Yves Cherel

ALTERNATIVE FORAGING STRATEGIES AND RESOURCE ALLOCATION BY MALE AND FEMALE WANDERING ALBATROSSES

Allocation processes play a central role in life history theories. Yet very few studies have been carried out on the link between foraging and life history in the context of allocation of resources. Here we report a study examining the relationship between foraging and allocation of resources in the Wandering Albatross Diomedea exulans of Crozet Islands. We simultaneously studied individual foraging strategies at sea and differential allocation to reproduction and storage by measuring the energy supplied to chicks and the variation of body mass of the adult. Satellite tracking and continuous monitoring of nest attendance by adults showed that while rearing a chick Wandering Albatrosses have two specific alternative foraging strategies. They either forage in short trips, short in duration and close to the colony over the southeastern slope of the peri-insular shelf, or in long trips far from the colony in the oceanic waters north of Crozet. On average, birds made five successive short trips before making a long trip. Chicks received a meal every 1.8 d and were fed with fresh prey, 72% squid and 24% fish, and a liquid fraction composed of oil and water. During short trips birds appear to rely to a great extent on Moroteuthis ingens, a squid species probably available in large numbers at the southeastern edge of the Crozet shelf. The measure of energy flows indicates that 74% of the energy delivered to the chick comes from short trips, whereas only 33.8% of the total energy is gained at sea during these trips. Males spent a greater proportion of their time foraging in short trips than females, and consequently chicks received 61.3% of their meals from males and 38.7% from females. Adult birds tended to lose mass after short trips and to lose more mass with increased duration of short trips, whereas they gained mass after long trips. They initiated long trips when their body mass was low. Although Wandering Albatrosses are able to provision their chicks at a rapid rate because of the proximity of an abundant resource, birds still have to forage far from the colony to restore their body condition. Estimates of energy yield explain this paradox, as they suggest that the rate at which prey is caught during short trips in shallow waters is half that during long trips in oceanic waters. The significance of the twofold foraging strategy in relation to food availability and foraging efficiency is discussed.

Diving Behavior and Energetics During Foraging Cycles in King Penguins

King Penguins are the second largest of all diving birds and share with their congener, Emperor Penguins, breeding habits strikingly different from other penguins. Our purpose was to determine the feeding behavior, energetics of foraging and the prey species, and compare these to other sympatric species of subantarctic divers. We determined: (1) general features of foraging behavior using time—depth recorders, velocity meters, and radio transmitters, (2) energetics by doubly labeled water, (3) food habits and energy content from stomach lavage samples, and (4) resting and swimming metabolic rate by oxygen consumption measurements. The average foraging cycle was ≈6 d, during which the mass gain of 30 birds was ≈2 kg. When at sea, the birds exhibit a marked pattern of shallow dives during the night, whereas deep dives of >100 m only occurred during the day. Maximum depth measured from 34 birds and 18 537 dives was 304 m, and maximum dive duration from 23 birds and 11 874 dives was 7.7 min. The frequency distribution of dive depth was bimodal, with few dives between 40 and 100 m. Overall, swim velocities when a bird was at sea averaged 2.1 m/s (N = 5), while descent and ascent rates of change in depth averaged 0.6 m/s for dives 150 m (N = 90). Night feeding dives occurred at a rate of ≈20 dives/h, and deep dives occurred at a rate of ≈5 dives/h. The energy consumption rate while resting ashore was 3.3 W/kg (N = 3) or 1.6 times the predicted standard metabolic rate (SMR). The average energy consumption rate while away from the colony was 10 W/kg (N = 8) or 4.6 x SMR, compared to 4.3 x SMR estimated from a time—energy budget. The latter value is based on an average metabolic rate of 4.2 W/kg for three birds while resting in 5°C water and 9.6 W/kg while swimming at 2 m/s, which was extrapolated from the average of three birds swimming at 1 m/s. The average energy intake based on 9 stomach content samples was nearly 24.6 kJ/g dry mass. The main prey by number are myctophid fish of the species Krefftichthys anderssoni and Electrona carlsbergi. It was concluded that: (1) feeding begins ≈28 km from the colony, (2) prey is pursued night and day through its vertical movements, (3) vertical distribution of the prey is reflected closely by diving habits of the birds, (4) deep—diving, for unknown reasons, is an important component of foraging success, (5) diving capacities of King Penguins are remarkable compared to other birds and many pinnipeds, and (6) calculated foraging energetics can be closely estimated from time—energy budgets.

