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Other Homing Experiments
Investigations into how salmon find their home stream
Nitin Patel - Univ. of Oregon
Background

Salmon are well known for their ability to return to the stream in which they were spawned to reproduce and complete their life cycle. This ability of migratory salmonids to accurately locate their natal streams has been thoroughly researched over the years. Sun compass, polarized light, ocean currents, temperature, olfaction and electrical and magnetic stimuli have all been proposed as sources of guidance information. Although all these may play a part, the recognition of the natal stream by the salmonids has been primarily been attributed to olfactory cues. "The speculation about the use of odors as cues for homing...dates back to the 19th century" (Trevanius, 1822) and has been resurrected several times by various researchers.
This report reviews the evidence for olfactory imprinting in salmon. The results of research performed by various investigators are remarkably consistent. The experiments conducted by these researchers were done in the field instead of the laboratory and thereby provide direct evidence that salmon use olfactory cues for homing.

The olfactory hypothesis for salmon homing, first presented by Hasler and Wisby in 1951, is based on three beliefs: (1) because of local differences in soil and vegetation of the drainage basin, each stream has a unique chemical composition and, thus, a distinctive odor; (2) before juvenile salmon migrate to the sea they become imprinted to the distinctive odor of their home stream; (3) adult salmon use this information as a cue for homing when they migrate through the home-streaming network to the home tributary.

There have been two proposed hypothesis to how salmon locate their natal stream. First in 1951, Hasler and Wisby proposed the "imprinting hypothesis." This hypothesis states that recognition of the home stream results from a relatively rapid odor learning process during a sensitive period called the smoltification process. The other hypothesis was proposed by Nordeng in 1971. He speculated that smolts that migrate to the ocean, release population specific odors called pheromones. It's these pheromones, in the end, that are used by mature adults as cues to guide them back to their home stream. Evidence supporting both the imprinting and pheromone hypothesis has accumulated over the last two decades (Hasler and Scholtz 1983; Smith 1985).

Life Cycle of Coho Salmon (from Nevitt, 1992)
Smoltification
Illustration from Hasler and Scholz, 1983
When they are 1.5 years old, in April or May, coho salmon undergo a metamorphosis referred to as smolt transformation or smoltification. Morphological, physiological, and behavioral changes that pre-adapt young salmon to life in sea water occur during this period. During the smolt stage, their parr marks disappear, and they turn silver, which is a color adaptation for living in the ocean. Their osmoregulatory mechanisms begin adjustments that will enable survival in salt water. They cease territorial behavior and form schools numbering in the thousands, and embark on their seaward journey. Just prior to the smolt stage, the endocrine system undergoes major transitions. Smolt transformation is thought to be induced by thyroid hormones. The smolt stage is of critical importance to understanding the homing process because it is during this period that salmon "imprint" to some property of their natal tributary that serves later to identify it when they return as adults to spawn [Hasler and Scholz, 1983].

Morpholine and PEA
Experiments with artificial odors indicate that imprinting occurs at the time of peak thyroid hormone levels during smolt transformation. Hasler and his colleagues showed that juvenile coho salmon exposed to synthetic chemicals, such as morpholine or beta-phenylethyl alcohol (PEA) during smoltification, could be attracted into an unfamiliar stream scented with one of these chemicals during their spawning migration. The basic procedure proposed by Hasler and Wisby was to imprint young salmon to a synthetic chemical in place of natural home stream odors, to determine if they would return to the stream scented with the chemical. Morpholine (C4H9NO), a heterocyclic amine, and phenylethyl alcohol (C8H10O) were selected because they can be detected by salmonids at low concentrations and are not known to occur in natural waters. A few salmon were exposed to these chemicals during smoltification and some were not.
Experiment 1
One cool experiment performed from 1971 to 1973, used ultrasonic tracking to conduct a behavioral experiment to test the imprinting hypothesis. Essentially this involved releasing morpholine-imprinted fish along the shoreline of Lake Michigan and tracking them into an area scented with morpholine (Scholz et al. 1973, 1975). Control experiments were conducted by tracking morpholine-imprinted fish through the test area when morpholine was absent or when a different chemical was present, as well as tracking fish that were not imprinted with morpholine present.
Adult salmon captured at Oak Creek, were transferred by boat to a point 3.2 km north of Oak Creek. Before releasing them, the researchers inserted an ultrasonic transmitter down the esophagus into their stomach to follow their movement.

