 September 2002 |
Their Game Is Mud
Skipping and jumping across the shore at low tide,
mudskippers give new meaning to the phrase “fish out of water.”
By Heather J. Lee and Jeffrey B. Graham
The coastal mangrove forests and mudflats of northeastern Australia are rather inconvenient places to visit. Occupied by man-eating crocodiles and bloodsucking insects, and offering only a muddy quagmire for footing, the habitat definitely challenges the mobility of a pair of biologists. But the organisms we seek thrive here. They skip across the surface of the mudflats, scamper over mangrove roots, and dive into their burrows at the slightest sign of danger or as the high tide reclaims their habitat twice each day.
The nimble, bulb-eyed creatures we study are mudskippers—amphibious fishes that inhabit Old World mudflats and mangrove forests from West Africa eastward to Papua New Guinea. Members of the diverse goby family, the twenty-five mudskipper species are classified, on the basis of body traits and behavior, into four genera: Scartelaos, Boleophthalmus, Periophthalmus, and Periophthalmodon. Mudskippers are the only fish to conduct many of their major activities—including feeding, courting, and defending territories—on land. In order to manage these feats, they rely on a number of evolutionary specializations. Their prominent eyes, for example, are so well modified for clear aerial vision that their ability to see underwater is diminished. Beneath each eye is a water-filled cup formed from skin folds; as a mudskipper’s eyes become dehydrated by exposure to the air, they can be retracted into this cup to be moistened. With their leglike fins, mudskippers can walk, climb, and leap when out of the water, and thanks to structural modifications in their skin and gill chambers, they are able to breathe both in water and in air. Indeed, observing these creatures encourages one to conjure up images of the first vertebrates that came ashore some 360 million years ago. Describing the mudskipper in his essay “The Snout,” renowned naturalist Loren Eiseley wrote, “Of a different tribe and a different time he is, nevertheless, oddly reminiscent of the [ancestral vertebrate].” Many biologists have investigated mudskipper specializations in order to understand the sequence of changes that enabled those early vertebrates to make the transition to life on land. From an evolutionary perspective, of course, mudskippers are very distantly related to the ancestral fishes that gave rise to terrestrial vertebrates. But, as Eiseley noted, “There are things down there still coming ashore.” Like our own ancient ancestors, a number of modern species have begun to come ashore, independently developing the capacity for both air-breathing and amphibious life.
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How do these fish manage to wait out
high tide in the oxygen-poor water within their burrows? |
Although the aboveground activities of mudskippers first caught the attention of naturalists some 300 years ago, little is known about their behavior below the surface. The ability to leave the water has enabled the fish to exploit shallow mudflats, but for many mudskipper species the watery burrow is still home base, from which it launches terrestrial forays and to which it retreats when threatened by predators. At low tide, mudskippers are at risk of being preyed upon by shorebirds as well as by a variety of other terrestrial animals, including snakes and mammals. At high tide, many mudskipper species take cover in their submerged burrows to avoid being attacked by predatory fish that cruise the shallows. Besides serving as a refuge, a burrow can also be used as a nursery for developing eggs: members of the genera Boleophthalmus and Periophthalmus are known to lay eggs in burrows, and quite possibly this occurs in the other two genera as well. Seemingly essential to the safety of both adults and young, burrowing nevertheless comes with a danger of its own—the water inside the burrow is perilously low in oxygen. Mudskippers must somehow tolerate or overcome this oxygen shortage, not only for their own sake but for that of their developing eggs.
The two of us have traveled around the world in an effort to unravel the details of mudskipper burrows, including how these fish manage to wait out high tide in the stagnant burrow water and how delicate mudskipper embryos manage to develop properly in this environment.
Working with Atsushi Ishimatsu, Toru Takita, and graduate student Naoko Itoki, all of Nagasaki University, and with Tatsusuke Takeda, of Kyushu University, we observed the mudflats of Japan’s Ariake Bay being transformed into a backdrop for the captivating courtship spectacle of Periophthalmus modestus. Each spring, the males carve up the available surface into individual territories and excavate burrows up to two feet deep. The burrow is shaped like a j (or sometimes a y, with two entrances), whose upturned lower tip will become the spawning chamber, where the eggs are deposited.
Its burrow prepared, the male sets about finding a mate. At low tide during P. modestus’s spawning season, which runs from late May through early August, males perform an enticing courtship dance for an audience of females. As if dressing for their performance, the males turn from drab brown to a pale beige color that contrasts with the darker mud. Each male tries to lure an egg-swollen female to his territory and down into his burrow. In his effort to capture a female’s attention, he puffs out his cheeks, mouth, and gill chambers by filling them with air; he also arches his back, points his tail fin, and sinuously wriggles his body. As a potential mate draws near, he continues to display, slowly drawing her to his burrow and pausing periodically to be sure she has not lost interest and fallen under the spell of a rival male. The suitor then dips into the burrow and quickly reappears, enticing the female, so it seems, to come and enjoy the comforts of his accommodations. If she hesitates, the male again pops in and out of his lair until she is finally tempted inside. Having lured her below, the male returns to the burrow entrance to “lock the door” with a mud plug.
Researchers have previously demonstrated that after being fertilized, the eggs are somehow embedded in the mud walls of the spawning chamber, where they take about a week to develop. But we have little information about what actually happens once the pair enters the burrow and descends into the burrow water toward the spawning chamber. To observe the developing eggs and the egg-care behavior, Ishimatsu’s team has been using an endoscopic camera inserted into the mud above the tip of the spawning chamber; with this device, they are making the first-ever observations of the mudskippers’ underground world.
