Pick from the Past
THE ROMAN NATURAL HISTORIAN Pliny the Elder asserted that seahorse ashes applied to the pate with a cuttlefish bone would cure baldness, but that wine in which a seahorse had been boiled was a violent poison. Seahorses have also been credited with curing leprosy, hydrophobia, and infertility. In 1753, Gentlemans Magazine reported that the ladies make use of them to increase their milk, and even today some cultures collect seahorses for their supposed aphrodisiac effect.
But of even greater significance than these legendary attributes is that the male seahorseand only the malebecomes pregnant. The female deposits eggs in the males abdominal pouchwhere they are fertilizedand then provides no further care. Males protect, aerate, osmoregulate, and nourish the developing embryos for several weeks before releasing them as independent young. Labor can last many hours or even days, and the male is ready to remate almost immediately after the young have emerged.
For those of us with an interest in the evolution of differences between the sexes, seahorses are among the worlds most interesting animals, and yet surprisingly little is known about them. For four years I have studied nine species of seahorses, both in my laboratory at the University of Cambridge in England and through fieldwork in the Florida Keys and Australia. I have been attempting to learn whether the intense investment by males in pregnancy affects the sex roles in other aspects of reproductive behavior. In most animals, we claim that the females greater role in producing and caring for young may indirectly explain many male traits, such as more conspicuous color and ornamentation, larger size, higher growth rates, higher levels of aggression, and higher mortality. Therefore, I wondered whether these sex roles would be reversed in seahorses.
A common question is how do we know that the pregnant seahorse is really a male? Why not call it the female? The answer is that male seahorses, like all other male animals, produce small, mobile gametes (sperm), whereas female seahorses produce fewer, larger, energy-rich gametes (eggs). The very question reveals something of our own mammalian bias, with its mandatory maternal care of young. In birds, both parents usually care for the young, and paternal care is the normal pattern in fishes. Male fishes provide the sole care for their young in about half of those fish families with any care and share care with the females in another quarter of the families. Nonetheless, no male animal is known to be more specialized for parental care than the seahorse.
From snout to tail, seahorses are surprising fishes. Their independently moving eyes allow these voracious ambush predators to be ever on the lookout for food. Once a suitable small crustacean is spotted, a very powerful suck from the seahorses long, tubular snout rapidly disposes of the prey. Without either teeth or a stomach, seahorses somehow digest these hard prey. The coronet on top of a seahorses head is nearly as distinctive as a human thumbprint and aids in identification of individuals. Gills are gathered in lobes and resemble bunches of grapes. Seahorses have no scales, and the skin is stretched taut over a series of interlocking bony plates, with spines and knobs at the junctions. The tail is prehensile and so strong that seahorses often cannot be pried loose from a holdfast. The fins have been reduced to just one propulsive dorsal fin, two little earlike pectoral fins used for stabilization and steering, and a tiny anal fin, which has no obvious function.
Seahorses are so unusual that it can be difficult to accept that they are fishes, closely related to the ubiquitous sticklebacks. The sole genus of seahorses (Hippocampus) is found in the family Syngnathidae, which also includes two genera of seadragons and more than fifty genera of pipefishes. In pipefishes, males also incubate young, but the genera differ in the degree to which they are specialized for pregnancy. The various arrangements for carrying youngranging from eggs glued to the underside of the body to slight walls protecting the eggs to flaps fully enclosing the eggs to the fully sealed pouch of the seahorsemay be a guide to how the pouch evolved.
There are about thirty-five species of seahorses in the world, ranging in adult size from the half-inch-long New Caledonian seahorse to the fourteen-inch-long eastern Pacific seahorse, found from southern California to northern Peru. At least three species live off the eastern coast of North and Central America: the dwarf seahorse, little more than an inch long, comes from the Gulf of Mexico; the eight-inch-long lined seahorse is found from Nova Scotia to the Gulf of Mexico; the ten-inch-long slender seahorse is found mostly in the Caribbean.
Whereas pipefishes are widely distributed in deep seas, at extreme latitudes, and even in fresh water, seahorses are restricted to shallow coastal seas and range only as far south as Tasmania and as far north as the English Channel. Seagrass beds are the primary habitat of the family, but seahorses are also found among mangrove roots, on more open, silty bottoms, and even living among vast mats of Sargassum weed. Unlike some pipefishes, seahorses are not coral reef species. Instead, they usually cling to vegetation or other holdfastssuch as sponges, pilings, or ropeson the bottom, sometimes in only a few feet of water and often only yards from shore.