NUTRITION, PHYSIOLOGY, AND STABLE ISOTOPES: NEW INFORMATION FROM FASTING AND MOLTING PENGUINS

Stable isotopes are increasingly used in animal ecology, but little attention has been paid to the underlying physiological processes accounting for changes in 15N/14N and 13C/12C ratios, for example, the influence of protein balance on δ15N values. We investigated a “professional” faster, the King Penguin (Aptenodytes patagonicus), to test the effect of long-term food deprivation on the isotopic signature of tissues that can be nondestructively sampled, i.e., blood and feathers. Fasting for 25 days induced a tissue 15N enrichment, thus leading to a moderate increase in the apparent trophic levels of penguins. As expected, 15N enrichment was higher in tissues with high protein turnover rates (e.g., plasma, 0.70‰) than in those with low turnover rates (e.g., blood cells, 0.24‰). Fasting decreased the δ13C value of plasma, which was due to an increase in its lipid content, as indicated by a concomitant rise in plasma C/N ratio. Finally, food deprivation induced a 15N enrichment in keratin (1.68‰), as indica...

Isotopic Discrimination between Food and Blood and Feathers of Captive Penguins: Implications for Dietary Studies in the Wild

Using measurements of naturally occurring stable isotopes to reconstruct diets or source of feeding requires quantifying isotopic discrimination factors or the relationships between isotope ratios in food and in consumer tissues. Diet‐tissue discrimination factors of carbon (13C/12C, or δ13C) and nitrogen (15N/14N, or δ15N) isotopes in whole blood and feathers, representing noninvasive sampling techniques, were examined using three species of captive penguins (king Aptenodytes patagonicus, gentoo Pygoscelis papua, and rockhopper Eudyptes chrysocome penguins) fed known diets. King and rockhopper penguins raised on a constant diet of herring and capelin, respectively, had tissues enriched in 15N compared to fish, with discrimination factors being higher in feathers than in blood. These data, together with previous works, allowed us to calculate average discrimination factors for 15N between whole lipid‐free prey and blood and feathers of piscivorous birds; they amount to +2.7‰ and +4.2‰, respectively. Both fish species were segregated by their δ13C and δ15N values, and importantly, lipid‐free fish muscle tissue was consistently depleted in 13C and enriched in 15N compared to whole lipid‐free fish. This finding has important implications because previous studies usually base dietary reconstructions on muscle of prey rather than on whole prey items consumed by the predator. We tested the effect of these differences using mass balance calculations to the quantification of food sources of gentoo penguins that had a mixed diet. Modeling indicated correct estimates when using the isotopic signature of whole fish (muscle) and the discrimination factors between whole fish (muscle) and penguin blood. Conversely, the use of isotopic signatures of muscle together with discrimination factors between whole fish and blood (or the reverse) leads to spurious estimates in food proportions. Consequently, great care must be taken in the choice of isotopic discrimination factors to apply to wild species for which no controlled experiments on captive individuals have been done. Finally, our results also indicate that there is no need to remove lipids before isotopic analysis of avian blood.

