Bernice M. Wenzel

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). Cobbs (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 Leachs 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

Olfactory perception and bulbar electrical activity in several avian species

Abstract Our earlier work on the olfactory responses of pigeons has been extended to six other species of birds, viz., canary ( Serinus canaris ), bobwhite quail ( Colinus virginianus virginianus ), mallard duck ( Anas platyrhynchos ), turkey vulture ( Cathartes aura ), raven ( Corvus corax ), and blackvented shearwater ( Puffinus puffinus opisthomelas ). Heart rate and respiration were monitored in all of these forms during presentation of olfactory stimuli of pure air or bright light. In all but raven, canary and quail, the electrical activity of the olfactory bulb was also recorded through permanently implanted electrodes. Amyl acetate, pyridine, and trimethylpentane were used as olfactory stimuli with all species; the vulture and shearwaters were also tested with natural stimuli of decayed meat and ground fish, respectively. Olfactory bulb electrical activity showed characteristic vertebrate components such as inspiration-linked intrinsic spindles in the frequency range between 20 and 40 Hz, a large ac spike at the onset of odor stimulation that probably corresponds to the electro-bulbo-olfactogram of dc recording, and desynchronization as a result of visual stimulation during a period of relaxation. No consistent species differences were seen. Responses to amyl acetate and trimethylpentane were characteristically different across species. All forms but the raven showed significant somatic responses to some, but not all, of the odorous stimuli presented. Surprisingly, the raven failed to show such responses even to the visual stimulus. The somatic responses were more reliable in species with larger olfactory bulbs, such as the ducks and shear-waters, but were found in birds with extremely small bulbs as well. It seems fair to say that perceptual capacity for olfactory stimuli is likely to exist in all avian species but may differ widely in amount and significance.

Olfactory bulb ablation or nerve section and behavior of pigeons in nonolfactory learning.

Abstract The possible significance of the primary olfactory system for behavior that does not involve olfaction was examined in a visual learning experiment with pigeons. Four groups were trained, one with bilateral section of the olfactory nerve, one with bilateral destruction of the olfactory bulb, one with an equivalent amount of damage on the hyperstriatal surface bilaterally, and one with anesthesia only. The final task required pecking the left of two keys when both keys were lighted with color 1 and pecking the right when both were lighted with color 2. Training was done in several stages which involved learning to eat from the food hopper in the training box, learning to peck one key while it was lighted with the first color, transferring pecking to the other key, and finally learning the complete task. The two groups with damage in the olfactory pathway were significantly slower in learning to eat from the hopper, in learning to peck the first key, and in transferring pecking to the second key. It is suggested that the olfactory system participates in some way in general limbic system functions.

Electrical activity of the olfactory bulb of the pigeon

Electrical activity was recorded from the olfactory bulbs of pigeons by means of chronically implanted electrodes. 1. 1. Intrinsic activity, in the absence of odor stimulation, characteristically showed prominent bands at 1–5, 15–25 and 30–45 c/sec, although wide individual differences were noted. No correlation between electrode position and type of activity was found. 2. 2. When odorants were added to the air stream, one of two changes typically occurred in the bulbar electrical activity; viz., either a marked increase in spindle amplitude at lower frequencies than non-stimulated spindle activity, or a desynchronization and flattening of the trace. Each of the six odorants used produced a characteristic pattern although individual differences were noted here also, primarily in the amount of spindling or desynchronization present. Bilateral olfactory nerve section abolished all odorant responses and most of the 15–25 c/sec activity in all cases but had little effect on the high frequency components, while trigeminal sections produced no changes in any of the activity recorded. 3. 3. When odorant concentrations were systematically varied, changes in bulbar activity paralleled them such that, within certain limits, increases in concentration led to increases in either spindling or desynchronization, whichever response was occurring at the time. Absolute thresholds as measured by just noticeable alterations in the recorded activity were of the order of 10−8–10−10 moles/ml of odorant in air. 4. 4. A phenomenon termed “augmentation” was studied in which the bulbar response to odor gradually shifted toward more spindling and less desynchronization when the same stimulus was presented several times with interstimulus intervals between 5 and 15 min. A possible mechanism for this phenomenon is discussed.