Although seahorses are slow swimmers, their cryptic appearance and armored exterior of bony plates and spines apparently allow them to escape many potential predators. Masters of camouflage, they change color in seconds to match their background, allow encrusting microorganisms and algae to settle on them, and grow longer dermal appendages to blend in with the vegetation around them. They lose these appendages if moved to a simple habitat. They can be so still that only the flicker of an eye tracking a food item betrays their whereabouts. Nonetheless, crabs occasionally prey on seahorses, as do large fishes such as tuna, snappers, skates, and rays. Storms may cause substantial mortality by tearing seahorses loose from holdfasts and casting them adrift to wash up on shore. Fungal, parasitic, and bacterial ailments may also contribute to seahorse deaths in the wild.
Although seahorses depend on their inconspicuousness for survival, the lengthy seahorse courtship is nevertheless active and colorful. It is also surprisingly similar across the nine species of seahorses that I have studied, which come from all over the world. Shortly after dawn, the male and female come together, the male inflates his pouch with water, and the pair signal their interest in courtship by brightening significantly. In the slender seahorse, for example, the male turns orange and the female becomes bright pink. Both seahorses grasp the same holdfast with their tails and, using it as a pivot, begin to circle like merry-go-round horses. At frequent intervals, the pair make their way, in tight parallel formation, across the bottom to another holdfast.
Eventually, they indicate their readiness to mate. The male begins to bend vigorously, jackknifing his tail to meet his trunk and thus compressing his pouch. This motion pumps water in and out of the pouch and closely resembles the motion used by the male to release the young at birth. This behavior may inform the female that the male has an empty pouch or may indicate his capacity to withstand the exigencies of birth.
On the third morning of courtship, the females trunk becomes much more rounded as the eggs ripen in her ovary, and her ovipositor begins to protrude. Larger females produce larger clutches, but clutch size may also depend on the size of a females prospective partner. When she is ready to transfer eggs, the female releases the holdfast and stretches upwardpointsas if to rise to the surface, keeping her tail tip on the ground. Females with large clutches are ready to mate sooner than those with smaller clutches. Eventually the male responds to the females pointing, and together they rise through the water. As they ascend, the seahorses face each other with their tails bent back, and the female inserts her ovipositor into the open pouch of the male and releases her eggs in a long, sticky string. To transfer the whole clutch-which, depending on the size of the species, ranges from tens to many hundreds of eggstakes only about six seconds, and then the pouch opening is sealed shut. The pair break apart, and the male gently sways to settle the eggs in his pouch. Both then settle down on the bottom with their tails wrapped around holdfasts. Each time I watch, I am newly astonished at the beauty and uniqueness of this graceful courtship and mating. During the period of pregnancy that follows, neither the male nor the female remates.
My laboratory experiments have shown that once he has prepared his pouch at the beginning of the reproductive season, the male can mate almost as soon as he is placed with the female. Thus the three-day courtship is imposed by the female, perhaps to insure that the male will be present once she has ripened eggs. Unless a female transfers the eggs to a male within twenty-four hours of ripening, she must literally drop the whole clutch. Dropping a clutch can be energetically expensive (it may weigh 15 percent of the females body weight) and deprives the female of a mating opportunity (she does not prepare eggs again until just before that clutch would have been born), so insuring that a male is waiting to mate has concrete benefits.
The eggs and ovaries of seahorses are distinctive. A cross section of the seahorse ovary reveals a sequence of developing eggs spiraling out from the center of the ovary to the outer edge, where they are shed. Ripe seahorse eggs are usually orange, pear-shaped, and about a tenth of an inch in diameter. Larger females have larger eggs, which usually become larger young. Since in most fish species larger young have higher survival rates, I suspect that male seahorses prefer larger females, although I have not yet tested this.
Sperm is produced in two long testes and released from the urogenital pore into a groove leading down to the pouch opening. Newly deposited eggs are fertilized during or just after entry into the males pouch, and then they are embedded in the pouch wall. What follows can truly be termed a pregnancy: each embryo is supplied with oxygen from capillaries in the tissue surrounding it; the chemical character of the pouch fluid changes from that of body fluids to that of salt water as pregnancy progresses, presumably reducing shock to the young at birth; and the hormone prolactin in the male induces enzymatic breakdown of the egg chorion to create a placental fluid that nourishes the embryos. There may be costs to pregnancy: researchers at the University of Uppsala in Sweden have found that reproductive male pipefishes have slower growth rates and are more vulnerable to predation, possibly because they are slower swimming and more visible.
