558 INTRODUCTION Procellariiform seabirds (albatrosses, petrels, shearwaters) are unusual among other avian orders in that most of these so-called ‘tube-nose’ birds have a well-developed olfactory neuroanatomy (Bang, 1966) and good associated capabilities. Procellariiforms use, or have been suggested to use, their sense of smell in various behaviours including foraging (Hutchison and Wenzel, 1980), homing (Bonadonna et al., 2001), ocean navigation (Nevitt and Bonadonna, 2005) and even some social aspects such as individual recognition and mate choice (Bonadonna and Nevitt, 2004; Hagelin and Jones, 2007; Mardon and Bonadonna, 2009). Following Grubb’s pioneering experiments (Grubb, 1972), most of the early work investigated sensitivity to food-related scents by exposing wild seabirds to odorous stimuli such as cod liver oil-soaked sponges (Jouventin and Robin, 1983; Lequette et al., 1989), scented oil slicks (Hutchison and Wenzel, 1980; Nevitt et al., 1995; Nevitt, 1999; Nevitt et al., 2004) or aerosol plumes (Nevitt et al., 1995). These experiments provided an extensive list of procellariiform species for which olfactory foraging was supported, including storm petrels (Oceanites oceanicus, Oceanodroma leucorhoa), petrels (Pagodroma nivea, Macronectes giganteus, Daption capense, Procellaria aequinoctialis), shearwaters (Puffinus gravis, P. creatopus, P. griseus, P. puffinus, P. tenuirostris), fulmars (Fulmarus glacialis, F. glacialoides), albatrosses (Diomedea nigripes, D. chrysostoma, D. melanophris, Phoebetria palpebrata) and prions (Pachyptila sp.). The wandering albatross (Diomedea exulans, Diomedeidae, Linnaeus 1758) is the largest of the procellariiform seabirds and has the largest wingspan of any living bird. Its foraging activity usually takes it over thousands of kilometres of open ocean, where it feeds on a variety of squids that are captured or found dead at the surface (Cherel and Weimerskirch, 1999). Yet, the sensory mechanisms used in this foraging search are still not completely understood. Early experiments on the response of albatrosses to olfactory foraging cues did not provide conclusive results. For instance, black-footed (Hutchison and Wenzel, 1980) and light- mantled sooty albatrosses (Lequette et al., 1989) are regularly attracted to food-related odours. In contrast, wandering, grey- headed and black-browed albatrosses do not appear to be attracted to either cod liver oil or dimethyl sulphide (DMS)-scented oil (Lequette et al., 1989; Nevitt et al., 1995), though black-browed albatrosses significantly respond to pyrazine- and herring-scented stimuli (Nevitt et al., 2004). Such intricacy probably explains why albatrosses are commonly thought to hunt visually (Prince and Morgan, 1990; Warham, 1990; Nevitt et al., 1995). New elements from telemetric studies (Weimerskirch et al., 2005; Phalan et al., 2007) have recently improved our understanding of wandering albatrosses’ behaviours. For instance, foraging activity is greater during daylight, when they feed mainly on large, isolated squids using active flight search (Phalan et al., 2007). At night, however, they feed on small, aggregated and bioluminescent squid by switching to a ‘sit-and-wait’ strategy at the water surface, probably because of the limited visual cues available for an active search (Phalan et al., 2007). Using the same GPS data, Nevitt and colleagues (Nevitt et al., 2008) showed that some spatial behaviours of foraging wandering albatrosses are consistent with the The Journal of Experimental Biology 213, 558-563 © 2010. Published by The Company of Biologists Ltd doi:10.1242/jeb.032979 Insight of scent: experimental evidence of olfactory capabilities in the wandering albatross (Diomedea exulans) J. Mardon 1,2, *, A. P. Nesterova 1 , J. Traugott 3 , S. M. Saunders 2 and F. Bonadonna 1 1 Behavioural Ecology Group, Centre d’Ecologie Fonctionnelle et Evolutive – CNRS, Montpellier, France, 2 AECR Group, School of Biomedical, Biomolecular and Chemical Sciences, The University of Western Australia, Perth, Australia and 3 Institute of Flight System Dynamics, Technische Universitaet München, München, Germany *Author for correspondence (jerome.mardon@cefe.cnrs.fr) Accepted 22 October 2009 SUMMARY Wandering albatrosses routinely forage over thousands of kilometres of open ocean, but the sensory mechanisms used in the food search itself have not been completely elucidated. Recent telemetry studies show that some spatial behaviours of the species are consistent with the ‘multimodal foraging strategy’ hypothesis which proposes that birds use a combination of olfactory and visual cues while foraging at sea. The ‘multimodal foraging strategy’ hypothesis, however, still suffers from a lack of experimental evidence, particularly regarding the olfactory capabilities of wandering albatrosses. As an initial step to test the hypothesis, we carried out behavioural experiments exploring the sensory capabilities of adult wandering albatrosses at a breeding colony. Three two-choice tests were designed to investigate the birds’ response to olfactory and visual stimuli, individually or in combination. Perception of the different stimuli was assessed by comparing the amount of exploration directed towards an ‘experimental’ display or a ‘control’ display. Our results indicate that birds were able to perceive the three types of stimulus presented: olfactory, visual and combined. Moreover, olfactory and visual cues were found to have additional effects on the exploratory behaviours of males. This simple experimental demonstration of reasonable olfactory capabilities in the wandering albatross supports the ‘multimodal foraging strategy’ and is consistent with recent hypotheses of the evolutionary history of procellariiforms. Key words: Diomedea exulans, behaviour, multimodal, olfaction, vision, signal-detection theory. THE฀JOURNAL฀OF฀EXPERIMENTAL฀BIOLOGY