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Testing Olfactory Foraging Strategies in an Antarctic Seabird Assemblage

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Testing Olfactory Foraging Strategies in an Antarctic Seabird Assemblage The Journal of Experimental Biology 207, 3537-3544 3537 Published by The Company of Biologists 2004 doi:10.1242/jeb.01198 Testing olfactory foraging strategies in an Antarctic seabird assemblage Gabrielle Nevitt1,*, Keith Reid2 and Phil Trathan2 1Section of Neurobiology, Physiology and Behaviour, University of California, Davis, California 95616, USA and 2High Cross, British Antarctic Survey, Madingley Road, Cambridge CB3 OET, UK *Author for correspondence (e-mail: [email protected]) Accepted 19 July 2004 Summary Procellariiform seabirds (petrels, albatrosses and chinned petrels (Procellaria aequinoctialis) were sighted at shearwaters) forage over thousands of square kilometres least 1.8–4 times as often at pyrazine-scented slicks than for patchily distributed prey resources. While these birds at control slicks. Black-browed albatrosses (Diomedea are known for their large olfactory bulbs and excellent melanophris) were only sighted at pyrazine-scented slicks sense of smell, how they use odour cues to locate prey and never at control slicks. Wilson’s storm-petrels patches in the vast ocean is not well understood. Here, we (Oceanites oceanicus), black-bellied storm-petrels investigate species-specific responses to 3-methyl pyrazine (Fregetta tropica), great shearwaters (Puffinus gravis) and in a sub-Antarctic species assemblage near South Georgia prions (Pachyptila sp.) were sighted with equal frequency Island (54°00′ S, 36°00′ W). Pyrazines are scented at control and pyrazine-scented slicks. As expected, compounds found in macerated Antarctic krill (Euphausia responses to herring oil were more common. With the superba), a primary prey item for many seabird species in exception of great shearwaters (Puffinus gravis), each of this region. To examine behavioural attraction to this these species was sighted up to five times as often at slicks odour, we presented birds with either scented or scented with herring oil compared with control slicks. ‘unscented’ vegetable oil slicks at sea. As a positive control Together, the results support the hypothesis that Antarctic for our experiments, we also compared birds’ responses to procellariiforms use species-specific foraging strategies a general olfactory attractant, herring oil. Responses to that are inter-dependent and more complex than simply pyrazine were both highly species specific and consistent tracking prey by scent. with results from earlier studies investigating responses to crude krill extracts. For example, Cape petrels (Daption Key words: procellariiform seabird, olfaction, smell, odour cue, capense), giant petrels (Macronectes sp.) and white- pyrazine, petrel, albatross, shearwater. Introduction Procellariiform seabirds (petrels, albatrosses and productive area is found, birds switch to an area-restricted shearwaters) forage over thousands of kilometres for patchily search strategy to pinpoint ephemeral prey patches (see Nevitt distributed prey resources using their sense of smell. and Veit, 1999). During area-restricted search, hunting Procellariiforms have among the largest olfactory bulbs of any strategies vary according to species and feeding conditions. For bird (Bang, 1965, 1966; Wenzel, 1987; Wenzel and Meisami, example, some species may track prey using their sense of 1990). While the olfactory abilities of many tubenosed species smell whereas others may be better adapted to use visual cues have been noted in the scientific and popular literature for well to locate prey patches, either by spotting prey directly or by over 100·years (reviewed by Warham, 1996), we are only seeing aggregations of other foraging seabirds alighting on the beginning to understand the variety of complex behavioural water (Silverman et al., in press). strategies that different species use to hunt by smell. We have been investigating foraging strategies used in area- Current theory suggests that procellariiform seabirds use restricted search in the procellariiform seabird assemblage in olfactory cues to forage at both large and small spatial scales the Atlantic sector of the Antarctic, near South Georgia Island (Nevitt and Veit, 1999; Nevitt, 2000, 2001). Over large scales (54°00′ S, 36°00′ W). This assemblage is made up of a number (hundreds or thousands of square kilometres), procellariiform of species that feed to a greater or lesser extent on a patchily seabirds detect productive areas for foraging by changes in the distributed prey resource, Antarctic krill (Euphausia superba; odour landscape. Dimethyl sulphide (DMS) has been e.g. Prince and Morgan, 1987). Thus, this species assemblage implicated as one of the odorants that birds use to identify areas offers a relatively simple