

ALTERNATIVE STRATEGIES AND CONCLUSION

Our study suggests that when eiders are searching for crabs in the Agarum beds they are behaving as risk-prone foragers. Cartar (1991) points out that the observation of risk-proneness in wild predators is impressive given the host of alternative strategies available. In the case of the eider, these include (i) selecting a diet that permits a higher energy intake, (ii) minimizing the energy expended, and (iii) increasing the time spent foraging. It is unlikely that eiders can select a diet of higher quality in our study area given the prey available in the subtidal zone are mostly unprofitable echinoderms and hard- shelled molluscs (Guillemette 1991). Eiders may in some way minimize energy expenditure to decrease the energy gain required for energy balance. One consequence of the poor condition and low body mass of small-flock eiders is that it may reduce energy expenditure for maintenance. Freed (1981) shows that female house wrens lose mass just before working intensively to feed their nestlings and inter- prets this as an adaptation rather than a stress. Although this is plausible for birds engaged in repro- ductive activities, since it could increase their fitness in terms of the number of chicks raised, it is unlikely for birds outside the reproductive period. Recent evidence supports the hypothesis that body mass (and reserves) in ducks in winter is positively corre- lated with the probability of survival (Haramis et al. 1986; Hepp et al. 1986). This is because metabolic reserves can be seen as an insurance against unpre- dictability in food abundance and weather conditions (Lima 1986 and references therein). The obvious alternative to the risk-sensitive strategy for a bird in winter is to increase the time spent feeding. For an eider in bad condition it could be better to spend a higher percentage of time feeding on mussels than to 'gamble' on catching crabs in the Agarum zone. Eiders spent 61% of their time ingesting prey in mid-winter when foraging on mussels in kelp beds (Table 4) and then decreases to 40% in the spring (M. Guillemette, unpublished). This suggests that

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609 M. Guillemette, R. C. Ydenberg & J.H. Himmelman

the proportion of time spent ingesting prey observed in mid-winter is the maximum attainable for these birds.

One important corollary of this risk-sensitive interpretation is that starvation is a probable event in eiders during winter. Preliminary determinations of total lipid content in wintering eiders show that total body fat in adult males ranges from 17 to 170 g (M. Guillemette, unpublished). This is very low for a bird the size of an eider. Moreover, massive die- offs of eiders have been reported during the spring migration along the Beaufort Sea and were associated with the absence of open water in this region (Barry 1967). Such die-offs have not been observed in winter in the Gulf of St. Lawrence even though this region can have extensive ice cover for long periods of time (Markham 1980; personal observation). In addition to preclusion of feeding, extensive ice cover would increase energy expended in flight, forcing eiders to migrate to more suitable regions. Thus, we have no difficulty imagining that starvation could be a major cause of natural mortality in wintering eiders. In this context, it would be highly adaptative for individuals in bad condition to select the Agarum beds because the survival probability of this habitat is greater than kelp beds. The question of whether our sample of shot eiders was representative of the entire population is also pertinent to our risk- sensitive interpretation. Large-flock eiders (>300) represent 95% of the population whereas small- flock eiders (<30) constitue less than 2% (Bourget, Dupuis & Whitman 1986; M. Guillemette, unpub- lished). Some authors indicate that ducks flying alone or foraging in small flocks either use the habitat differently or are in poor physical condition (Bain 1980; Hepp et al. 1986). Our study indicates that small-flock eiders both use the habitat dif- ferently and are in worse condition than large-flock individuals. We suggest that small-flock eiders behave as risk-prone foragers and seek the Agarum habitat to enhance their survival. An experiment in which eiders are captured and starved, and then released for determination of their subsequent selection of habitat and prey, is required to further test the applicability of risk-sensitivity theory to eiders foraging in winter.

Acknowledgments

We would like to thank L. Gauthier, A. Genereux and V. Lesage for their assistance and Drs G. Beauchamp, C. Carbone, R.V. Cartar, L.A. Giraldeau, J.N. McNeil, A. Reed and an anonymous referee for their critical comments on the manuscript. This study was supported by the Minister of Supply and Services Canada (contract 14sd.ka313-5-2123), the Canadian Wildlife Service, the Park Branch of Environment Canada and through a grant of the Natural Sciences and Engineering Research Council of Canada to J.H.H.

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Received 24 May 1991; revision received 20 January 1992

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