Olfactory Guidance in Foraging by Procellariiforms

-Systematic field experiments show that procellariiform birds, viz., Black-footed Albatrosses (Diomedea nigripes), shearwaters (Puffinus griseus, P. creatopus, P. puffinus, P. bulleri, and P. tenuirostris), Northern Fulmars (Fulmarus glacialis), and storm-petrels of several species, are consistently attracted to sources of food-related odors under natural conditions at sea with controlled visual cues. They approach predominantly from downwind, in proportions above control levels, when food odors are presented as surface slicks, slicks spread in large shallow pools of plastic floating on the ocean, and by saturated wicks on free-floating rafts. Control stimuli and odorous materials unrelated to food do not attract procellariiforms. Birds of other orders are not attracted by any odorous stimulus, and approach the areas from all directions only when discrete visual stimuli are added. Observations and photographs reveal a flight pattern displayed only by procellariiforms in their apparent foraging approaches to food-related stimuli. Tube-nosed birds are most numerous under conditions of reduced visibility, high winds, large swells, and turbulent ocean surface. The results of this study strongly support the view, previously based on comparative anatomy and uncontrolled observations, that procellariiforms use olfaction in locating food. The ethology of olfaction is still largely unexplored in all vertebrates, and notably so for birds. Among avian olfactory systems, the nasal architecture and olfactory bulbs of the procellariiforms are impressive (Bang 1965, 1966, 1971). Cobb's (1960) measure, the ratio of olfactory bulb diameter to the largest diameter of the cerebral hemisphere, places tube-nosed species in 10 of the first 12 ranks for the 151 species among 23 orders on which measurements have been made (Bang 1971). These high values range from 0.27 for the Northern Fulmar (Fulmarus glacialis) to 0.37 for the Snow Petrel (Pagodroma nivea). The two other highest-ranking species, the Brown Kiwi (Apteryx australis) in rank 2 and the Turkey Vulture (Cathartes aura) in rank 10, have already been shown to respond discriminatively to appropriate food odors (Stager 1964, Wenzel 1969, 1971). The Rock Dove (Columba livia), now thought to be partly dependent on olfactory cues for homing (Papi et al. 1978, Keeton 1979), falls in midrange with a ratio of 0.17. Anecdotal evidence has long suggested that procellariiforms can distinguish odors (for review see Wenzel, in press). Some species can be attracted over long distances by griddle drippings, especially bacon fat, poured on the ocean surface and they often collect more quickly when the fat or oil has been heated (Murphy 1936, Miller 1942, Kritzler 1948). Several species of albatrosses discriminate between slicks of paint or petroleum and bacon fat or whale oil (Murphy 1936, Miller 1942). Two Snow Petrels in captivity accurately found hidden pieces of herring either outside in the snow or concealed inside a room (Jouventin 1977). In addition to feeding, other features of procellariif rm biology also suggest the possibility of olfactory guidance. Many species eject redolent stomach oil when disturbed. Secretion from the uropygial gland is typically odorous, accounting for the wellkno n musky scent of many procellariiforms. Such compounds might serve as olfactory markers to aid in identifying individual nesting burrows, chicks, and mates in densely populated breeding colonies (Stager 1967). Members of several species must find their burrows when they are obscur d by fog, clouds, overlying forests, d rkness, or snow cover. Few controlled experiments have been attempted on the olfactory behavior of procellariiforms. Grubb (1974, 1979) studied th role of olfaction in the return of Leach's Storm-Petrel (Oceanodroma leucorhoa) to its nesting burrow. After approaching their island upwind at twilight or after dark and crashing through the heavy wooded cover, breeding birds typically walked upwind to their burrows, in contrast to the inconsistent orientation of nonbreeders. Grubb found