14.6: Reproduction

To reproduce successfully, each species must ensure that enough of its offspring survive to reproductive age and that these progeny in turn produce enough of their own offspring to continue the cycle. Reproductive cycles are poorly documented or poorly understood for all but a few marine species, but the basic elements of their diverse strategies are known.

Separate-Sex Reproduction

The majority of marine species reproduce by sexual interaction between male and female. Sexual reproduction increases genetic diversity (CC17), which improves the species’ ability to survive and adapt to environmental change.

In sexual reproduction, sperm is transferred from male to female by a copulatory organ or directly from the male sexual organ to eggs laid previously by the female. Alternatively, sperm is either discharged into the water, where it fertilizes eggs retained by the female, or eggs released into the water, where fertilization occurs.

Direct transfer of sperm from male to female requires relatively few eggs and sperm to ensure sufficient fertilizations. Hence, this strategy minimizes the energy needed to produce eggs or sperm. However, it requires that males and females locate each other for breeding, which for many species is a major problem, especially if they are permanently attached to a surface. Many motile fishes and invertebrates find mates in mating congregations that assemble at a specific time of year and place. Mating congregations enable some fishes to select mates that have desirable characteristics.

The mate location problem has been solved in an unusual way by a number of species, including some barnacles and fishes that live at depth, in the dark. In these species, one sex is relatively small and resides either near or directly on the other. The smaller sex is usually the male because producing sperm requires less energy, and hence less body weight, than producing eggs does. The deep-sea anglerfish (Fig. 14-15) is a good example of a species that uses this strategy.

In pelagic reproduction, sperm and often eggs are released into the water (Fig. 14-28a,b,c,l). Sperm are attracted to eggs or females of their own species probably by chemotaxis (“tasting” or “smelling” of chemical clues released into the water by eggs or females). If sperm are released far from the eggs or females, or at a different time than the eggs, the probability of fertilization is very small. Consequently, pelagic spawning often occurs synchronously among all males and females of a given species in a specific region. Often this synchronous spawning occurs at a specific time of year or on a specific day. The timing is usually coordinated with a particular phase of the tides, such as high spring tides at full or new moon. Corals (Fig. 14-28a), many other benthic invertebrates, and many fishes spawn synchronously. In some fish species, a male and female pair will spin around each other or swim in contact with each other (Fig. 14-28b), simultaneously releasing and mixing a cloud of sperm and eggs. Other species form spawning congregations in which vast clouds of sperm and eggs are released simultaneously. Often the individuals swim in a school or swarm that spirals inward and upward toward the surface as sperm and eggs are released. This movement ensures that sperm and eggs are concentrated in an intensely mixed, dense cloud; keeps the eggs away from benthic predators; and probably reduces loss to pelagic predators.

 

 

 

 

Figure 14-28. Reproduction. (a) Synchronous spawning of a hard coral colony (Acropora sp., Papua New Guinea). The eggs, the pinkish white globules, are all released within minutes of each other to float up and join the plankton where they hatch. (b) Mandarinfish (Synchiropus splendidus, Indonesia) male and female pair photographed almost exactly at the instant that they spawned. At dusk, they swim very rapidly upward about a meter from the rubble patch where they live, release their eggs and sperm at the same instant, and then return rapidly to safety. (c) This female Lembeh frogfish (Antennarius sp., Indonesia) is swollen with eggs. She and the much smaller male that was waiting close by swam upward and spawned near the surface a few hours later that night. (d) Although they are all hermaphrodites, nudibranchs exchange sperm through ducts in their side, seen connected in this image (Hypselodoris bullocki, Indonesia). Each individual retains and lays its own fertilized eggs. (e) Nudibranch laying eggs (Kentrodoris rubescens, Papua New Guinea). (f) On rare occasions, three nudibranchs may exchange eggs and sperm simultaneously (Nembrotha rutilans, Indonesia). (g) Nudibranch eggs are laid in a characteristic spiral ribbon pattern encased in a protective gel (species unknown, Hawaii).

 

 

 

 

Figure 14-28. Reproduction. (h) Snails, although related to nudibranchs, nearly all reproduce sexually, but they also lay eggs encased in a protective gel (Epitonium billeeanum, Papua New Guinea). (i) Common reef squid eggs (Sepioteuthis lessoniana, Papua New Guinea) laid in rubbery gel casings in a seagrass bed. (j) Flamboyant cuttlefish eggs (Metasepia pfefferi, Indonesia) laid under a coconut shell half. The individual near the center of the image is close to hatching, and the unhatched cuttlefish can be seen through the transparent egg case. (k) Many species of damselfishes, including this Indo-Pacific sergeant (Abudefduf vaigiensis, Vanuatu), lay eggs on the reef surface and then stay to defend the eggs aggressively from potential predators until they hatch. The eggs are the tiny reddish brown dots covering the reef surface behind the sergeant. (l) Sea cucumbers that normally lie flat on the substrate (see inset) rear up as high as they can before releasing clouds of eggs or sperm. Fertilization takes place in the water column, where the sperm are attracted to the eggs by chemical sensing; but the fertilization rate is low, and large numbers of eggs and sperm must be produced (Thelenota rubralineata, Papua New Guinea). (m) Most of this burrowing sponge (Oceanapia sagittaria, Indonesia) lies buried under the sediments. It reproduces vegetatively by growing the round ball-like structure in the image, which is released to the currents. (n) Banggai cardinalfish (Pterapogon kauderni, Papua New Guinea). The male shown here is incubating eggs (the orange spherical objects) in his mouth. If you look closely you can see the eyes of some of the young that are almost ready to hatch.

