Tuesday, February 16, 2016

The Pike and the Fathead Freakout: A piscine sensory problem, by Don Orth

First, there's this story.  Joey Fishwater is an avid freshwater angler and fish watcher, and keeps native fish in tanks at his home. He is fascinated by all things fishy. His most recent fascination has to do with Northern Pike (Esox lucius) and Fathead Minnows (Pimephales promelas).   

He caught a juvenile Northern Pike and transferred it to his aquarium without realizing just how many live fish they eat. He named the pike “Jaws” and “Jaws” nearly starved to death while Joey Fishwater scrambled to find live fish. Then he discovered a small spring creek location where he could seine all the Fathead Minnows he needed; there were no Northern Pike in the creek so there were plenty of Fathead Minnows. 
He held the Fathead Minnows in an acclimation tank until he was ready to feed “Jaws.”  He created a partition with netting in his “Jaws” aquarium to separate the “Jaws” from the minnows on “death row.”  This allowed him to control the exact feeding time and rate and observe “Jaws” hunt and capture prey. As an avid fish observer, he spent hours just observing the behavior of Fathead Minnows. It was so cool to watch those Fathead Minnows.  

After several days he noticed behavior of the Fathead Minnows changed in the “death row” section of the tank. In the “death row” section they spent most of the time under shelters whereas the Fathead Minnows in the acclimation tank spent more time feeding and swimming. He called it the “fathead freakout.”  He thought they were frightened at the mere sight of “Jaws.”  So next he added an opaque barrier so the Fathead Minnows could no long see “Jaws.”   Same response.  Then he took “Jaws” out of the tank.  Same response.  Then he did a complete water change and in June he began to seine up males with tubercles (see below) and began to feed “Jaws” only males.  Now the Fathead Minnows did not show the same “fathead freakout.”   Hmm!     
Male Fathead Minnow.  Photo by Robert Aguilar, SERC
Female Fathead Minnow.  Photo by Robert Aguilar, SERC
So Joey Fishwater, knowing that you are a student of Ichthyology, calls you. “The Fathead Minnows know that “Jaws” is in that tank! And they freak out.”   “How do they do that?”  “But why don’t the males freak out?”  What sensory system do you hypothesize is used by the Fathead Minnows to detect “Jaws?”   How could you test your hypothesis?   And how can you explain the lack of male “fathead freakout?”

The Solution:  Let’s consider the behavior and hypothesize what sensory mechanisms are involved that permit a Fathead Minnow on “death row” to detect danger and “freak out.”  The behavior that Joey observed was a fright response.  Joey ruled out vision by installing the opaque barrier and observing no change.  The next likely sense would be olfaction.  Fish have a very keen sense of smell. It appeared that they were not immediately responding to the presence of the Northern Pike.  The sentence “After several days he noticed behavior of the Fathead Minnows changed in the “death row” section of the tank.” provides an important clue.    The Fathead Minnows were not simply detecting the presence of Northern Pike and showing a fright response.  And later, when Joey fed the “Jaws” only male Fathead Minnows, the fright response stopped.  

The answer to this problem also requires a basic knowledge of sensitive olfaction in fishes in general.  It also requires a specific understanding of the minnow alarm pheromone (aka Schreckstoff) that is produced when the specialized epidermal club cells are injured.  This alarm substance is produced by fishes in the superorder Ostariophysii; this group includes Fathead Minnows.  In Joey’s case, the Northern Pike that had been eating Fathead Minnows became chemically labeled with the alarm pheromone.  The chemical label is the residual alarm substance from the ingested Fathead Minnow that persisted as a byproduct of digestion and is excreted by the Northern Pike. The alarm pheromone chemically labels Northern Pike as dangerous to other Fathead Minnows, even Fathead Minnows that never have witnessed a Northern Pike before. 

Why don’t the males freak out?  The males had secondary sex characteristics (tubercles and enlarged head) that indicated they were preparing to breed.  In the course of courtship behavior or agonistic behavior as they defend a breeding territory, the release of the any alarm pheromone would send a signal to all potential mates to swim away from this location. This is exactly the opposite reaction the breeding male wants.  Consequently, as the breeding season approaches and secondary sex characteristics develop in the male, the epidermal club cells are shed and not replaced. Production of alarm substance cells by fathead minnows is inhibited by androgens.  Therefore, the male Fathead Minnows do not chemically label the Northern Pike because they had no (or fewer) alarm cells.

The experiments to demonstrate this phenomenon were done by Alicia Mathis and Jan Smith (1993). First they confirmed that pike-naive Fathead Minnows exhibited a fright response following exposure to water from a tank containing northern pike that had eaten Fathead Minnows.  Next, they confirmed that the Northern Pike were excreting the minnow alarm substance; they used the chemical stimuli from pike that had eaten breeding male minnows as a control stimulus.   

To the student who claims that “this question is unfair!” I respond that the problems that students of the fishes must solve on a daily basis are at least as complex.  They require one to integrate knowledge from different chapters of the text, different disciplines, and past experiences of many specialists.  The fact that fish as small and plain as a Fathead Minnow are able to survive in a world filled with threats indicates that they are adjusting to changing threats all the time.  

The Fathead Minnow has become an excellent model species for studies of estrogen disruptors because of its adaptability in aquaria, short-life span, and well-understood reproductive requirements.  Recent findings highlight the significance of hormones in our environment. Cattle are fed growth promoters to enhance yields before slaughter.  These are androgens (17-β-trenbolone) that disrupt normal reproductive development in male and female Fathead Minnows (Ankley et al. 2001, 2003).   Males and females exposed to feed lot effluents have altered reproductive development (Orlando et al. 2004).  Endocrine disruption is a pervasive problem in our freshwaters and the Fathead Minnow has become a well-studied model used in many studies of endocrine disruption (Watanabe et al. 2016).  If the Fathead Minnow cannot regulate it's reproductive cycle in our natural waters, perhaps we should be more concerned about the water we drink.
Ankley, G.T., K.M. Jensen, M.D. Kahl, J.J. Korte, and E.A. Makynen.  2001.  Description and evaluation of a short-term reproduction test with the fathead minnow (Pimephales promelas).  Environmental Toxicology and Chemistry 20(6):1276-1290.
Ankley, G.T., and twelve coauthors. 2003.  Effects of the androgenic growth promoter 17-β-trenbolone on fecundity and reproductive endocrinology of the fathead minnow. Environmental Toxicology and Chemistry 22(6):1350-1360. 
Mathis, A. and R.J.F. Smith.  1993.  Chemical labeling of Northern Pike (Esox lucius) by the alarm pheromone of the Fathead Minnow (Pimephales promelas).  Journal of Chemical Ecology 19(9):1967-1979.
Orlando, E.F., and eight coauthors. 2004. Endocrine-disrupting effects of cattle feedlot effluent on an aquatic sentinel species, the fathead minnow.  Environmental Health Perspectives 112(3):353-358.  
Watanabe, K.H., M. Mayo, K.M. Jensen, D.L. Villeneuve, G.T. Ankley, and E.J. Perkins. 2016.  Predicting fecundity of fathead minnows (Pimephales promelas) exposed to endocrine-disrupting chemicals using a MATLAB®-based model of oocyte growth dynamics.  PLoS ONE 1(1): e0146594. doi:10.1371/journal.pone.0146594

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