Olfaction in Birds

If it were not for a long history of doubt concerning the existence and functioning of an olfactory system among birds, there would be no particular reason to single out this class for discussion. The tone for one prevailing attitude about birds’ sense of smell was set more than a century ago by the advice of Audubon, the American naturalist and painter of birds, who recommended that his readers “... abandon the deeply-rooted notion that this bird (the turkey vulture) possesses the faculty of discovering, by his sense of smell, his prey at an immense distance...” (1826, p. 173). Although it became known that at least some forms had well-developed olfactory epithelium, nerves, and bulbs, the ability to detect odors and to respond differentially to them remained a highly controversial topic. Anecdotes were exchanged in the literature to support each side, and contradictory results were reported from experiments of variably skillful design (see Soudek, 1927; Stager, 1964; Strong, 1911; and Walter, 1943 for reviews), the sum of which created a generally negative impression. This era of skepticism has been replaced recently by a more positive one, for which the work of Cobb (1960 a) is proposed as a suitable origin. He studied certain aspects of the comparative anatomy of the avian brain and included a section on the olfactory bulbs that provided impetus for a systematic consideration of the possibility of an olfactory system with different degrees of function in different avian forms.

The Olfactory System and Behavior

In 1933, Herrick proposed that “At all stages of cortical elaboration an important function of the olfactory cortex, in addition to participation in its own specific way in cortical association, is to serve as a nonspecific activator for all cortical activities” (p. 14). Among these activities he included overt behavior, learning, memory, and affective reactions. This theme from Herrick, so reminiscent of Sherrington’s description of the distance receptors as “the great inaugurators of reaction” (1906, p. 350), serves as the keynote for this article. The concern here is not with the physiology of olfaction as a specific sensory system, but rather with the contribution of the primary and secondary portions of the olfactory system to such patterns of behavior as Herrick mentioned, patterns that are not typically classified as olfactory. The terms olfactory system or direct olfactory system (Girgis, 1970) will be used to refer collectively to the olfactory mucosa in the nasal cavity; the fibers of the olfactory nerves, which originate in the mucosa; the olfactory bulb, where the mucosal fibers make synaptic contact with the second fibers in the pathway; and the secondary fibers, the courses of which are discussed below.

Electrophysiology of the Olfactory Pathway in the Pigeon

SummaryThis work is part of an extensive study of anatomical, physiological, and behavioral characteristics of the olfactory system of birds. The present report deals primarily with the evoked potentials recorded from the olfactory bulb and several forebrain sites following electrical stimulation of one olfactory nerve. Our previously reported results of degeneration following unilateral olfactory bulb lesions were confirmed by these physiological data, and basic agreement was also observed between the physiological characteristics of the pigeons olfactory pathway and those reported for mammals. Nerve conduction velocity is 0.2–0.4 m/s. Response latency in the olfactory bulb is 20–40 ms ipsilaterally and 2–5 ms longer contralaterally, with amplitudes to 4 mV and polarity reversal across the mitral-granular cell region. Responses in sites that show degeneration after bulbar lesions (ipsilateral cortex prepyriformis, lobus parolfactorius, and ventral hyperstriatum; contralateral paleostriatum) are biphasic, 2–5 ms slower than those in the bulb, and fail to follow repetitive stimulation. Those in other ipsilateral forebrain regions showing no degeneration (paleostriatum, caudal neostriatum, and anterior hyperstriatum) are polyphasic, are much slower than those in the bulb, and have smaller amplitudes. Unit activity in all of these sites was modified by olfactory nerve stimulation. Poststimulus time histograms of unit activity show firing patterns that were correlated with amplitude variations in simultaneously recorded evoked potentials.