system for investigating how of high primary productivity (Nevitt et al., 1995; Nevitt, 1999, different species use olfactory cues associated with krill to 2000; reviewed by Hay and Kubanek, 2002). Once a exploit prey patches. Given the extensive information on 3538 G. Nevitt, K. Reid and P. Trathan foraging ecology and diet of seabirds in this area (e.g. Croxall attracted to scents associated with macerated krill in et al., 1984, 1997; Croxall and Prince, 1987), we can also begin combination with social cueing by other birds. By contrast, to formulate and test hypotheses about the sensory ecology of smaller, less aggressive species may be better adapted to how different species forage. For example, it has been hunting prey opportunistically, primarily by tracking scents suggested that larger, more aggressive species are likely to be linked to krill or zooplankton grazing, such as DMS (Nevitt et al., 1995; Nevitt, 1999). A 70°00Ј 60°00Ј 50°00Ј 40°00Ј 30°00Ј The present study was designed to test this idea 40°00Ј by surveying responses of a much broader range of foraging procellariiforms to 3-methyl pyrazine, a scented compound found in extracts of macerated Antarctic krill (Kubota et al., 1989). Unlike crude extracts, 3-methyl pyrazine is colourless, and its concentration can be tightly 50°00Ј controlled. Thus, in this study, we were able to examine the behavioural responses to the odour cue independent of any visual cues associated with prey. Since many species in the area are conditioned to fishy-smelling compounds (Nevitt et al., 1995), we also tested birds’ responses to herring oil as a positive control for the experiment. 60°00Ј Materials and methods The study was carried out as part of the British Antarctic Survey’s Marine Life Science Core Program (Cruise # JR17; December 1996 – January 1997). Experimental trials were conducted along the Maurice Ewing Bank (MEB) where previous olfactory studies on DMS sensitivity were performed (Nevitt et al., 1995; Fig.·1). The 70°00Ј transect runs north towards the Sub-Antarctic Front (43°40′ W, 48°10′ S) and south to the Willis Islands (west of Bird Island; 38°00′ W, 54°00′ S.) As in previous studies (Nevitt et al., 1995), B 40°W 35°W working along this transect allowed us to sample olfactory responses from a wide range of species (Fig.·2) under variable environmental conditions that foraging birds typically encounter (Table·1). Experimental design 50°S Controlled experiments were designed to identify whether any procellariiform species might be attracted to 3-methyl pyrazine (‘pyrazine’), a scented component of macerated Antarctic krill (Euphausia superba; Kubota et al., 1989; Clark and Shah, 1992). As in other studies (Nevitt et al., 1995), our aim was to produce a downwind odour concentration in the nanomolar range. We did this by deploying pyrazine-scented Fig.·1. (A) The location of South Georgia Island relative to the Antarctic Peninsula. (B) Detail of the Maurice Ewing Bank (MEB) transect line and 23 stations. Experiments were conducted at stations 3, 4, 8, 9, 10, 55°S 13, 15, 19 and 20. Abbreviations: NGR, Northwest Georgia Rise; NEGR, Northeast Georgia Rise. Olfactory foraging in Antarctic seabirds 3539 55 Fig.·2. Species composition of birds along the Maurice Ewing Bank (MEB) transect as determined by survey 50 counts leading up to experimental stations (see text). 45 Species codes are: unpr, unidentified prion (Pachyptila sp.); waal, wandering albatross (Diomedea exulans); grsw, great 40 shearwater (Puffinus gravis); sopt, soft-plumaged petrel (Pterodroma mollis); bbsp, black-bellied storm-petrel 35 (Fregetta tropica); capt, Cape petrel (Daption capense); 30 blpt, blue petrel (Halobaena caerulea); ugpt, unidentified giant petrel (Macronectes sp.); bbal, black-browed 25 albatross (Diomedea melanophris); wisp, Wilson’s storm- 20 petrel (Oceanites oceanicus); ghal, grey-headed albatross (Diomedea chrysostoma); wcpt, white-chinned petrel 15 Mean percent composition (Procellaria aequinoctialis); knpn, king penguin (Aptenodytes patagonicus); sosw, sooty shearwater 10 (Puffinus griseus); roal, Southern royal albatross 5 (Diomedea epomophora); soal, sooty albatross (Phoebetria fusca); whpt, white-headed petrel (Pterodroma lessonii); 0 lmal, light-mantled sooty albatross (Phoebetria unprwaalgrsw sopt bbsp capt blpt ugpt bbal wisp ghal wcpt knpnsosw roal soalwhpt lmalundp spsk palpebrata); undp, unidentified diving petrel (Pelecanoides sp.); spsk, South polar skua (Catharacta maccormicki). vegetable oil slicks on the ocean surface at seven different bias, the order of slick presentation (control, pyrazine or locations along the MEB transect (Fig.·1B). Because herring) was randomised at each location, and deployments environmental conditions varied and surface slicks also were separated by at least one hour. We generally tested only presented visual cues to seabirds,
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