Amphibian water to land transition reveals physical limits of olfaction
The evolutionary transition from water to land required animals to sense chemicals under fundamentally different physical constraints. Because chemicals diffuse orders of magnitude more slowly in water than in air, aquatic olfaction faces significant challenges in odor capture. Yet, aquatic organisms exhibit strikingly sensitive and rapid chemosensory behaviors. Amphibians represent a powerful model to address this discrepancy because they transition from aquatic to terrestrial environments within a single lifetime. Here, we combine metamorphosis of adult axolotls with asymptotic theory and numerical simulations to show that odorants are captured by diffusion in tens of seconds in water compared with milliseconds in air; yet aquatic axolotls respond to odorants on a much more rapid timescale. Despite inefficiency, we find that proximity to large patches of highly concentrated odor supports sensation in the presence of flow. While aquatic axolotls did not display any respiratory flow, they display behavioral adaptations that generate flow and may even draw in odor through ciliary pumping. Thus, aquatic olfaction is slower and more wasteful than terrestrial olfaction, but behavioral adaptations support olfaction as an effective proximal sense.