Sticklebacks urinate differently when nestbuilding
Fish also build nests. Among sticklebacks this is done by the male, requiring so many of his resources that he cannot function normally while at work: He loses his ability to produce urine normally. Now scientists reveal how the hard-working males manage to get rid of surplus fluid from their body.
Male sticklebacks are very dedicated when it comes to bringing the next generation into the world. They compete to build the best nest and then lure females into it. When a female has laid her eggs in the nest, the male fertilizes them and then defends his offspring vigorously until it hatches.
Males put a lot of energy into building the nest - so much that some of their vital organs are forced to completely change their appearance and function. This applies especially for the kidney.
All animals use their kidney to excrete excess water and waste products from their organism. This leaves the body as urine. Sticklebacks also do this – however, the males only until they start getting sexually mature. When the male matures, he starts building a nest, and at that time his kidney stops producing urine.
He ought to explode
"For the nest he needs a special slimy substance, which is produced by the kidney. The production of this substance, resembling spider silk, completely takes over thus compromising the normal kidney function to produce urine. This situation compares to a person losing the ability to urinate”, explains Steffen Madsen, Associate Professor, Department of Biology, University of Southern Denmark.
Steffen Madsen is the lead author of a scientific paper on the subject, published in the journal Comparative Biochemistry and Physiology Part A: Molecular & Integrative Physiology.
The anatomy of a fish kidney differs from a human kidney, but the principle of function is the same: to excrete water and waste products from the organism. When sticklebacks live in freshwater they tend to absorb more water into the body than they need, so a compromised kidney should pose a serious threat for nest building males.
Sticklebacks as doping watchdogs
When the male stickleback matures his kidney function changes. This is initiated when his levels of testosterone and other male hormones increase in his body, and it causes his kidney to grow so big that it can be seen with the naked eye. The enlarged kidney produces the mucus substance spiggin, needed for nest building. This reaction is very specific and sensitive to androgenic chemicals.Thus an enlarged kidney is a sure sign that the stickleback has been affected by male hormones.
Any immature stickleback – female or male – will react the same way, and this turns sticklebacks into valuable bio-markers for anthropogenic compounds that mimic male hormones. For example, sticklebacks may be used to detect steroids in gyms: Expose a stickleback to the sewage from the gym’s men’s room and watch if its kidney swells. Under controlled conditions, a swelled kidney may be a sign that androgenic steroids are used in the gym.
"If he cannot get rid of the excess water, he ought to swell up like a sponge, absorbing water and eventually explode”, says Madsen.
But he doesn’t. Somehow the surplus water is released, but how?
A most unusual way to get rid of excess water
"It has previously been a mystery, but today there is evidence that the males release “urine” from the intestine instead of the kidney. Our research now gives a good and detailed clue to how this is possible”, explains Madsen.
According to Madsen, secretion of dilute fluid by the intestine as an active way of osmoregulating has never previously been observed in an animal, so this is an unusual ability and an interesting biological phenomenon.
Madsen and his colleagues studied stickleback intestinal cells in the laboratory and by analyzing several selected salt and water transporting proteins they were able to identify the molecular mechanism that ensures fluid excretion through the intestinal wall.
The researchers demonstrated that the urine does not seep out between the intestinal cells – something that could have been a plausible explanation. Instead the urine is transported through the cells via some specific channels in their membranes.
"The experiments suggest that the excretion takes place via so-called aquaporins: molecular water channels in the membranes of the intestinal cells, a process driven by simultaneous transport of salt. Sticklebacks have a large number of different variations of aquaporins, many more than, for example, humans", says Madsen.
In contrast to the kidney, where fluid secretion is based on filtration of the blood, the intestine secretes fluid by secreting salt, followed by diffusion of water.
"This particular stickleback capability is an example of how animals have become specialized and managed to adapt to almost any situation during evolution”, says Madsen.
Ref: Comparative Biochemistry and Physiology Part A: Molecular & Integrative Physiology, volume 188, October 2015, Pages 107–119: Sexual maturation and changes in water and salt transport components in the kidney and intestine of three-spined stickleback (Gasterosteus aculeatus L.). Steffen S. Madsena, , Claus Webera, Andreas M. Nielsena, Mohammad Mohisenic, Maryline C. Bosssusb, Christian K. Tipsmarkb, Bertil Borgd. a Department of Biology, University of Southern Denmark, Denmark, b Department of Biological Sciences, University of Arkansas, USA, c Behbahan Khatam Alanbia University of Technology, Iran, d Department of Zoology, Stockholm University, Sweden.
Photo A stickleback (Pungitius pungitius) by a nest. From Wikipedia.
Video A male builds a nest and courts a female. From The Environment Agency, the University of Leicester and Gledhow Primary School.
Contact
Associate Professor Steffen Madsen, tel. + 45 6550 2450. E-mail: steffen@biology.sdu.dk.
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