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Twenty-Five Years in the Mud: How a Quirky Little Fish Changed My Life
Guest post by D. Scott Taylor
Counting mosquitoes is never easy, especially when they are biting you, but that’s what I was getting paid for.
There I was, a mosquito biologist on a hot summer day, knee deep in the mud of a mangrove swamp bordering the Indian River Lagoon, the long estuarine system along the Florida east-coast. I had given up trying to get a “biting count” (believe it or not, you actually try to count the number landing on you in one minute…an ‘index’ of misery!).
I had stood in this very spot two weeks before, and there were none, but shortly after that the tide had risen sharply, flooding the mangrove swamp and apparently hatching the myriad of saltmarsh mosquito eggs secreted in the mud. I had missed finding the larvae, a critical part of any control effort.
Frustrated, I jammed my dipper, the long-handled scoop which is the main tool of the mosquito larvae sleuth, into a small puddle. No larvae, of course, but four small fish darted frantically about in the dipper. Always interested in fish, I glanced at them and could not immediately identify them, so I placed them in a bucket.
Sometimes it is the smallest things that are life-changing: this simple act, placing the four little fish in a bucket, has led to over 25 years of research and insights into the remarkable life of a very unusual fish.
It turns out that the four fish were specimens of the mangrove rivulus, Kryptolebias (formerly, Rivulus) marmoratus. Rivulus were very well known to ichthyologists, but very seldom collected at this time: fewer than 50 had been taken in Florida, a state thoroughly sampled for fishes, and although known from Brazil to Florida, they appeared to be equally scarce elsewhere.
The “well known” part was due to a very unusual sex life: this is the only known vertebrate which is a selfing, simultaneous hermaphrodite—they “clone” themselves. Adult rivulus have a complex reproductive organ, and internally self-fertilized eggs are laid which hatch into exact genetic duplicates of the parent…with some exceptions, as you shall see. Oddly enough, pure male rivulus, which differ from the “herms” in having a bright orange/red tint, had been caught in the wild, but their function was unknown: sexual reproduction had been documented in the lab but never in the wild…but more on this later.
Covered with mosquito bites, I kept glancing in the bucket on the way back to my office that day. Once I got an ID on my fish, a few days later I was back in the mangrove swamp, peering at the small puddle where I had collected the fish. But this was no common puddle! I immediately recognized it as a water-filled land crab burrow. With a quantum leap in collecting technology, I plunged a small net into the murky depths of the burrow, and withdrew it with 5 more rivulus. A few more dips, and I had a total of 13. I was floored to realize that I had just collected more rivulus in one location than anyone ever had before.
More than a Hole in the Ground
After gently placing the fish back in the burrow, I left, wondering if this association was mere coincidence.
The great land crab (Cardisoma guanhumi) is a large blue crab found throughout the shorelines of the tropical Atlantic, but it is actually a terrestrial crab. It digs burrows in saltmarshes and mangroves and sometime inland for some distance. The burrows are dug to the depth of groundwater, typically about 2-3 ft. deep, and the crab uses the pool of water to moisten its gills.
I began to suspect that the “scarcity” of rivulus had more to do with “looking in all the wrong places.” I was right. I checked crab holes far and wide, in every saltmarsh and mangrove swamp where my job led me. In the ensuing years, I have collected several thousand rivulus, and not just in Florida: I have found them in Belize, and also in Honduras, the Bahamas and Cuba.
The relationship seems well established. So, in Florida at least, rivulus is not as rare as originally thought, but still rare enough to warrant designation by the state as a “Species of Special Concern” and collection is prohibited without a permit.
Fish or Amphibian?
Early in my burrow-peering days, I found that sometimes rivulus would be out of the water, stuck to the side of the burrow, well above the water line. This behavior apparently offers the fish a means of avoiding poor quality water. During these aerial jaunts, the fish becomes torpid and respires through an extensive capillary network in the skin and fins.
