UC Berkeley

Olfaction is an important process by which animals sense dissolved chemical cues (odors), in the surrounding fluid. Many organisms, including malacostracan crustaceans, use information provided by odors throughout their lifetimes to find suitable habitats for larval settlement, locate food, interact with conspecifics, avoid predation, locate mates, and mediate reproductive behaviors.

The first step in smelling chemical signals in the environment is capture of odorant molecules from the fluid around an organism. I used the crab, Callinectes sapidus, to study the physical process of odor capture. The lateral flagellum of a crab antennule, which bears a dense tuft of chemosensory hairs (aesthetascs), flicks through the water with a rapid downstroke and a slower return stroke. We measured fluid flow around and through the aesthetasc arrays on dynamically scaled models of lateral flagella to determine how such brush-like antennules sample the water around them. During the rapid downstroke of the flick, the closely spaced chemosensory hairs on the upstream side of the lateral flagellum splay apart passively because they are flexible. Water flows into the spaces between the aesthetascs in the array during the downstroke and then is retained within the array during the slower return stroke, when the hairs are pushed closer together into a clump on the downstream side of the flagellum. There is enough time during the return stroke and inter-flick pause for most of the odorant molecules in that trapped water sample to diffuse to the surfaces of the aesthetascs before the next flick, when a new water sample is taken. Thus, an antennule of C. sapidus takes a discrete sample of ambient water and the odorants it carries each time it flicks, so each flick is a sniff. I found that the flexibility of aesthetascs, which causes the gaps between aesthetascs to widen during the downstroke and narrow during the return stroke, has a big effect on water flow through the array of aesthetascs, but only if the antennule moves rapidly. Likewise, positioning the aesthetasc array on the upstream rather than the downstream side of the lateral flagellum only causes an increase in water speed within an array if the antennule moves rapidly. The change in antennule speed between the rapid downstroke and the slower return stroke of a flick is more effective at altering water speed within an aesthetasc array if the gaps between the aesthetascs are wide. Ambient water current enhances the sniffing by flicking antennules of C. sapidus.

Capturing odors from the surrounding water is important not only for adult crabs, but also for juvenile crabs, which can be up to two orders of magnitude smaller in length than adults. Sniffing by the flicking antennules of aquatic malacostracans occurs when water can flow into the aesthetasc array during the rapid downstroke and can be trapped in the array during the slower return stroke, which only occurs in a narrow range aesthetasc diameter, spacing, and flicking speed. Juvenile crabs have much smaller antennules than adults, but they do display flicking behavior. Are crabs able to sniff throughout their ontogeny? I used the Oregon shore crab, Hemigrapsus oregonensis, as a model organism to study the ontogeny of sniffing by antennules. Antennule flicking behaviors of crabs ranging in carapace width from 4 to 28 mm were recorded using high speed videography, and a morphometric analysis of one antennule from each of these crabs was conducting using scanning electron microscopy. Many features of antennule morphology (including aesthetasc diameter and length, antennule width, and number of aesthetascs) increased at a rate of only 28-60% the rate of increase in carapace width. Velocities of the downstroke and return stroke keep juvenile crabs within the range in which sniffing for malacostracan is possible. Furthermore, the aesthetascs on the antennules of juvenile crabs are bent and splayed apart more during the rapid flick downstroke than are those of adults. I modeled the exoskeletons of aesthetasc s of different sizes as a hollow, cylindrical cantilevers and calculated their deflection by the hydrodynamic force they experience during the downstroke. I found that the greater deflection of juvenile aesthetascs was not due to differences in antennule shape, but rather to ontogenetic changes in the material properties of the aesthetasc cuticle.

To investigate water flow within aesthetasc arrays due to flicking during ontogeny, we constructed dynamically scaled physical models of antennules representing animals at seven different stages of growth, from 5-mm to 25-mm carapace width. I used particle image velocimetry (PIV) to measure fluid flow within the array of each model. Average water speed within the aesthetasc array increased with carapace width for the downstroke, where water speed was consistently low in the array during each return stroke. For each carapace width modeled, the fraction of the dendrite-containing area of the array that was refreshed with new water was high during the downstroke and very low during the return stroke, supporting the hypothesis that crabs' ability to sniff starts as early as post-settlement and continues throughout a crab's lifetime.

The fluid dynamics of discrete odor sampling are well studied in several marine species (spiny lobster, blue crab, Oregon shore crab), but odor sampling is unstudied in their air-dwelling relatives. The physics of odor capture in air is different than in water. Air has a higher kinematic viscosity than water, affecting the flow around the antennule. Molecular diffusivities in air are typically three to four orders of magnitude higher than water, affecting the delivery of odor molecules to the surface of aesthetascs. The terrestrial hermit crabs (Anomura: Coenobitidae) live their entire adult lives on land. The antennules of terrestrial hermit crabs have arrays of short, leaf-like aesthetascs in an shingle-like arrangement, and crabs wave their antennules back and forth in a motion similar to flicking by marine crabs. To investigate odor capture by antennule flicking of a terrestrial hermit crab, I examined: 1) the kinematics of antennule flicking by filming flicking behavior of ruggie hermit crabs (Coenobita rugosus); and 2) the antennule morphometrics by collecting the antennules of each crab for scanning electron microscopy. I constructed a dynamically scaled physical model of the antennule, and particle image velocimetry (PIV) was used to measure fluid flow around the model. PIV results show that no air flows between the aesthetascs on the antennule's array during either the downstroke or return stroke. Although terrestrial hermit crabs share similar antennule movements and morphological features with marine crabs, they do not discretely sample odors. An odor-transport model based on the convective currents measured with PIV and diffusion of a common odorant was created to investigate the odor-capture performance of the antennule of C. rugosus in air and in water. This model revealed that odor-capture performance is three times higher in air than in water. In air, the majority of odor capture occurred during the downstroke (99.9%). In water, the trend was reversed and the majority of odor capture occurred during the return stroke (94%). Flicking movements serve to increase the probability of encountering odors in environmental air flow, and the high molecular diffusivity in air removes the need for a fluid-trapping return stroke, as seen in aquatic malacostracans.