Scholz and his colleagues selected a release site assuming that fish released near the shore would follow the shoreline and intercept an intervening point where Oak Creek flowed into Lake Michigan. Morpholine was introduced into test area perpendicular to shore, extending from the mouth of Oak Creek to about 100 m offshore. This created a narrow band which acted as an "odor barrier" through which the fish had to swim. The morpholine concentration was kept at 5.7 x 10-10 M. The water currents were measured with the use of various instruments to determine how long the chemical remained there. Before tracking, the fish were held for 3 to 17 days in tanks containing Lake Michigan water to reduce the possibility that they might react to morpholine only because they had been recently exposed to the odor.

Scholz and his colleagues tracked 56 fish through this test area. Most of the salmon remained near the release point for about one hour before moving. In all cases (20 tracks) when morpholine was present in the test area, morpholine-imprinted fish stopped their migration and remained in scented area from 1 to 4 hours. The salmon's stay correlated roughly with the time it took for water currents to dissipate the chemical. When morpholine was not present in the test area, morpholine-imprinted fish moved through without stopping. On the other hand, 13 control (not imprinted) fish did not stop when morpholine was present. [Hasler and Scholz, 1983] See the results of this Lake Michigan Experiment. Illustration from Hasler and Scholz, 1983

Experiment 2
A similar test was conducted by Johnsen in 1978. He imprinted coho salmon smolts to morpholine (M) or phenethyl alcohol(P) in a hatchery, stocked them in Lake Michigan, and captured them as adults in streams scented with either of these chemicals. The protocol was very similar to the test previously discussed above. Morpholine was introduced on either the right or left side of the stream. Flow patterns of the chemical morpholine were estimated by charting the distribution of an orange dye (Rhodamine introduced at the same point as the morpholine before and after each experiment. Dye introduced on one side of the channel did not extend beyond mid-stream. Because the dye did not spread to cover the width of the river, movements of the morpholine fish were confined to the right half of the river when morpholine was on the right side and on the left half when morpholine was introduced on the left-side. Fish that happen to swim out of the odor trail, swam downstream until detecting the odor again. Morpholine-imprinted fish swam upstream toward the morpholine introduction site. On the other hand, phenethyl-alcohol (PEA) imprinted fish swam downstream, away from the morpholine introduction point. Morpholine-imprinted salmon migrated upstream when morpholine was present and downstream when it was absent. PEA treated fish swam downstream in both cases. In addition, morpholine-imprinted fish were able to decipher which side of the river the scent was emanating from. See results: (illustration from Hasler and Scholz, 1983)
Experiment 3
Brain electrical response (EEG) responses of morpholine-imprinted and control salmon to morpholine over the course of the spawning season. The amplitude of the response to morpholine by morpholine-imprinted fish increased over the course of the spawning season. Note that at the end of the spawning season morpholine imprinted fish stopped responding to morpholine. At this time they began to respond strongly to odors from other salmon (Cooper and Hasler 1973, Scholz et al. 1973).
In salmon, sex hormones play a role in modifying olfactory sensitivity and discrimination capability. The effect of sex hormones on olfactory sensitivity is interesting in light of the fact that olfactory sensitivity of salmon to their imprinted odor increases over the course of the spawning season during which there is increased circulating levels of sex hormones. See EEG response to Morpholine: (illustation from Hasler and Scholz, 1983)

Exposure to micromolar concentrations of PEA for as little as 10 days during a sensitive period for olfactory imprinting (parr-smolt transformation) correlated with a specific increase in the responsiveness of olfactory receptor cells to PEA. when tested 6-9 months later (Dittman, 1994). See behavioral responses to PEA: (illustration from Dittmann, 1994)

Conclusion:
All these experiment show without a shadow of a doubt that the supernatural sense of smell of salmon is crucial in the maintenance of their life cycle. It also demonstrates the great importance of the smoltification process in imprinting the natal steam's unique odor. The rate of return in these experiments was observed to be about 0.5%-2% (ocean runs) or 2%-5% (freshwater runs), with about 95% of the recovered fish captured in the stream of release, which compares favorably with homing in natural populations [Hasler and Scholz].

In contrast, transplanting fish after smolt transformation, resulted in poor recovery (.025%). These findings suggest that imprinting terminates soon after smolt transformation begins, thereby preventing fish from becoming imprinted to other tributaries during the course of their downstream migration.

Hasler and Scholz summarize that two important conclusions can be drawn from these transplantation studies. First, the memory of the home stream is not inherited. Second, homing is connected with a period of rapid and irreversible learning -- i.e., imprinting -- of the cues that identify the home stream at the time the young salmon begin their downstream migration. After three or four years at sea, the salmon recall what they learned as smolts from their long term memory.

