From Here to Maternity

Mothers are remarkable. They can be comforting, exasperating, nurturing, admonishing, smothering, conniving, inspiring, and sometimes downright pains in the backside. They say motherly things, like: "Don't cross your eyes or they'll stay that way", "If you fall and break your legs, don't come running to me", and (my personal favorite) "Always wear clean underwear, so if you're ever in an accident ..." But when it comes down to a crunch, most of us know we can count on our mothers to do whatever they can to help us out, no matter what. Mothers do all these things because they have a deep desire to give their children every edge in a complex and frightening world. Eventually, all children grow up and leave their mothers. And most of us will never have it so good again.

The mothers of other animals also invest an enormous portion of their resources toward the health and welfare of their offspring. In many species without alimony (and sometimes even in one that does), mothers provide the only parental care their young will ever know. That is why the females of most species are larger than the males: they need large bodies to store enough energy to grow, feed, and otherwise care for their young. Males, conversely, are often benefited by 'traveling light' leaving them free to deposit more of their genes elsewhere. Nowhere is large body size and the need to stockpile huge energy stores more apparent than in K-selected females which give birth to large, well-formed young. Elasmobranchs (sharks and rays) are a group of large to gigantic K-selected creatures with a very long history of evolutionary success. This is due in part to their sophisticated methods of conceiving and nourishing their young.

All extant elasmobranchs practice internal fertilization. Male sharks and rays are equipped with paired intromittant organs called 'claspers', modified from cartilages and muscles comprising the inner edge of the pelvic fins. In order to assure the kind of mutual understanding and co-operation necessary for successful mating, elasmobranchs have evolved a wide range of complex pre-copulatory rituals including such behaviors as synchronous swimming, spiraling about one another, gentle biting ('shark hickeys'), color changes, and possibly electrical signals. Prior to intromission, males of some sharks flex their claspers alternately to pump seawater into one of the paired, subcutaneous sacs along the belly. These muscular 'siphon sacs' force several litres of seawater into the female's cloaca, flushing the helical sperm along with it. These sacs are also lined with glandular cells which secrete serotonin, a hormone which stimulates contraction of smooth muscle lining the female's reproductive tract, facilitating fertilization.

The clasper tip of many elasmobranchs is mind-bogglingly complex. Each is capable of unfolding like a flower, exposing a bizarre array of hooks, spurs, and fans which dig into the walls of the female's oviduct to anchor the clasper during copulation. Mating usually occurs on or near the bottom, with the male grasping the female with specialized teeth while his body arches or wraps around his partner, allowing one clasper to flexed across the midline of his body and inserted into her cloaca. The sexual hardware and gymnastics of male elasmobranchs serve to prevent an untimely falling out during copulation (one could, no doubt, write an interesting Kama Sutra for elasmobranchs!). Mating may last many minutes, after which the both partners swim away each apparently unmoved by the experience. If a female elasmobranch mates opportunistically or unseasonally, she can store sperm in her nidamental (shell) gland in a viable state for up to 16 months.

Fertilization in elasmobranchs occurs in the anterior part of the oviduct or in the nidamental gland, depending upon species. Upon fusion of sperm and ova, genes dance and a new generation begins. Elasmobranch ova are very yolky and up to 18 cm long, making them the largest germ cells known. Each ovum is a self-contained life support system, providing the nutriment an embryo shark or ray needs for all (or at least the earliest, most energy-demanding part) of its development. As the developing embryo passes through the nidamental gland, it is wrapped in additional membranes of varying thickness and structure, depending upon the method of parturition characteristic of its species.