The length of pregnancy in seahorses varies with water temperature but usually lasts about two weeks in most tropical species. Males release the young by pumping and thrusting repeatedly through a labor that can last several days. The record for the greatest number of young produced in my laboratory is held by a male slender seahorse, which released, from a pouch with a volume of little more than half a tablespoon, a brood of 1,572 young. As soon as they are born, the young rise to the surface to gulp air and fill their swim bladders. They are immediately free swimming and independent, feeding and grasping holdfastsoften each other-with their prehensile tails. Offspring from larger broods are smaller at birth, which suggests that there may be some competition among them in the pouch. Young seahorses of most species probably reach reproductive size in the next year.
One of my most interesting discoveries is that some (maybe all) species of seahorses are tightly pair bonded; that is, a male and female form a bond by mating repeatedly and performing daily greeting rituals. In Sydney Harbor, Australia, male Whites seahorses can be found in almost exactly the same place each morning and move less than three feet all day. The females home range has a radius of up to about nine feet around her mate. In the wild, the paired seahorses come together every morning (whether or not the male is pregnant), change color, and perform the first movements of courtship for a few minutes. I suspected that daily greeting is probably more important than mating in establishing the pair bond, so I experimented by removing a pregnant male from a tank and replacing him with another male. Because a female seahorse does not mate again until after her mate has given birth, the female performed greeting rituals with the new male but did not mate with him during her former mates pregnancy. At the end of this period, I returned the first male to the tank to see which male the female would mate with. She chose her greeting partner over her former mate.
Pair bonding increases reproductive efficiency in seahorses. I have shown that if a male and a female have been together for a long time (at least seven days) before mating, the male gives birth to significantly more young, probably because the male is somehow stimulated by the females presence to increase his pouch capacity or his production of hormones, such as prolactin, important in incubation. Also, the time between matings decreases in pair-bonded seahorses because a female that has been with a male while he is pregnant has already prepared eggs and is ready to remate as soon as he has given birth, instead of requiring a three-day courtship. Furthermore, pairing diminishes the probability that a female will have to drop her clutch for want of a mate. Predation risks should also be reduced in pair-bonded seahorses because they do not need to search for mates, have shorter courtships, and can probably transfer eggs after fewer mating rises.
Among unpaired seahorses in the wild, each lone female stays in a home range, but lone males range widely and try to interact with the females they encounter. Paired seahorses never respond to these males in any way, either by greeting or by competing. In the laboratory, however, I could induce competition by putting two strange males with a single female for three daysor vice versa. Since males do all the work of incubation, I expected that females would compete most for a mate. However, males proved to be much more competitive than females and showed their aggression in behavior never seen in females. Males would wrestle violently or snap at each other by flicking their snouts at each others heads. When competition got very fierce, one male often adopted a submissive posture by darkening and flattening his body against the ground. Sometimes he used this posture as a subterfuge to sneak up and snap at the dominant male. Generally, the biggest and most active males won competitions and succeeded in mating and becoming pregnant. Competition may occur when pairs are initially formed.
Seahorses are not, therefore, sex-role reversed. Males compete more intensely for mates probably because, among unpaired seahorses, there are more males available to mate. Males can mate at once and remain ready to mate for weeks, whereas females take three days to prepare to mate and drop their eggs within twenty-four hours of preparing them. Thus, any nonpregnant male represents a potential rival to a courting male, whereas a second female will not threaten a courting female because the former will most likely not have ripe eggs. As expected from the greater male competitiveness, malesnot femalesare the modified sex, and in at least one species (the big-bellied seahorse) they are larger, more colorful, and more conspicuous than females.
My work on seahorses has produced many more questions than answers. Of the questions, the conservation status of seahorses today is particularly pressing. We know very little about the long-term prospects for most fishes, and seahorses are even less studied than other species. However, fishermen with good local knowledge claim that seahorses are smaller, scarcer, and less colorful than previously. Because of their inshore habitat, seahorses are probably locally threatened by trawling, pollution, and dredging. In addition, the large market for dried seahorses, which are sold as souvenirs and for use in traditional Oriental medicines and aphrodisiacs, may threaten their numbers. I find it disturbing that anyone should want to have a dried seahorse when such a trade encourages the killing of wild seahorses. Also worrisome is that seahorses are popular aquarium fishes, because almost all captive seahorses come directly from the wild. Notoriously difficult to feed and keep healthy in captivity, seahorses are not pets for novice aquarists.
Close acquaintance with seahorses has given me enormous pleasure and provoked a whole host of new ideas about the evolution of sex differences. Although seahorses are not closely related to us taxonomically, a careful examination of their social and reproductive systems gives us a fresh perspective on the roles of the sexes in humans and in other animals.
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