A fish out of water.
The California grunion, Leuresthes tenuis, may have the most curious reproductive strategy of any fish. The California grunion stands apart from its relatives because it mates completely out of water, leaving the fertilized eggs buried in the sand to incubate until the next semilunar tide.1 To understand the evolution of this unique behavior, one must consider the advantages of terrestrial spawning over aquatic-based reproduction cycles. California grunion have adapted to use the terrestrial environment to their reproductive advantage – the question is: why?
Life History of Leuresthes tenuis
Grunion reproduction occurs in large nocturnal spawning runs, where thousands of grunion ride tidal waves to the shore to mate upon the sand.2 Local citizen scientists known as “Grunion Greeters” have recorded that grunion runs may occur on any night of the high-tide lunar series in any patch of smooth sand. Between February and March, spawning occurs in coordination with lunar tides, which enable the grunion to coast to shore and mate.1 When on shore, female grunion burrow tail-first about five centimeters into soft sand. Male grunion then wrap around the head of the female, depositing milt on her eggs. Once the reproductive process is complete both male and female grunion return to the ocean. Turbulence generated by the waves then covers the fertilized eggs, placing them under about fifteen centimeters of sand over the next couple of days.2 As the adult grunion return to the ocean, the fertilized embryos remain buried under the moist sand. Maturing underneath the sand, the embryos rely on lunar tides to carry them out to sea as soon as ten days later.1 In 1999, Karen Martin and her research team discovered that the California grunion is able to prolong incubation for at least thirty-five days, hatching when exposed to motor agitation and liquid.3 After hatching, grunion larvae stay relatively close to the shoreline for approximately forty days, feeding off of plankton until reaching juvenile status.1
It is rare for a grunion to die out of water unless stranded by an obstruction or a strong wave.1 Grunion may, at most, survive approximately one hour above water – most fish succumb within thirty minutes.4 If placed under forced terrestrial exercise, grunion demonstrate a high blood lactate level, suggesting the use of an anaerobic metabolism.4 Anaerobic metabolism is the ability of an organism to create energy without the use of oxygen. When under low-oxygen conditions, the organism will generate high amounts of lactate as a by-product of producing energy. Karen Martin and colleagues (2004) also tested the possibility of anaerobic metabolism by catching male and female grunion after mating, freezing them on-site in liquid nitrogen to analyze blood lactate levels in the lab. No significant difference was found, indicating that grunion do not breathe air.4
Evolutionary Advantages and Disadvantages
“Grunions live an amphibian-like lifestyle. The California grunion has evolved to fit an interesting niche: it lives an amphibian-like lifestyle, emerging from the ocean to improve chances for its offspring’s survival. In aquatic environments, eggs exist largely at the mercy of the elements. As a part of the oceanic environment, marine eggs commonly drift and are lost with currents. Other threats include egg predation and suffocation: without proper aeration, the embryos die due to lack of oxygen. Terrestrial breeding is extremely risky for parents, but offers low predation, warm temperatures, relative safety and aerobic conditions – each factor increasing chances for embryo survival.
Grunion embryos are buried beneath the sand, providing a protective buffer against potentially harmful aspects of the environment. Despite this, embryos are delicate and are easily affected by external stimuli. Major weather systems, global climate change and pollutants easily interrupt the development of these fragile embryos. Tracking the effects of salinity (the concentration of salt in a volume of water) and temperature on grunion embryos may provide an easy medium through which to study environmental change.5,2
Desiccation, or extreme dryness, of the embryo is a major risk of terrestrial breeding. Grunion egg development has evolved to reduce the chance of desiccation through environment-induced hatching and the ability to maintain constant maturation for prolonged periods of time. Alienated from water, the California grunion relies on the semilunar spring tides to stimulate hatching. The tides then function to carry the newborn grunion to the ocean.6
Grunion are fascinating fish, providing endless opportunities for research. Having mastered a unique niche in nature, the fish lives an aquatic life while mating and incubating eggs on land. Terrestrial pros and cons indicate that spawning on land offers a stable environment for the embryo with a constant air supply and reduced predation.
These fish offer an interesting study in neurobiology. Sensory mechanisms in embryonic systems may open a new world of understanding about neurosystem development. The embryos are also very fragile organisms, and are thus very responsive to scientific testing and treatment. This, coupled with their sensitivity to environmental change, makes them an excellent specimen through which to monitor overall pollutant levels, and to gain insight into how pollution affects neurological development.
While the terrestrial mating system of the grunion is a well-known phenomenon, very little is known about this behavior. Further research in the field and laboratory will add significant contributions to our understanding of fish behavior and evolution.
1 Martin, K. 2006. Introduction to grunion biology. 1-5. Personal communication.
2 Smyder, EA and Martin KLM. 2002. Temperature effects on egg survival and hatching during the extended incubation period of California grunion, Leuresthes tenuis. Copeia 2: 313-320.
3 Martin, KLM. 1999. Ready and waiting: delayed hatching and extended incubation of anamniotic vertebrate terrestrial eggs. American Zoology 39: 279-288.
4 Martin, KLM, RC Van Winkle, JE Drais and H Lakisic. 2004. Beach-spawning fishes, terrestrial Eggs, and air breathing. Physiological and Biochemical Zoology 77: 750-759.
5 Matsumoto, JK and KLM Martin. 2008. Lethal and sublethal effects of altered sand salinity embryos of beach-spawning California grunion. Copeia 2: 484-491.
6 Griem, JN and KLM Martin. 2000. Wave action: the environmental trigger for hatching in the California grunion Leuresthes tenuis (telostei: atherinopsidae). Marine Biology 137: 177-181.
Tagged as: behavior, development, grunion, mating, model organisms, pollution