Mode of embryonic nutrition and parturition in elasmobranchs embraces a remarkable spectrum, from simple oviparity (egg-laying) through advanced forms of viviparity (so-called 'live birth'). In oviparous species such as skates, bullhead and cat sharks the fertilized ovum is packaged in a thick case. Elasmobranch egg cases are comprised of a unique collagenous protein organized as a tough, cholesteric liquid crystal. The eggs are then moved through the remainder of the reproductive tract and extruded via the cloaca. Elasmobranch egg cases are typically rectangular, but those of the bullhead sharks (family Heterodontidae) are unusual: ovoid with a broad, spiral flange wrapped from end to end. Elasmobranch eggs are usually laid by attaching them to the substrate in some way, where they will continue their development for five to twelve months. Most oviparous elasmobranchs are relatively small, bottom-dwelling species that are evolutionarily conservative. The egg case of the Whale Shark (Rhincodon typus) a gigantic pelagic species is the largest of any known animal, about the size of a briefcase. (Actually, there is some question whether this species is oviparous, as the only egg case ever collected was rather thin-walled). Oviparity is generally considered to be the most 'primitive' form of embryonic nutrition. But oviparous elasmobranch mothers have some marvelous ways to increase the survival odds of their young.

The beautiful deep-sea catshark known as the Chain Dogfish (Scyliorhinus retifer) lays two box-like egg cases at a time, each with long, stringy tendrils at the corners. These tendrils are extruded as a precursor to egg-laying, whereupon the mother Chain Dogfish swims around a deepwater gorgonian or sponge until the tendrils snag. She then uses the bottom growth as a convenient 'hitching post' to pull out and secure her eggs. After the eggs are laid, they will receive no further parental care. Lack of parental care is generally true of both oviparous and viviparous elasmobranchs. An exception is an Australian species of bullhead shark known as the Port Jackson Shark (Heterodontus portusjacksoni). When first laid, the corkscrew-shaped egg cases are pliable and a soft amber in color. Immediately after laying an egg, the mother Port Jackson Shark grasps it gently in her jaws, swims to a nearby rocky reef, and pushes the rubbery case into a crevice. After a few hours in seawater a Port Jackson egg case hardens, the spiral flange making it very difficult to extract for most predators the egg cases must be literally 'unscrewed'. Even for determined divers wanting to collect egg cases for research or display in aquaria, extraction of these cases is not an easy task: some egg cases are 'right-handed', while others are 'left-handed'.

Generally, the larger the shark, the longer the gestation period. But even the smallest viviparous elasmobranchs have rather long gestation periods far too long for the initial yolk supply to stretch. About 60% of elasmobranch species are viviparous, ranging in size from the Lilliputian to the Bromdignagian. Viviparous elasmobranchs include the tiny Dwarf Lantern Shark (Etmopterus perryi) the smallest of all sharks maturing at 16 centimetres in length. At the other end of this size spectrum is the gigantic Basking Shark (Cetorhinus maximus) largest after the oviparous Whale Shark maturing at 900 centimetres in length. Most of live-bearing elasmobranchs are 'ovoviviparous', in which fertilized ova are wrapped in thin, cellophane-like membranes and retained within the mother shark's body to be born alive. In some dogfishes (family Squalidae), several fertilized ova are stacked and packaged in a 'candle', resembling a roll of candies. The ovoviviparous Spiny Dogfish (Squalus acanthias) has a gestation period of 24 months the longest known gestation of any vertebrate. Based on my own studies on vertebral calcification patterns, the gestation period of the ovoviviparous Basking shark may be even longer an incredible three years!

After the yolk supply is depleted, viviparous elasmobranchs have some ingenious ways to nourish their young. In bat rays (family Rhinopteridae), the lining of the mother ray's uterus secretes a whitish, a protein-rich histotroph known as 'uterine milk' which the developing young absorb through the gills, spiracles and other exposed membranes. Diamond stingrays (Dasyatidae), butterfly rays (Gymnuridae), and eagle rays (Myliobatidae) have taken this mode of embryonic nutrition further the uterine lining forms thousands of long, nutritive threads called 'trophonemata' which deliver histotroph into the embryos' esophagus via the spiracles. In many lamnoid sharks, including the threshers (Alopiidae) and mackerel sharks (Lamnidae), late-term embryos are nourished by a continual stream of small, unfertilized eggs into the uterus. This type of embryonic nutrition is termed 'oophagy' (egg-eating). The yolk of these 'mini eggs' is synthesized from phosphoproteins in the mother shark's huge liver, further reducing the energy stores available for her own growth and maintenance.

