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I would like to know if there is a reason why fishes (and many aquatic species) have both an olfactory and a gustatory system. As far as I know, in all fish species the chemoreceptors, organs and neuronal pathways are different for taste and olfaction, but why is it an asset to have two distinct sensory systems for chemical compounds in an aqueous medium ?

For terrestrial animals it makes sense to separate information stemming from remote sources mediated by volatile molecules and from the oral cavity, where the molecules are everything one can find in food. But in aqueous medium this distinction is far less obvious, especially when one considers that in some species there are taste receptors located on the body surface (lips, barbels).

I've read a few articles and this thread describing the physiological and neurological aspects of this separation, but it's not answering my question (and it actually aroused my curiosity even more).

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In addition to olfactory and gustatory, fishes have two more chemoreceptor systems, solitary chemoreceptor cells and free nerve endings (Finger TE 1997). Asking why do they have all these chemorecepor systems is 'little bit' difficult in the light of evolution. But we can definitely look at this question by using some comparative studies. Hence, this answer will not give you answer to 'why' but will give you enough information to understand roles of these systems.

Reference provided by you explains much of the mechanism of olfactory and gustatory system. I will highlight the important difference between these mechanisms.

  • In olfactory system, signal is directly detected and transmitted to Central Nervous System (CNS) by neurons of cranial nerve I (Liu and Zhang 2019)
  • In gustatory system, signal is first detected by specialized gustatory cells and then transmitted to CNS via cranial nerve VII (Purves D et al 2001)

As both of them have similar function, it has been difficult to assign specific function to specific system due to lack of robust behavioral assays (Hara TJ 1994)*

Nonetheless, there are following functions in different kinds of fishes are preferred by one system over another,

  1. Hara TJ 1994 comment that spatial feeding behavior is supported by olfactory system in contrast to gustatory system which helps in consummatory feeding like turning, biting, snapping and mastication**
  2. Morais s 2016 suggests, olfactory system is involved in kin-nonkin recognition, prey–predator interactions, and territory or homing recognition because it is less plastic while gustatory system only plays a role in feeding behavior.
  3. Discrimination of Pheromones is done by olfactory system (Lastein et al 2014)

From reading all these papers, I can 'guess' answer lies in the physiology of these sensory systems. Following conclusion is mine and I am no expert to tell whether this is correct. So just take it with pinch of salt :)

Fish has to survive in the water which is filled with tons of different chemical signals. So it has to distinguish these signals from each other. Many functions might not need very careful separation of signal (e.g. searching for resources) while other might need (e.g. which resources to eat). Some functions might need quick response (e.g. presence of predator) while other can be delayed for short time (e.g. migration). If you give responsibility to one system to perform all these functions simultaneously, it might get confused when multiple important signals arrive. From this I can speculate that this would have put some selection pressure during evolution so that there are multiple chemosensory systems.

From the literature cited above it looks like, Olfactory is less plastic and less sensitive than gustatory and hence involved in functions where you need little sensitivity to distinguish between multiple signal. While gustatory is involved where you need more specific selection of chemical signal.

*I could not get any recent paper directly comparing these two systems in fish. My hope is now we will be in more favorable place to perform some complex behavior experiments. **I did not understand difference between these behaviors conceptually, but you can look it up if you are interested.

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  • $\begingroup$ Nice, well referenced answer, +1. One comment I have is that I doubt "Olfactory is less plastic and less sensitive" -Though I have little knowledge about fish, there are fairly obvious ecological reasons for olfaction to be very very sensitive. I wonder if you really meant a different word here. Maybe less specific, in that the olfactory system is responding to a broader range of odorants versus just a few in the gustatory sense? Additionally the review you cite does say that about plasticity but also later says "showing low plasticity" about taste; I think the earlier statement is a typo. $\endgroup$ – Bryan Krause Jul 25 at 22:36
  • $\begingroup$ @BryanKrause, yes. I also wondered first. But I thought maybe it is like this for aquatic animals. The review I cited did not go into those details. $\endgroup$ – Dexter Jul 26 at 7:38
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Imagine what happens inside a fishes mouth after it has eaten an insect or another fish, It's the same if I eat a sardine... the sardine stays stuck in my mouth for a while afterwards. Then if i used my mouth to smell, I would just smell sardines everywhere, literally for an hour.

If the fish only used it's mouth to sense the water, it's sense of smell would be impaired for a while after it has crunched a meal. So it hunts a lot better if it has the ability to check healthy and moldy food through taste, and also sense pristine water for other meals.

The scientific research states that the precise function of the olfactory system is not totally known, it seems to aid behavioral functions not related to eating, for mating and prey detection.

This research is very well written and it's recommended reading. https://www.tandfonline.com/doi/full/10.1080/23308249.2016.1249279

Ultimately, a different olfactory receptor repertoire confers specialization towards different tasks. Take a shark's ability to detect blood, it makes sense to have a receptors to detect chemicals that are abundant at close range, it's specialized sensing abilities which are geared towards different peak detections and that guide responses in different zones of the brain.

Fish don't have as many receptor genes as mammals, so the evolution pressure is apparently less strong in water, i.e. mice and frogs have 1500 receptor genes versus 50-100 for fish.

catshark: 65 genes elephant shark: 54 genes zebra fish: 176 lamprey: 56 frog: 1500 elephant: 1900 stickleback: 159 platy: 98 ( https://academic.oup.com/gbe/article/doi/10.1093/gbe/evp003/597551 ) mammals: 1000 ( https://www.a.u-tokyo.ac.jp/english/topics/2014/20140812-1.jpg )

https://www.google.com/search?ei=Hz89XaK2JuCGjLsP4rGJoAk&q=receptor+repertoire+size+fish+gustatory

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