The Function of Bilateral Odor Arrival Time Differences in Olfactory Orientation of Sharks

Abstract

The direction of an odor signal source can be estimated from bilateral differences in signal intensity and/or arrival time. The best-known examples of the use of arrival time differences are in acoustic orientation. For chemoreception, animals are believed to orient by comparing bilateral odor concentration differences, turning toward higher concentrations. However, time differences should not be ignored, because odor plumes show chaotic intermittency, with the concentration variance several orders of magnitude greater than the concentration mean. We presented a small shark species, Mustelus canis, with carefully timed and measured odor pulses directly into their nares. They turned toward the side stimulated first, even with delayed pulses of higher concentration. This is the first conclusive evidence that under seminatural conditions and without training, bilateral time differences trump odor concentration differences. This response would steer the shark into an odor patch each time and thereby enhance its contact with the plume, i.e., a stream of patches. Animals with more widely spaced nares would be able to resolve smaller angles of attack at higher swimming speeds, a feature that may have contributed to the evolution of hammerhead sharks. This constitutes a novel steering algorithm for tracking odor plumes.

Laterality and Symmetry in Rat Olfactory Behavior and in Physiology of Olfactory Input

“…Similarly, bilateral odor sampling contributes significantly to odor localization in many species. This has been shown in fruit flies (Borst and Heisenberg, 1982;Duistermars et al, 2009;Gomez-Marin et al, 2010, sharks (Gardiner and Atema, 2010), rats (Rajan et al, 2006), and humans (von Bekesy, 1964;Porter et al, 2006). In principle, bilateral comparison of odor concentration provides instantaneous information about the odor gradient of the plume (Webster et al, 2001).…”

“…This may have provided the rat with enough time to sample the odor by moving its head from side to side to sample different parts of the odor stream. This strategy has been shown to be effective in odor localization in Drosophila larvae (Louis et al, 2008;Gomez-Marin et al, 2011). To address this issue, we tracked the position of the nostrils of three rats during the task.…”

From chemotaxis to the cognitive map: The function of olfaction

“…Some pinnipeds use their mobile vibrissae to haptically search the benthic sea floor for stationary prey, and others use the vibrissae to track the hydrodynamic trails of prey such as fish (23). Schools of highly mobile prey may represent an ephemeral food source that is easier to find than predict in the absence of olfaction, the main sensory modality of other marine carnivores, such as sharks (42), and even aerial marine piscivores, such as albatrosses (43). The pinniped loss of olfaction, combined with low predictability in prey movements, would decrease selection for spatial tracking (44) and pinnipeds may have deinvested in predicting and reinvested in detecting.…”

“…Across all spatial scales, fish orient to odorants by calibrating odor sampling to their lateral line perception of hydrodynamic trails (56). The smooth dogfish not only requires intact lateral lines to use odorant sources for orientation (18), but uses the internostril time delay to determine its location relative to the plume (42). Experimental studies of navigation in goldfish demonstrate that it is mediated by the medial pallium homologue in teleosts, the dorsolateral ventral region of the telencephalon (70).…”

Morphological Study of the Eye Bulb of the Hammerhead Shark, Sphyrna lewini (Elasmobranch: Carcharhinidae)

“…Also, the hypothesis of head shape alterations for better adaptions in the sensorial system with the development of structures associated to olfaction, expansion of the distribution of Ampullae Lorenzini and binocular sight. (Johnsen & Teeter, 1985;Kajiura, 2001;Kajiura, 2003;Kajiura et al, 2005;McComb et al, 2009;Gardiner & Atema, 2010). Given the variety of characteristics, the study aims to describe the anatomical constitution of the hammerhead shark eye bulb.…”