Jelle Atema

Sensory biology of aquatic animals

This volume constitutes a series of invited chapters based on presentations given at an International Conference on the Sensory Biology of Aquatic Animals held June 24-28, 1985 at the Mote Marine Laboratory in Sarasota, Florida. The immediate purpose of the conference was to spark an exchange of ideas, concepts, and techniques among investigators concerned with the different sensory modalities employed by a wide variety of animal species in extracting information from the aquatic environment. By necessity, most investigators of sensory biology are specialists in one sensory system: different stimulus modalities require different methods of stimulus control and, generally, different animal models. Yet, it is clear that all sensory systems have principles in common, such as stimulus filtering by peripheral structures, tuning of receptor cells, signal-to-noise ratios, adaption and disadaptation, and effective dynamic range. Other features, such as hormonal and efferent neural control, circadian reorganization, and receptor recycling are known in some and not in other senses. The conference afforded an increased awareness of new discoveries in other sensory systems that has effectively inspired a fresh look by the various participants at their own area of specialization to see whether or not similar principles apply. This inspiration was found not only in theoretical issues, but equally in techniques and methods of approach. The myopy of sensory specialization was broken in one unexpected way by showing limitations of individual sense organs and their integration within each organism. For instance, studying vision, one generally chooses a visual animal as a model.

Smelling home can prevent dispersal of reef fish larvae

Many marine fish and invertebrates show a dual life history where settled adults produce dispersing larvae. The planktonic nature of the early larval stages suggests a passive dispersal model where ocean currents would quickly cause panmixis over large spatial scales and prevent isolation of populations, a prerequisite for speciation. However, high biodiversity and species abundance in coral reefs contradict this panmixis hypothesis. Although ocean currents are a major force in larval dispersal, recent studies show far greater retention than predicted by advection models. We investigated the role of animal behavior in retention and homing of coral reef fish larvae resulting in two important discoveries: (i) Settling larvae are capable of olfactory discrimination and prefer the odor of their home reef, thereby demonstrating to us that nearby reefs smell different. (ii) Whereas one species showed panmixis as predicted from our advection model, another species showed significant genetic population substructure suggestive of strong homing. Thus, the smell of reefs could allow larvae to choose currents that return them to reefs in general and natal reefs in particular. As a consequence, reef populations can develop genetic differences that might lead to reproductive isolation.

FUNCTION OF CHEMORECEPTOR ORGANS IN SPATIAL ORIENTATION OF THE LOBSTER, HOMARUS AMERICANUS: DIFFERENCES AND OVERLAP

Three of the lobsters main chemoreceptor organs, the lateral and medial antennules (representing smell) and the dactylus-propodus segments of the walking legs (representing taste), are physiologically quite similar. We examined their role in spatial orientation in a food-odor stimulus field.Control animals almost always oriented correctly and immediately to an odor plume. Lobsters with unilateral ablations of lateral antennules lost this ability, but did not show preferential turning toward the intact side. Unilateral medial antennule ablation did not affect orientation. Removal of all aesthetasc hairs from one lateral antennule caused loss of orientation ability less severe than unilateral ablation of the entire lateral antennule. Lobsters with unilaterally ablated lateral antennules and blocked walking leg receptors turned preferentially toward the side of the intact antennule.Thus, it appears that intact lobsters orient in odor space by tropotaxis principally using aesthetasc receptor input. The first...

Biomimetic robot lobster performs chemo-orientation in turbulence using a pair of spatially separated sensors: Progress and challenges

Abstract Lobsters are capable of tracking turbulent plumes to their sources faster than can be accomplished by estimating a spatial gradient from time-averaging the concentration signal. We have used RoboLobster, a biomimetic robot lobster to investigate biologically scaled chemotaxis algorithms using two point concentration sampling to track a statistically characterized turbulent plume. Our results identify the range of effectiveness of these algorithms and, with studies of lobster behavior, suggest effective strategies beyond this range. They suggest that a lobster’s chemo-orientation strategy entails an unidentified means of dealing with the intermittency of the concentration signal. Extensions of these algorithms likely to improve are discussed.

Spatial Information in the Three-Dimensional Fine Structure of an Aquatic Odor Plume

Turbulent odor plumes play an important role in many chemically mediated behaviors, yet the fine scale spatial structure of plumes has not been measured in detail. With the use of a newly introduced microelectrochemical recording technique, we have measured, in some detail, the fine structure of an aquatic odor plume in the laboratory. We sampled a turbulent odor plume at 10 Hz with a spatial sampling area of 0.02 mm2, approximately that of a chemoreceptor sensillum of the lobster, Homarus americanus. A 3-min record was sampled at 63 different sites in 3 dimensions (x, y, z). As expected from time averaging models, the mean values of pulse parameters such as height and onset slope were greatest near the source. However, what cannot be described by time averaging models is the instantaneous distribution of pulses: periodically high peaks with steep concentration slopes (well above the local average and far above predictions from averaging models) can be found far away from the source. However, the probability of above-average pulse heights decreases with distance from the source in x, y, and z directions. The most intense odor fluctuations occurred along the x axis (the cross-sectional center of the plume). Odor profiles were analyzed with three different models of sensory filters; logarithmic, probability, and temporal filters. This analysis indicates that features contained within the plume structure could be used as directional cues for orienting animals. It remains to be demonstrated that animals use such sensory filters to extract biologically relevant spatial information from odor plumes.

