Orientation by Olfaction Trails Flows and Plumes

Many animals are guided by olfaction. They are able to detect the gradient of molecule concentration find the source that emits these molecules. However, homogeneous gradients are rare on Earth, because molecules are transported by the media of air and water and therefore do not disperse in a homogeneous fashion. Rather, they are subject to diffusion and turbulence, processes that cause them to be very unequally and patchily distributed after a short distance of travel from the source. Animals have adapted to this pattern of molecule dispersal on Earth and have acquired optimal strategies to detect the source of such turbulent plumes. The best way of doing so requires the following simple rules (Figure 7): first, if a substance is detected, its most likely origin is upwind or upstream. So, first of all, move against the flow. Second, if you fail to detect it again, move across the flow direction in a zigzag fashion. Third, the moment the substance is detected again, move upstream or upwind. A recent theoretical study has shown that this is actually the only strategy that assures that an animal finds the source of a substance in turbulent media. Pinpointing the source of an odor is important for animals in a variety of tasks: to find food, like carcasses and flowers, to find mates, in which case very specific pheromones are being produced, and released into the medium, to detect predators and to find places that carry a specific olfactory signature, like a nest marked with pheromones or a river inlet. Some animals use odors to mark homes, territorial boundaries, or, in the case of ants, pheromone trails to a food source that serve to recruit and guide nest mates to such a significant place. It has even been suggested that locally varying blends of odors can be used like a map by animals, helping them link places they visit by their distinct olfactory signatures.

Odors in the context of orientation and navigation have some interesting and unique properties: in the case of pheromone markers or trails, for instance, they carry information, not only about the sender, but also about time. Since molecules diffuse, depending on their volatility, their ambient concentration will decline with time and thus indicate the time elapsed after they were deposited. Olfactory trails and signposts can also be made very specific, compared to visual or sound signals, and thus can help avoid unintended eavesdroppers. The problem with odors is that they are affected by the movement characteristics of the medium. So, marking a nest entrance, for instance, will only help in homing if returning animals are downwind from it. There is no signal to be detected from all other directions. For the same reason, it is also unclear at present - with the exception of rivers -how stable the distribution of natural odors is in the atmosphere and water, which is crucial for their utility as navigational aids, directional compass cues, and cues for localization. This gap in our knowledge is mainly a technical challenge at the moment, because monitoring biologically relevant chemical cues over long periods of time and with sufficient spatial and temporal accuracy is currently impossible to achieve. Being able to monitor, track, map, and modify olfactory information would be truly exciting, because many experiments with homing pigeons seem to suggest that they attend to olfactory information in one way or other when being released tens of kilometers away from their loft. These observations lead to the suggestion that birds may possess an olfactory map, knowing places and their relative locations by their unique olfactory signatures.

Flow direction

Flow direction

Flow direction

Flow direction

Flow direction

Flow direction

Ant Mark Pheromone

u = upwind turn c = casting

Figure 7 Orientation in turbulent pheromone plumes. (a) A flight path of a silk moth male in a pheromone plume. The open arrowhead marks the time when the pheromone release was switched off. Shortly afterward, the insects starts casting, flying perpendicular to the wind direction. Moth positions are shown every 67 ms. This is an example of a class of undirected locomotory reactions called 'kineses', in which the movement speed or the rate of turning depend on the intensity of a stimulus (Fraenkel and Gunn, 1961). (b) Principle of finding the source of a turbulent plume: if a molecule is encountered, move upwind or upstream ('u'); if no more molecules are encountered, move cross-wind or cross-stream ('c'). (c) The path generated by an optimal plume search algorithm. Dashed line encloses area of highest probability to encounter a patch of odor. Dots mark odor patch encounters. (a) Modified from Baker TC and Vogt RG (1988) Measured behavioural latency in response to sex-pheromone loss in the large silk moth Antheraea polyphemus. Journal of Experimental Biology 137: 29-38. (b) Modified from Kaissling K-E and Kramer E (1990) Sensory basis of pheromone-mediated orientation in moths. Verhandlungen der Deutschen Zoologischen Gesellschaft 83: 109-131, with permission. (c) Modified with permission from Balkovsky E and Shraiman BI (2002) Olfactory search at high Reynolds number. Proceedings of the National Academy of Sciences of the United States of America 99: 12589-12593, Copyright (2002) National Academy of Sciences, USA.

u = upwind turn c = casting

Figure 7 Orientation in turbulent pheromone plumes. (a) A flight path of a silk moth male in a pheromone plume. The open arrowhead marks the time when the pheromone release was switched off. Shortly afterward, the insects starts casting, flying perpendicular to the wind direction. Moth positions are shown every 67 ms. This is an example of a class of undirected locomotory reactions called 'kineses', in which the movement speed or the rate of turning depend on the intensity of a stimulus (Fraenkel and Gunn, 1961). (b) Principle of finding the source of a turbulent plume: if a molecule is encountered, move upwind or upstream ('u'); if no more molecules are encountered, move cross-wind or cross-stream ('c'). (c) The path generated by an optimal plume search algorithm. Dashed line encloses area of highest probability to encounter a patch of odor. Dots mark odor patch encounters. (a) Modified from Baker TC and Vogt RG (1988) Measured behavioural latency in response to sex-pheromone loss in the large silk moth Antheraea polyphemus. Journal of Experimental Biology 137: 29-38. (b) Modified from Kaissling K-E and Kramer E (1990) Sensory basis of pheromone-mediated orientation in moths. Verhandlungen der Deutschen Zoologischen Gesellschaft 83: 109-131, with permission. (c) Modified with permission from Balkovsky E and Shraiman BI (2002) Olfactory search at high Reynolds number. Proceedings of the National Academy of Sciences of the United States of America 99: 12589-12593, Copyright (2002) National Academy of Sciences, USA.

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