Using stable-isotope analysis of feathers to distinguish moulting and breeding origins of seabirds

Abstract To determine whether stable isotope measurements of bird feathers can be used to identify moulting (interbreeding) foraging areas of adult seabirds, we examined the stable-carbon (δ13C) and nitrogen (δ15N) isotopic composition of feathers of chicks and adults of black-browed albatrosses (Diomedea melanophrys) from Kerguelen Islands, southern Indian Ocean. Albatross chicks are fed primarily fish (75% by mass), the diet being dominated by various species of the family Nototheniidae and Channichthyidae which commonly occur in the shelf waters in the vicinity of the colony. δ13C and δ15N values in chick feathers, which are grown in summer in the breeding area, were lower than values in adult feathers, which are grown in winter (δ13C: –19.6‰ versus –17.6‰ and δ15N: 12.4‰ versus 15.7‰, respectively). No differences in δ13C and δ15N values were found in adult wing feathers moulted in 1993 and 1994 and in adult feathers formed at the beginning, middle and end of the 1994 moulting period. These data are consistent with adults moulting in the same area and feeding at the same trophic level from one year to the next and with no major changes in foraging ecology within a given moulting season; they suggest that foraging grounds were different in summer and winter and that these differed in their stable-isotope signature. Changes in both feather δ13C and δ15N values indicated feeding south of the Subtropical Front (STF) during chick rearing, which is in agreement with the known foraging ecology at this time and feeding north of the STF during moult. This, together with band recoveries from adult birds, indicates that black-browed albatrosses from Kerguelen Islands wintered in subtropical waters off southern Australia. The stable-isotope markers in feathers, therefore, have the potential for locating moulting areas of migratory seabird species moving between isotopically distinct regions and for investigating seabirds’ foraging ecology during the poorly known interbreeding period. Such information is needed for studies of year-round ecology of seabirds as well as for their conservation and the long-term monitoring of the pelagic environment.

PREY DISTRIBUTION AND PATCHINESS: FACTORS IN FORAGING SUCCESS AND EFFICIENCY OF WANDERING ALBATROSSES

Seabirds are considered to rely on prey that are patchily distributed and whose abundance differs greatly according to physical processes or water masses. However, very little information is available about the environmental factors and individual factors that affect the foraging success of marine predators. We studied the distribution of prey encounters, foraging success, and efficiency in different water masses and during two stages of the breeding season when energy requirements differed in Wandering Albatrosses (Di- omedea exulans) of known experience and sex. The birds were simultaneously fitted with satellite transmitters, stomach temperature sensors, and activity recorders. Only 27% of prey were captured in patches (distance between two prey , 1 km); the rest were caught at an average distance of 64 km. Prey in patches were smaller than isolated prey and were caught mainly at night. Diet analysis indicated that albatrosses preyed mainly upon adult squid: squid taken at night were smaller (bioluminescent species), whereas those taken during the day were larger (nonbioluminescent species). Birds spent more time foraging farther from the colony during incubation than during brooding, when their energy re- quirement was highest, but foraging effort (landings per hour, or kilometers per hour), foraging success (grams of prey per hour), and efficiency (grams of prey per landing per hour) were similar during the two stages. The rate of prey encounter and foraging efficiency did not differ between water masses or between oceanic and shelf-slope waters. We found no differences between the sexes in terms of foraging success and efficiency. Young, in- experienced individuals had foraging success and efficiency similar to those of older, ex- perienced birds but had a different strategy: they foraged more actively and caught more prey at night than did experienced birds. These results suggest strongly that Wandering Albatrosses rely on prey that are highly dispersed, catch few prey within the same patch, and do not adjust foraging effort according to energy requirements. The unpredictability of the location of prey and the type of prey caught by Wandering Albatrosses indicate that the species has a unique foraging strategy compared to most seabirds, which generally concentrate in more predictable foraging areas.

Distribution of trace elements in the tissues of benthic and pelagic fish from the Kerguelen Islands

New information on the concentrations of Cd, Cu, Hg and Zn in the liver, kidney and muscles of eight marine benthic and pelagic sub-Antarctic fish species are presented to determine the importance of these metals in the marine systems of the Kerguelen Islands. Compared to the reported metal concentrations in other Antarctic fish species, the present results are globally within the same range of concentrations, although Cd displayed a very high interspecific variability in liver and kidney. Indeed, the highest Cd concentrations in liver, ranging from 10.0 to 52.1 microg x g(-1) dry wt. but also the lowest Cd concentrations in muscles (<0.030 microg x g(-1) dry wt.) have been displayed by the pelagic Myctophidae Gymnoscopelus piabilis. Metal concentrations differences might be related to diet and feeding habits of benthic and pelagic fish species. However, Cd and Hg concentrations in the edible muscle are lower than the French limit values (<or=0.155 microg x Cd x g(-1) dry wt. and <or=1.51 microg x Hg x g(-1) dry wt.) for these toxic metals as well as for edible and non-commercially interesting fish species. Results for Cd in fish tissues are consistent with the hypothesis of Cd-enrichment in the polar food webs typically explained by essential elements depletion. In fact, Zn concentrations in fish from the Kerguelen Islands are comparable to those of other areas but low Cu concentrations in fish livers, ranging from 0.9 to 24.7 microg x g(-1) dry wt., might indicate low availability of this essential element in these sub-Antarctic waters.