In addition, it was recently discovered Pacific and Atlantic salmon use photoperiodic cues to initiate spawning migration by activating production of a sex hormone called gonadotropin. Plasma levels of gonodotropin increase in fish exposed to gradually decreasing day lengths. Gonadotropin stimulates differentiation of gonads, induces production of sex steroid hormones, and induces migration.

Investigations into the imprinting have been applied to management applications. For example, information about the timing of imprinting or external indicators of imprinting are important for determining the time for stocking fish to insure homing to the stream of release.

"Surely any step toward saving salmon is worthwhile, for they are a gift from nature to man. We neither feed them nor take care of them in any other way. Yet, as young fish, they go out to sea where they grow fat on the ocean's rangeland and then deliver themselves, free of charge, to our back door for the catching and eating." [Hasler and Scholz, 1983].

References:
Dittman, Andrew H., et al. "Evidence for a peripheral olfactory memory in imprinted salmon." National Academy of Sciences, USA 91: 4288-4292, May 1994 [Neurobiology].
Dodson, Julian J., et al. "Facilitative Effect of Pre-exposure on Heart-Rate Conditioning to an Olfactory Cue in Atlantic Salmon (Salmo Salar)." Journal of Comparative Psychology. 104 (1990) : 340-344.

Hara, Toshiaki J., et al. "Sibling Recognition and Olfactory Sensitivity in Juvenile Coho Salmon (Oncorhynchus kisutch)." Canadian Journal of Zoology 64 (1986) : 921-924.

Hasler, A.D. and A.T. Scholz. Olfactory Imprinting and Homing in Salmon. New York: Springer-Verlag Berlin Heidelberg, 1988.

Hassler, Thomas J., et al. "Homing of Chinook Salmon Exposed to Morpholine" California Fish and Game 76 (1990) : 31-35.

Maxwell, Jessica. "Swimming with Salmon." Natural History. September 1995: 29-39.

Morin, Pierre-Philippe., et al. "Changes in the Olfactory Function of Atlantic Salmon, Salmo salar, in the course of smoltification." Canadian Journal of Fisheries and Aquatic Sciences 49 (1992) : 1704-1713.

Nevitt, Gabrielle A. "An Electrophysiological characterization of ciliated olfactory receptor cells of the coho salmon Onchohynchus kisutch." Journal of Experimental Biology 166 (1992) : 1-17.

Quinn, Thomas P., et al. "Pacific Salmon Migrations and Homing: Mechanisms and Adaptive Significance." Tree 5 (1990) : 174-177.

Rehnberg, Bradley G., et al. "Olfactory Sensitivity during Parr and Smolt Developmental Stages of Coho Salmon." Tranactions of the American Fisheries Society. 114 (1985) : 732-736.

Rehnberg, B.G., et al. "Homing of Coho Salmon (Oncorhynchus kisutch) Exposed to Morpholine." Aquaculture 44 (1985) : 253-255.

Scholz, Allan T., et al. "Imprinting to Chemical Cues: The Basis for Home Stream Selection in Salmon." Science 192 (1976) : 1247-1249.

Back in the late 70's early 80's morphline was experimented with right here on the south end. Our Kings were stocked inside the east branch of the Port Of Indiana for a few years. It was an attempt to control where the kings would return as spawners.
Morphline was used when the fish were introduced to the Port. The experiment was if the returning kings could be controlled to spots along the lake shore, from the ditch to USS. Between trespassing and the smell of rotting fish on the streams, the thought would be that we could be able to surf fish for the kings. There was to be drip stations delivering Morphline along the lake front, and the kings were to return to the drip station spots. But, the kings imprinted on the east branch of the Port and returned to the Port. We could fish there back then. Imagine 300 boats all fishing in a big wagon wheel, and when hooked up you moved to the center of the east branch and fought your fish. Then like fishing on a nascar oval, you got back in to the wagon wheel. Early morning the kings were so thick on the south end of the east branch that your down rigger balls would be bouncing off of fish. If there was no cloud cover, by 8 am all the fish had moved under any tied up ship, to get out from the sun. No fish ran the ditch when these years were stocked this way. And, very few fish were caught on the west branch of the Port. During these few years, the state record king was tied by Jack Perry who wrote the outdoor articles for the Post Tribune. A few days after Jacks big fish, my wife got her 32 lb female king. There was around 30 kings that had approached the 30lb mark caught the first year this happened. I had alot of fun back then working for Bob Cash as his first mate.

Ed: Interesting stuff. I fished in those "wagon wheels" back in the day. Fun stuff. Brings up many thoughts and theories on past and current practices too snarky to list.