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.coral reef ͉ olfaction ͉ population genetics
While evidence is mounting that larval reef fish are active participants in the process of dispersal and settlement, the sensory and behavioural mechanisms by which these fishes disperse and return from their oceanic phase to the reefs remain unknown. On One Tree Island (Great Barrier Reef, Australia), we tested freshly collected animals in a large choice-flume on the shore. Here, we present the first evidence that larval reef fish (primarily apogonids) approaching the time of settlement are capable of detecting differences between ocean and lagoon water and prefer lagoon water. We also demonstrate that they sniff actively with well-innervated noses and that attraction to lagoon water was not affected by warmer or colder temperatures. We conclude that they used chemical signals to orient toward lagoon water. Finally, we describe ebb tide plumes of lagoon water that extend many kilometers from reefs. Such plumes could provide chemosensory cues for dispersal and settlement stages of reef fish as they develop swimming efficiency. We argue that fishes may imprint to reef odour as embryos and/or early larvae and that this could facilitate both retention near the natal reef and navigation toward reefs from greater distances.
Exclusive elimination of the sense of taste in fishes is not possible by severing ''the'' taste nerve as one can do in mammals, because their taste buds are sometimes spread over very large skin areas. For this reason the effects of taste ablation and the functions of the two specific taste systems of fishes have remained unknown.One taste system is innervated by the facial nerve (VII) subserving all the taste buds on the body skin, lips and anterior part of the mouth; the other is innervated by the vagal and glosso-pharyngeal nerves (IX and X) and contains all the taste buds on the posterior part of the mouth and gill arches. It is known that the catfish finds food by taste only, since destruction of peripheral smell does not interfere with food finding abilities; taste was found earlier to function as a true distance receptor. It also serves as a testing device controlling food intake. The interaction between the two taste systems became evident when selective ablations were performed, removing either the entire sensory area of the facial lobe or the entire sensory area of the vagal lobe in the dorsal medulla oblongata. In the former case the catfish was unable to localize food accurately and to pick it up; in the latter case the fish could not swallow the food, but had no problems in localizing or picking up the pieces. Thus, the two sensory (taste) inputs have distinct functions. The facial taste system operates in accurate localization by bilaterally steering the trunk musculature, and it also triggers the ''pick-up'' reflex (in combination with tactile inputs). The vagal taste system controls the swallowing reflex. Taste functions are essentially different from the functions of the olfactory system.
Chemical signals connect most of life's processes, including interorganismal relationships. Chemical signals identify biologically important targets for those who have the proper receivers. We assume that selection pressure can act on both the biochemical and the physiological regulation of the signal and on the morphological and neurophysiological filter properties of the receiver. Communication is implied when signal and receiver evolve toward more and more specific matching, culminating in well-known sex pheromone systems. In other cases, receivers respond to portions of a body odor bouquet that is released to the environment not as a (intentional) signal but as an unavoidable consequence of metabolic activity or tissue damage. Breath, sweat, urine, feces, their aquatic equivalents, and their bacterial and other symbiotic embellishments all can serve as identifiers for chemoreceptive animals interested in finding food or hosts. Body fluids released from damaged tissues and decay products from dead organisms can be particularly potent signals. Since all organisms must release metabolites in order to live, and sinceThe publication costs of this article were defrayed in part by page charge payment. This article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. §1734 solely to indicate this fact.any such release is a potential target of opportunity for predators and parasites, one may expect that several forms of chemical camouflage have evolved to obscure one's chemical presence. Both communication signals and camouflage depend on signal-to-background contrast or lack thereof: communication emphasizes contrast; camouflage works toward lower contrast.Contrast can be provided by chemical specificity of the signal (spectral contrast) and by temporal changes in concentration of the signal (dynamic temporal contrast). Spectral contrast is created by unique compounds and by unique mixtures of compounds, including ordinary ones. Temporal contrast emerges from the rate at which the concentration of a compound changes with time, including the repetition rate. Temporal changes reflect spatial patchiness and hold information for chemotactic behavior at different spatiotemporal scales. The two classical methods of camouflage, well known in the visual signal world, may also operate in the chemical signal world, although they are virtually unstudied. To avoid detection, animals with visual predators hide and remain motionless, or they look and move like their background; animals with chemically hunting predators may build impermeable shells and store urine and feces until it is safe to release them, or they may produce metabolites that match the environment in mixture composition. and temporal distribution.Unlike wave or wave-like propagation of acoustic, visual, and other electromagnetic signals, chemical signals disperse through the environment by molecular diffusion and bulk flow. At small spatial scales-in practice below 10 ,umdiffusion is a biologically useful transport mechanism and, g...
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.
The behavior of reef fish larvae, equipped with a complex toolbox of sensory apparatus, has become a central issue in understanding their transport in the ocean. In this study pelagic reef fish larvae were monitored using an unmanned open-ocean tracking device, the drifting in-situ chamber (DISC), deployed sequentially in oceanic waters and in reef-born odor plumes propagating offshore with the ebb flow. A total of 83 larvae of two taxonomic groups of the families Pomacentridae and Apogonidae were observed in the two water masses around One Tree Island, southern Great Barrier Reef. The study provides the first in-situ evidence that pelagic reef fish larvae discriminate reef odor and respond by changing their swimming speed and direction. It concludes that reef fish larvae smell the presence of coral reefs from several kilometers offshore and this odor is a primary component of their navigational system and activates other directional sensory cues. The two families expressed differences in their response that could be adapted to maintain a position close to the reef. In particular, damselfish larvae embedded in the odor plume detected the location of the reef crest and swam westward and parallel to shore on both sides of the island. This study underlines the critical importance of in situ Lagrangian observations to provide unique information on larval fish behavioral decisions. From an ecological perspective the central role of olfactory signals in marine population connectivity raises concerns about the effects of pollution and acidification of oceans, which can alter chemical cues and olfactory responses.
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