Field Observations of Social Behavior, Shelter Use, and Foraging in the Lobster, Homarus americanus

Over a three-year period (1978-1981) behavioral observations of the lobster, Homarus americanus, were made by snorkeling in a shallow cove. Three hundred and thirty-four (334) animals were individually marked and this was the only time they were disturbed. In summer, the resident population numbered about 30 animals. The size composition, activity patterns, and habitat use of this population are described in a companion paper (Karnofsky et al., 1989). Shelters are of prime importance in the life of the lobster. Lobsters spent most of their time in shelters, leaving only at night. They dug shelters under eelgrass, rocks, and boulders; shelter locations appeared clustered. Some animals changed shelters frequently whereas others occupied the same shelters for up to 10 weeks. Premolt behavior was characterized by multiple shelter use. Cohabitation in the same shelter occurred only during periods of pair formation: when a mature female shared a males shelter prior to and following her molt. We report the only field evidence for such courtship cohabitation. Food foraging behavior was rare (0.35 instances/observation hour); most foraging involved live prey. Similarly, intraspecific interactions were surprisingly infrequent (0.2 instances/observation hour) and most, by far, did not involve physical contact. Although puncture wounds suggested intraspecific aggression, actual observations of escalating fights were rare. Premolt residents were involved in 65% of the interactions observed. In 70% of the interactions the larger animal won. However, smaller males and females could successfully defend their shelters against larger females. We report results from three homing experiments. The results suggest that much of the time that resident lobsters spend outside shelters is used to remain familiar with their constantly changing physical and social environment.

The importance of the lateral line in nocturnal predation of piscivorous catfish

SUMMARY In a previous study we showed that nocturnal piscivorous catfish track the wake left by a swimming prey fish to locate it, following past locations to detect the present location of the prey. In a wake there are hydrodynamic as well as chemical signatures that both contain information on location and suitability of the prey. In order to determine how these two wake stimuli are utilised in prey tracking, we conducted experiments in catfish in which either the lateral line or the external gustation was ablated. We found that a functional lateral line is indispensable for following the wake of swimming prey. The frequency of attack and capture was greatly diminished and the attacks that did occur were considerably delayed when the lateral line was ablated. In contrast, catfish with ablated external taste still followed the wakes of their prey prior to attacking, albeit their attacks were delayed. The external taste sense, which was reported earlier to be necessary for finding stationary (dead) food, seems to play a minor role in the localisation of moving prey. Our finding suggests that an important function of the lateral line is to mediate wake-tracking in predatory fish.

Chemical orientation of lobsters, homarus americanus, in turbulent odor plumes

The lobster,Homarus americanus, relies upon its lateral antennules to make initial directional choices in a turbulent odor plume. To determine whether chemical signals provide cues for source direction and distance during orientation, we studied the search patterns of the lobster orienting within a turbulent odor plume. In an odor plume, animals walked significantly more slowly and most often up the middle of the tank; control animals (no odor present) walked rapidly in straight lines, frequently along a wall. Search patterns were not stereotyped either for the population of experimental animals or for individuals. Three different phases of orientation were evident: an initial stage during which the animals increased their walking speeds and decreased their heading angles; an intermediate stage where both the walking speed and headings were constant; and the final stage close to the source, where heading angles increased while walking speed decreased. During this last stage the animals appear to be switching from a distance orientation (mediated by the antennules) to a local food search (mediated by the walking legs) as evidenced by a great increase in leg-raking behavior.

Distribution of Chemical Stimuli

In the study of chemoreception, one encounters two principal difficulties that are unique to chemical stimuli. Stimulus qualities (i.e., the spectrum of all stimulatory chemical compounds) are not organized in one linear dimension such as the frequency spectra of mechanical and electromagnetic stimuli; and stimulus quantities (i.e., the distribution of the stimulus in space and time) cannot be expressed easily in mathematical formulations of stimulus dispersal comparable to the wave equation for radiating light and sound sources. Instead, the chemical spectrum of qualities consists of all reactive chemical compounds in the environment organized in what could be perceived as an unknown “n-dimensional hyperspace,” and the distribution of chemical stimuli from their source of release through the environment depends on molecular diffusion and on fluid dynamics of the carrier medium. At the spatiotemporal scale of micro- to millimeters and seconds, diffusion dominates the distribution process; at various larger spatiotemporal scales, chemical stimuli are dispersed by fluid motion. This chapter will focus on the distribution of chemical stimuli and its consequences for chemoreceptive processes, such as receptor physiology and stimulus acquisition behavior.

Behavior and substrate selection during larval settling in the lobster Homarus americanus

ABSTRACT During the molt from third- to fourth-stage, larvae of Homarus americanus metamorphose into their adult form and pigmentation. In the course of the fourth stage, their pelagic life changes to a benthic existence. Artificial substrate choice experiments and qualitative illumination experiments show that during the early fourth stage the phototactic response reverses from positive to negative. Together with positive thigmotaxis, this results in a choice of dark crevices. Among natural substrate choices, preferential settlement occurred on macroalgal-covered rocks, followed by rocks on sand, mud, and sand. Moreover, when no choice was given, settling occurred most rapidly on macroalgal-covered rocks (34 h), followed by scattered rocks on sand (38 h), and mud (62 h); no settling occurred on sand even two weeks after the last animal had settled on all other substrates. These animals continued to explore the sand substrate with dives to the bottom. Although mud was not a preferred substrate in choice tests, the animals that chose mud and those that were presented only with mud settled successfully and were immediately efficient in their burrowing behavior, constructing U-shaped tunnels even in the center of the aquarium without using a pebble or rock as a starting point. These laboratory tests confirm field observations that lobsters can successfully exploit a variety of substrates. They show that a substrate with preformed crevices is preferred for settling, but other substrates can be manipulated to make suitable burrows.