Once the eggs have completed development, the tiny, transparent, newly-hatched larvae drop into the burrow water and from there make their way to the open ocean. During the first hours of a larva’s planktonic existence, it is sustained by a small yolk sac. After about forty-five days, the juvenile fish returns to settle on the mudflat and begin its amphibious adult life. The Ishimatsu team’s studies of spawning and egg care in P. modestus, along with other ongoing work, promise to contribute to an understanding of how the larvae survive after hatching in the oxygen-poor burrow water and how the fish journey to the open sea.
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We do not yet know the biological importance of turrets and moats. Envisioning the mudflat surface from a mudskipper’s perspective, we suspect that moats may deter other species from entering the burrow complex and that turrets could serve as observation posts from which to spot predators or prey. In the early morning hours, we have seen P. minutus lounging just inside the mouth of a turret, which, as shown by our measurements, can be as much as 7° C warmer than the burrow’s depths. It may be that the structure provides the fish with a safe place to warm up efficiently in preparation for the day’s activities.
Details of mudskipper burrowing were beginning to come into focus, but we wanted to compare our findings about Periophthalmus with what is known about another mudskipper, Scartelaos histophorus—the bearded, or walking, goby. The Australian coastal town of Cardwell is famous not only for tasty prawns and mud crabs but also for the dense bearded-goby population that inhabits the mudflat bordering the town. The city’s public pier provides an excellent vantage point from which to observe thousands of the fish as they race around at low tide, their long dorsal fins bobbing up and down like bumper-car antennas. Males staunchly defend territories roughly one to three feet in diameter. In areas with a high density of fish, the territories are crowded together and, as University of California marine biologist Nancy Aguilar reports, become pentagonal or hexagonal in shape. Low mud walls sometimes mark their perimeters. Defending his turf from other males, the resident male uses a combination of threat displays and direct confrontations that culminates in the loser retreating or being chased away.
| The male of one species tries to attract females with a maneuver that has been termed the “tail-stand-and-sideways-flop.” |
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When not protecting his territory, a male Scartelaos tries to attract a female by performing an ostentatious maneuver that Australian marine biologist Norman Milward terms the “tail-stand-and-sideways-flop.” The fish “stands” briefly on its tail fin before flopping sideways onto the mud. To woo a mate, a diligent fish may do tail-stands again and again—we’ve witnessed eighty-three flips in a row. If courtship is successful, the pair shares a territory and a burrow; the two fish maintain contact by occasionally aligning themselves and wriggling their bodies together, and they appear to communicate with each other by flagging with their dorsal fins as they move about the territory, feeding on plankton and algae (other species eat crustaceans, insects, and worms). The male keeps track of the female as they travel, and if she strays too far, he herds her back toward the burrow.
As the rising tide covers the mudflat, the bearded gobies retreat to the safety of their burrows, where they remain until the tide recedes again. As is the case for Periophthalmus burrows, the water inside those of Scartelaos is low in oxygen, and the fish compensate for this by laying in a supply of air to last through the high tide. Much like farmers lugging bucket after bucket to fill a trough with water, both male and female bearded gobies repeatedly gulp air and transport it into the burrow, creating an underground air pocket. We were able to observe the fish gulping air at the surface, but we didn’t know exactly what was happening inside the burrows. To find out, we developed an artificial mudskipper-burrow system while working at the Australian Institute of Marine Science and at the Scripps Institution of Oceanography in La Jolla, California. Our construction, the first of its kind, was equipped with a viewing porthole through which we could watch the fish create an air pocket. A bearded goby with a mouthful of air must swim vigorously to overcome buoyancy; once inside the burrow, we observed, it floats against the ceiling until the mouthful is released. The fish may then either settle to the floor of the burrow, make immediate use of the reserve by taking a breath of air, or return to the surface to collect another gulp. This air pocket is probably essential to Scartelaos when confined in their burrows at high tide and would thus be doubly important for mating pairs. We further suspect that pairs may lay their eggs in or near the air pocket. Ishimatsu and his colleagues have found that in P. modestus, an air reserve may be essential for proper egg development, and we hope that our experimental system will soon provide similar findings for Scartelaos as well as answers to other questions.
In a 1961 paper describing the natural history of a mudskipper, zoologists Robert C. Stebbins and Margaret Kalk wrote, “Watching these gobies one can readily appreciate the survival value of the terrestrial habit.” By coming ashore, mudskippers have gained an advantage over their aquatic relatives in avoiding competition with other fish and in searching for food. But mudskippers are still fish, and they remain tied to the water—which, because of their knack for burrowing, is never far away.
Heather J. Lee decided by the age of eight that she would become a marine biologist, never mind having grown up in Chicago with “no saltwater in sight.” Now a Ph.D. candidate at the Scripps Institution of Oceanography in La Jolla, California, she's near plenty of ocean. When not underwater or wading through mud, she rides high on her quarter horse, Jet. Jeffrey B. Graham is a physiologist and marine biologist at Scripps. His book Air-Breathing Fishes (Academic Press, 1997) stems from “a career-long interest in the origin of terrestrial vertebrates.” In addition to mulling over our early prehistory, he spends his time painting in oils and enjoying his grandchildren. Lee and Graham thank the National Science Foundation and the University of California's Pacific Rim Research Program for the opportunity to become so intimately involved with mudskipper habitat; returning each day from their fieldwork muddied from head to toe, says Lee, they often inspire both curiosity and laughter from the locals.
Copyright © 2002 American Museum of Natural History