Interactions between longline vessels and seabirds in Kerguelen waters and a method to reduce seabird mortality

Abstract A longline fishery for Dissostichus eleginoides has recently developed in the vicinity of South Georgia and Kerguelen islands, two internationally important breeding areas for procellariiform birds. The number of hooked birds and a method to reduce mortality were investigated during 13 days of fishing activity in Kerguelen waters in February 1994. Between 100 and 600 seabirds were always observed behind the longline vessel during daytime. The main ship-following species were the white-chinned petrel Procellaria aequinoctialis (67% of counts), giant petrels Macronectes spp. (8%) and the wandering albatross Diomedea exulans (11%), black-browed albatross D. melanophris (6%) and grey-headed albatross D. chrysostoma (2%). Only diving species were caught on the lines, i.e. the white-chinned petrel (n = 36) and the grey-headed albatross (n = 2). Marked differences in the mortality rate were observed between day and night (1·00 versus 0·38 birds per 1000 hooks), and at night when the decklights were on or off (0·59 versus 0·15 birds per 1000 hooks). Dumping of homogenized offal during line settings greatly reduced incidental capture of seabirds, mainly because birds were more attracted by offal than by hooked baits. We therefore propose that the dumping of offal during line settings should be included in the regulations of the longline fishery for Dissostichus in order to minimize seabird mortality.

Foraging white-chinned petrels Procellaria aequinoctialis at risk: from the tropics to Antarctica

In the Southern Ocean white-chinned petrels Procellaria aequinoctialis form the majority of the bird bycatch in longline fisheries. Satellite tracking of breeding birds from the Crozet islands and from South Georgia indicates that during incubation they have the longest mean foraging ranges ever recorded for a seabird, 2390 and 2190 km. Crozet birds travel to the coast of South Africa at 3495 km, into subtropical waters as well as to Antarctic waters. South Georgia birds reach the northern Patagonian shelf. In all these areas birds are potentially in contact with fisheries. These results indicate that conservation measures limited to Antarctic waters are insufficient to protect seabirds with such extensive foraging ranges.

Stable isotope evidence of diverse species-specific and individual wintering strategies in seabirds

Although there is increasing evidence that climatic variations during the non-breeding season shape population dynamics of seabirds, most aspects of their winter distribution and ecology remain essentially unknown. We used stable isotope signatures in feathers to infer and compare the moulting (wintering) habitat of subantarctic petrels breeding at two distant localities (South Georgia and Kerguelen). Petrels showed species-specific wintering habitat preferences, with a similar pattern of latitudinal segregation for all but one taxon. At both localities, δ13C values indicated that blue petrels (Halobaena caerulea) moult in Antarctic waters, South Georgian diving petrels (Pelecanoides georgicus) in the vicinity of the archipelagos and/or in the Polar Frontal Zone and Antarctic prions (Pachyptila desolata) in warmer waters. In contrast, common diving petrels (Pelecanoides urinatrix) showed divergent strategies, with low and high intrapopulation variation at South Georgia and Kerguelen, respectively. Birds from Kerguelen dispersed over a much wider range of habitats, from coastal to oceanic waters and from Antarctica to the subtropics, whereas those from South Georgia wintered mainly in waters around the archipelago. This study is the first to show such striking between-population heterogeneity in individual wintering strategies, which could have important implications for likely demographic responses to environmental perturbation.