WFSC 448 – Fish Ecophysiology(Week 6 – 30 Sep 2010)

Sensory biology – Chemoreception

Major point: Physical and chemical properties of water dominate lives of aquatic organisms in ways largely alien to terrestrial vertebrates

For fish, nearly all aspects of life—food and predator detection, species and mating cue assessment, parental behavior, migration, etc.—depend on chemoreception. Different than our umwelt*—we experience a few chemicals that are volatile in air, through a thin interface of moist tissue. Fish live in the universal solvent and are literally imersed in water. Chemical senses are comensurately important to the increased information content of their medium.

*Umwelt (“oom-velt”): Brought to the field of ethology by Jakob von Uexküll—the world as it is experienced by a particular organism.

Chemoreception includes olfaction (smell) and gustation (taste).

Olfaction results from stimulation of sensory receptor cells in the olfactory organs within the “nose” which are innervated by the olfactory nerve (cranial nerve I).

Teleost brain showing major brain lobes and nerves: (I) olfactory (II) oculomotor (III), trochlear (IV), trigeminal (V), abducens (VI), facial (VII), auditory (VIII), glossopharyngeal (IX), and vagus (X).

Gustation is mediated by taste buds in the oral and branchial cavities, gill arches, and body exterior which are innervated by the facial, glossopharyngeal and vagus nerves (cranial nerves VII, IX, and X).

A third type of chemoreception is often recognized, usually referred to asa common or general chemical sense, mediated by alternative sensory receptors located on exposed body surfaces of a fish, and better developed in scale-less, bottom-living forms.

Taste buds are not involved; instead, the receptors are free nerve endings supplied by the spinal nerves. It is low in sensitivity compared to smell and taste. But importantly, it is yet another evolutionary channel that can be crafted into adaptation.

Structure/function of chemosensory organs The fish “nose” is composed of two channels

arrayed in a manner that they appear as nostrils.

The paired channels are called nares. Each naris is ciliated to create water flow over a bed of sensory cells.

Fluid ramming and branchial pumps (in some taxa) have evolved as well. The narial fold is like a hood scoop, acting to increase ventilation of fluid through a designed architecture, much like a racing car uses a hood scoop

This cell bed is a series of folded tissues (lamellae) covered with olfactory epithelia.

Feathery lamellae increase surface area and so allows for a larger number of receptors exposed to a larger laminar layer of water containing chemicals to be detected.

The conformation of chemoreceptive anatomy varies greatly among fishes. For example, hagfishes and lampreys have only a single medial naris. Scale-less fishes tend to be more dependent on body chemoreception, and the number and composition of lamellae varies by fish species and habitat. Olfactory morphology also varies ontogenetically. E.g.,

As a contrast among habitats, consider the three-spine stickleback, which relies mostly on vision to make its way in the world and accordingly has a minimized olfactory chamber (red box in next figure). Whereas, most eels rely heavily on olfactory cues and have large, elongate olfactory chambers with numerous (>60) lamellae.

In more derived fishes the nares have both channel openings on the body surface.

Hagfishes (Myxini), a very few teleosts (some uranoscopids and the bathydraconidgenus Gymnodraco), and, of course, the lungfishes (Dipnoi) have internal nares (exhalent openings into the pharynx) comparable to those of terrestrial vertebrates.

Why the lamellar structure?What is the cost?

Anterior nares

Olfactory sensitivity/acuity of the sense of smell is very high in many species of fishes, both with respect to the (1) perception of very low concentrations of odorsand to (2) discrimination of two or more odors in a mixture.

Early research on thresholds involved behavioral experiments in which individuals trained by reward or punishment were conditioned to select or avoid water that held the chosen chemical and then were tested on more and more diluted concentrations.

More modern methods involve conditioned heart rate, electroencephalograms, recordings from nerve tracts, and other electrophysiological methods. Various published sources for a number of fish species and chemical substances show wide variation.

One calculation of olfactory sensitivity shows that olfactory acuity corresponds to 1 ml of alcohol dissolved in a lake of a volume 58 times as great as that of Lake Constance (bounded by Germany, Austria, and

Switzerland; 207 square miles), which equates to one or two molecules of alcohol in the olfactory chamber at any one time.

The European eel (Anguilla anguilla), with its highly developed olfactory chambers and numerous olfactory lamellae, can detect phenyl-ethyl alcohol at concentrations of 3 x 10-20 molar or about the same concentration detectable by dogs.

Gustation, the sense of taste, is important to fishes primarily in the location and identification of possible food sources. Depending on the ecology of the species, it can be a very highly developed sense. For example, in certain minnows the sensitivity to various sugars and salts has been found to be 512 and 184 times greater, respectively, than that of humans.

Unlike olfactory sense receptors, taste receptors are not restricted toa single location. In addition to positions throughout the mouth, gill arches and skin, catfishes in particular but also many other taxa evolved well-developed barbels (sometimes longer than the fish itself) that bear dense concentrations of taste receptors and can be controlled with musculature.

What other taxa can you think of with evolved sensory filaments?

What elements of natural history would you imagine select for elaboration of barbels?