Does the olfactory system modulate affective behavior in the pigeon

On the basis of his knowledge of the patterns of evolutionary development of the olfactory system and other forebrain structures, Herrick’ proposed that the olfactory cortex served an activating function for “all cortical activities.” In recent years, without addressing Herrick’s proposal directly, several investigators have provided evidence that is pertinent to it. In an extensive review of this topic, Wenzell concluded that a number of behaviors are altered by a greatly diminished olfactory input and that this effect is not readily explicable in terms of perceptual loss alone. One of the principal themes emerging from this review is the apparent lack of influence on the cognitive or problem-solving aspect of behavior, as compared with the motivational or affective aspect. Regardless of the species being studied, after reducing or removing olfactory input it is typical to find significant changes occurring in such characteristics as reactivity to handling, aggression, and shock-avoidance learning. By contrast, relatively little effect is reported for such tasks as lever pressing with different schedules of food reinforcement or complex visual discriminations reinforced by food. Because so much of this work has been done with rodents, a group of animals for which olfactory signals are of notable importance, it is difficult to determine the degree to which reduced olfactory input represents a loss of specific information rather than a more general effect. For this reason, we have chosen to work exclusively with the pigeon so that the contaminating influence of the cue value of olfaction can be minimized. Although good evidence exists3 that pigeons rely to some extent on olfactory cues for guidance in homing, no other segment of their behavior has as yet been shown to depend directly on odorous information. In addition to this fundamental advantage, the pigeon also presents a distinct anatomical advantage in the ease with which the olfactory nerve fibers can be completely sectioned as compared with the rat, for example, in which such an operation is much more problematic. In a series of reports beginning in 1968,4-6 several types of behavior in the pigeon were shown to be affected by bilateral removal of the olfactory bulbs or bilateral section of the olfactory nerves. No effect on the behaviors in question was observed following the control operation of unilateral removal of a superficial piece of the hyperstriatum dorsale approximately equal in size to that of the olfactory bulbs.

The effect of immunosympathectomy on the behavior of mice in aversive situations

Abstract Webster Swiss mice were almost completely sympathectomized during the first week of life by injections of nerve-growth-factor antiserum and were studied subsequently for their behavior on a test battery that included open field, water escape, water maze, shock avoidance runway, food-reinforced lever pressing, and jiggle-cage activity. Their performance was compared with that of three control groups, viz. saline-injected, handled, and nonhandled. The experimental group was significantly slower than the three control groups on the two water tests and the avoidance task; did not differ from the saline-injected group in lever-pressing; was less active in the open field than the two uninjected groups but more active than the saline group; and showed a tendency to be less active in the jiggle-cage than the other groups. These results support the hypothesis that the sympathetic nervous system influences behavior at least in aversive situations.

Effects of androgens on body weight, feeding, and courtship behavior in the pigeon

Abstract Adult male pigeons, some intact and some castrated in adulthood, were housed in individual cages kept in an isolated room with temperature and lighting controlled. Weekly measurements were made of ad lib. food intake and body weight for 4 mo after surgery. Castration was followed by a significant depression in body weight and by initially depressed but then progressively enhanced feeding. Food deprivation elicited an increase in food intake proportional to body weight loss, but castrates consumed less food at 100%, 90%, and 80% of ad lib. feeding weight than either intact birds or castrates treated daily with testosterone propionate (TP). Castrates gained weight and ate more than controls in response to daily treatments (im) with TP (6 mg/400 g) or 5a-dihydrotestosterone (DHT, 6 mg/400 g), while androstenedione (15 mg/400 g) and androsterone (15 mg/400 g) were ineffective. Administration of 100 mg DHT (sc) to castrates produced a significant enhancement of body weight without elevating the level of food intake. The biological potency of these diverse androgens on male courtship behavior was reciprocal to that for weight-promoting potency. The results suggest that the structural requirements of the androgen molecule for promoting body weight differ from those for stimulating sexual behavior.