But the most amazing form of embryonic nutrition among ovoviviparous elasmobranchs must be that found in the Sandtiger Shark (Carcharias taurus). At the tender age of five-and-a-half months (about half-way through their development), embryo Sandtigers develop precocious dentition and swimming ability. The largest embryo in each of two uteri attacks and consumes its lesser siblings, which neatly circumvents any arguments about which sib gets its own room (womb?). This intra-uterine cannibalistic stage lasts about six weeks (or as long as the supply of sibs lasts), after which the pup in each uterus feasts, uncontested, on unfertilized 'mini-eggs'. This rather gruesome form of embryonic nutrition is termed 'adelphophagy' (literally, 'eating one's brother'). Such pre-natal cannibalism is unknown elsewhere in the Animal Kingdom and has been called "the ultimate solution to sibling rivalry". Only two Sandtiger pups are born, one from each uterus. Each pup is unusually large, about 1 metre in length (or about half the length of its mother) and with a characteristic paunch known as a 'yolk stomach'.

This gargoyle-like creature is a 10-cm-long embryo Sandtiger Shark. Despite its tender age of only 5.5 months, it is a miniature murderer, having killed and eaten its smaller brothers and sisters while still in its mother's uterus. Its face rather reminds me of Prince Charles go figure!

The most advanced form of embryonic nutrition occurs in the whaler sharks (Carcharhinidae) and in the closely-related hammerheads (Sphyrnidae). About one-third through their 10-16 month gestation, the whaler and hammerhead pups have used most of their yolk supply. At this stage, the yolk sac undergoes a remarkable transformation: vascularization increases dramatically in density and complexity and the distal portion folds and 'wrinkles' in such a way that allows it to interdigitate with the lining of the mother shark's uterus. This structure facilitates an intimate connection between fetal and maternal blood streams, allowing dissolved nutrients to pass from mother to offspring and nitrogenous wastes from pup to mother. The yolk sac has become a placenta, astonishingly like that of mammals in form and function.

Shark placentas, however, are not exactly like mammalian placentas. In eutherian mammals, the placenta is formed from the embryonic tissues known as 'amnion' and 'chorion', whereas in higher carcharhiniform sharks the placenta is formed directly from the yolk sac. Because of this fundamental difference in tissue derivation, some developmental biologists prefer to term this form of fetal-maternal connection a 'pseudoplacenta'. But since in every other respect the shark placenta is entirely analogous to the mammalian version, I prefer to term that of sharks a 'yolk-sac placenta'. Regardless of which terminology one prefers, it is remarkable that mother whaler and hammerhead sharks independently derived almost precisely the same solution to the challenges of embryonic nutrition as mammalian mothers .... Although, it might be pointed out that sharks 'invented' the placenta some 100 million years before mammals did.

The amazing diversity and complexity of elasmobranch fetal-maternal relationships belies the notion hat these fishes are 'primitive'. The enormous time and resources elasmobranch mothers invest in their young is characteristic of K-selected animal mothers, including whales, elephants, and humans. So why do K-selected mothers do it? Why would a mother Basking shark endure a three-year gestation period, during most of which she is sharing her energy stores via unfertilized 'mini-eggs', to give birth to a half-dozen pups each 1.5 metres long (ouch!!)? Classic ecological theory suggests that by producing such large, well-formed young, K-selected mothers greatly increase the survival odds of their young and thereby, greatly increase their chances of genetic immortality. But maybe there's a simpler explanation: giving birth to kids that are already big enough to pack off to college may get them out of Mum's face a little sooner. Mothers are remarkable but they're not stupid!

Originally published in Diver Magazine, April 1994


ReefQuest Centre for Shark Research
Text and illustrations R. Aidan Martin
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