My colleague Dr. Patricia Wright from the University of Guelph in Canada has been studying the physiology of emersion in her lab for years, and her findings are remarkable. My own lab study has shown that they can live at least two months out of the water in damp habitats: when re-flooded after 66 days, they were skinny, but eager to eat and devoured mosquito larvae immediately!
The adaptive value of emersion was dramatically revealed when I came upon a macabre scene inside a crab burrow where dozens of small minnows had been stranded by receding tides. Not as hardy as rivulus, the minnows began to die and rot, and I observed several rivulus emersed above and on the rafts of floating corpses, waiting for conditions to improve. A week later, when all trace of the dead fish was gone, only live rivulus were left in the burrow.
It turns out that rivulus will also occupy small, shallow pools at higher elevations in the mangroves. These pools flood and dry intermittently with higher tides or heavy rainfall. It is rare to find other fish species here, as they die when the pools dry. In Belize, my colleagues William P. Davis and Bruce J. Turner and I were puzzling over where the rivulus went when such pools dried. We had assumed that they would retreat to adjacent crab burrows or burrow into masses of mangrove leaf litter. It turns out that there were other housing options when your pool dries up.
In the tropics, beetle larvae and termites attack dead mangrove tree limbs/logs and excavate tunnels and galleries inside. The limbs fall into pools, and we found a pool that had recently dried, in which lay a number of dead mangrove branches. When we broke open the rotten branches, we discovered that dozens of rivulus were inside, filling the galleries like so many hibernating salamanders. This damp, secretive habitat allowed them the opportunity to survive until the next flooding event, perhaps some months distant. When these logs are carefully broken open, the fish have two options: try to retreat further into the log’s galleries or bail-out and flip wildly away. Trying to catch them once they flip away is like catching so many grasshoppers!
The Birds and the Bees
Speaking of sex (were we?), I have already alluded to the mysterious presence of male fish in an hermaphroditic species. Why would nature find this necessary? We know that male fish regularly show up in laboratory colonies of rivulus, and rearing the developing eggs at lower temperatures (~ 20° C /68° F) produces a high percentage of males, but low temperatures are not a common phenomenon in the tropics. So, my colleagues and I were shocked in our initial collections in Belize to discover that fully 25 percent of the population was male, and this high ratio has now persisted for over two decades. A few stray males have shown up in Florida, and a couple from the Bahamas and Honduras, but something strange is going on in Belize, because there the fish is reproducing sexually.
Apparently, in the presence of these flashy males, the herms somehow suppress internal self-fertilization (a fascinating physiological problem in itself!) and lay unfertilized eggs, which are then fertilized externally by the males. Of course, in the murky confines of a crab burrow (not the most romantic of settings), this has never been observed, but geneticists can tell by looking at the DNA that ‘sex’ is happening here!
When some wild Belize fish produce self-fertilized eggs in captivity, the offspring are not genetically identical. This means that at some point in prior generations, sexual reproduction occurred. Cloning has taken a lesser role here. Why? We don’t know. And the real puzzler is why would you need sex in an animal that appears to be eminently successful without it? After all, if you are distributed from southern Brazil to central Florida and throughout the entire Caribbean and western tropical Atlantic, you must be doing something right. This extensive range does speak to the advantages of ‘waif dispersal’: it only takes a single individual to found a population.
As they say, much remains to be done, but I thank my lucky stars that I did not discard that dipper full of murky water on that fateful, mosquito-ridden day 25 years ago. I still stalk the mangroves and look for other miracles. And there are others out there, to be sure.
D. Scott Taylor was raised in east central Florida and has a PhD in marine biology. His career interests are in mangrove fishes, where he has studied at field sites in Belize, Honduras, Cuba, the Bahamas and coastal Florida, battling mosquitoes the entire time. He is currently a land manager with the Brevard County (Florida) Environmentally Endangered Lands Program, charged with managing and restoring Florida’s diverse natural habitats.
This guest blog is part of our 2013 National Wildlife Week celebration of trees and the wildlife that depend on them.