The underestimated role of olfaction in avian reproduction?

Abstract

Until the second half of the 20th century, it was broadly accepted that most birds are microsmatic if not anosmic and unable to detect and use olfactory information. Exceptions were eventually conceded for species like procellariiforms, vultures or kiwis that detect their food at least in part based on olfactory signals. During the past 20-30 years, many publications have appeared indicating that this view is definitely erroneous. We briefly review here anatomical, electrophysiological and behavioral data demonstrating that birds in general possess a functional olfactory system and are able to use olfactory information in a variety of ethological contexts, including reproduction. Recent work also indicates that brain activation induced by sexual interactions with a female is significantly affected by olfactory deprivation in Japanese quail. Brain activation was measured via immunocytochemical detection of the protein product of the immediate early gene c-fos. Changes observed concerned two brain areas that play a key role in the control of male sexual behavior, the medial preoptic nucleus and the bed nucleus of the stria terminalis therefore suggesting a potential role of olfaction in the control of reproduction. The widespread idea that birds are anosmic or microsmatic is thus not supported by the available experimental data and presumably originates in our anthropomorphic view that leads us to think that birds do not smell because they have a rigid beak and nostrils and do not obviously sniff. Experimental analysis of this phenomenon is thus warranted and should lead to a significant change in our understanding of avian biology.

Figure 1

Behavior frequencies recorded during four hours of observations (16 × 15 min in January) in male ducks that had their olfactory nerves sectioned bilaterally (black bars) and in control subjects (open bars). Frequencies were statistically compared in the two groups and asterisks above a pair of bars indicate a significant difference (p<0.05). A marked decrease in the expression of social displays and sexual behaviors was detected after the nerves section but aggressive behaviors (given or received) were not affected. Abbreviations: JGW: grunt-whistle; HU: head-up tail-up; DU: down-up; NG: neck grab; M: mount; COP: copulation; TH: threat; PE: peck; CH: chase. Modified from data in [3].

Figure 2

Seasonal changes from December to June of the percentage of male or female domestic ducks (Rouen breed) synthesizing two types of lipids in their uropygial (preen) gland: branched ester waxes and diester axes. The pattern of changes for unbranched ester waxes was similar to the pattern observed with branched esters. Drawn from data in [49].

Figure 3

Occlusion of the nostrils in Japanese quail does not lead to any significant change in sexual behavior but alters the expression of immediate early gene Fos in their brain. A. Photographs of the head of a male Japanese quail in which the nostrils were blocked by dental cement (arrow). B. Frequency of two sexual behaviors (mount attempts and cloacal contact movements) recorded in males that were either used as control (black columns) or had their nose blocked by dental cement (gray columns). C–D. Photomicrographs of sections through the preoptic area stained by immunohistochemistry for the immediate early gene Fos in a male that had been allowed to copulate in control condition (C) or a male which had copulated after his nose was blocked by dental cement (D). In both panels, Fos expression is illustrated in: (a) the caudal mPOA and the rostral BSTM at low magnification (4x objective); (b) the rostral BSTM at high magnification (40x objective); (c) the caudal mPOA at medium magnification (20x objective). The boxes in panel C indicate the position of the fields shown at higher magnification. Scale bars = 500 μm in a, 50 μm in b and 100 μm in c. CA, commissura anterior; FPL, fasciculus prosencephali lateralis. E. Numbers of Fos-immunoreactive (Fos-ir) cells observed in three brain areas of male quail that had been allowed to copulate with a female either in the normal condition (SEX) or after their nose was blocked with dental cement (SEX/PLUGGED). Cells where also counted in control birds that stayed in their home cage and were not exposed to a female (CTRL). *= p<0.05 compared to CTRL, #= p<0.05 compared to SEX. mPOA: medial preoptic area; BSTM: medial part of the bed nucleus striae terminalis. Redrawn from data in [97].

Figure 4

A. Photomicrographs illustrating zenk expression in the olfactory bulb of male quail that copulated with a female in the absence (left) or the presence (right) of a nasal plug. Scale bar = 100 μm. B. Numbers of zenk-immunoreactive cells observed in the olfactory bulb of male quail that had been allowed to copulate with a female (SEX; n=4) or copulated with that female after there nose was blocked with dental cement (SEX/PLUGGED; n=5). Control birds (CTRL; n=2) stayed their home cage and were not exposed to a female. Birds that showed, for unexplained technical reasons, no Zenk expression at all in the olfactory bulbs were removed from this analysis resulting in the reduced numbers of subjects mentioned here. Although the average difference illustrated here was not statistically significant, it became significant when results of the present subjects were pooled with results of other birds that had additionally their cloacal gland anesthetized before the behavioral tests (see [97] for additional description of these results). Redrawn from data in [97].