Hermaphroditism

In many species, hermaphroditic life cycles have solved the problem of finding or ensuring the presence of a mate. Hermaphrodites are individuals that have both the sexual organ (gonad) necessary to produce sperm and the sexual organ necessary to produce eggs. In certain species, including most nudibranchs, the individual may perform either the male or female function, or both, at any time in its sexually mature stage (Fig. 14-28d,f). The common acorn barnacle is also a hermaphrodite in which each individual has a penis that can be used to inject sperm into any other barnacle because each barnacle also has ovaries. Thus, although adult barnacles are permanently attached to a surface, a suitable mate is always present in any location where these barnacles are well established (Fig. 14-7c).

Sequential hermaphroditism is the ability of an individual to change from female to male or from male to female at an appropriate time in its adult life. The female-to-male sex change confers an advantage to species in which reproductive success is aided by the presence of a strong, experienced male during reproduction. For example, damselfishes (Fig. 14-28k), including anemonefishes (Fig. 14-20), lay their eggs on the reef surface (under the edge of the anemone in the case of anemonefishes). Reproductive success in these species depends on the successful defense of fertilized eggs against predators. For a given anemone, an anemonefish family may consist of a large aggressive male, a somewhat smaller female, and usually 4 to 10 smaller subadults or juveniles. The male defends the eggs from predation and defends his anemone from predation by butterflyfishes. If the male dies, the female grows and changes sex, and one juvenile grows to become a sexually mature female.

A male-to-female sex change is the preferred strategy of many species in which the female produces more eggs as it becomes larger. This strategy is common in invertebrates. For example, the common eastern oyster (Crassostrea virginica) is a male for several years as it grows, and then it transforms into a female. In transitional individuals, both sperm and eggs may be produced and the individual may even fertilize itself.

Asexual Reproduction

There are several different methods of asexual reproduction, including binary fission, fragmentation, and vegetative reproduction. In another form of asexual reproduction, unfertilized eggs develop into adults, but this reproductive strategy is rare in marine life.

In binary fission, a single-celled organism divides into two offspring. Diatoms reproduce by binary fission (Fig. 12-17). Fragmentation is a reproductive process of multicelled organisms that is similar to binary fission. For example, fragments of certain macroalgae and of some invertebrates, including various worms and sea stars, can break off and develop into new individuals. In some cases, fragmentation occurs through the production of special buds that are designed to break off the main individual. This budding process is common in macroalgae and sponges.

In vegetative reproduction, a single individual divides into many individuals that may or may not be physically connected. Vegetative reproduction is the most important marine asexual reproductive mechanism and occurs in many marine algae and invertebrate species, particularly colonial forms, including corals, sponges (Fig. 14-28m), and anemones. In benthic invertebrates, a single larva may settle on a substrate, metamorphose, and then reproduce vegetatively to cover a broad area of substrate.

Asexual reproduction produces many individuals that are genetically identical clones. Therefore, colonies of vegetatively reproduced anemones or encrusting sponges, for example, are all the same sex and color. Cloned colonies can occupy a substrate very densely because the cloned individuals do not have aggressive territorial responses toward each other as they would toward other individuals of their species. This lack of aggression may be important in colonial species, such as the Portuguese man-of-war, in which millions of cloned individuals must cooperate, each performing only one of a variety of separate and different functions needed to feed, defend, move, and reproduce the colony.

Asexual reproduction allows the successful colonization of suitable benthic microhabitats encountered by a single settling larva and avoids the difficulties of ensuring that sperm and eggs are united successfully. However, asexually generated populations have little genetic diversity, and hence the colony, and the species, may be poorly adapted to survive any unfavorable changes in its environment.

Egg Laying 

Most marine fish and invertebrate species are oviparous and lay large numbers of eggs that hatch on the seafloor (Fig. 14-28e-k) or in the water (Fig. 14-28a,b,c,l) to become larvae that are meroplankton. In most cases, the vast majority of the eggs and larvae (sometimes more than 99.999%) are consumed by carnivores before they reach adulthood. For benthic species, many additional larvae may die because they settle on unsuitable substrates. Therefore, species that have pelagic eggs and/or larvae generally must produce very large numbers of fertilized eggs to ensure survival of the species. Species that spawn eggs to the water for fertilization must produce especially large numbers of eggs because many will not even be fertilized.

Production of very large numbers of pelagic eggs ensures the wide dispersal of larvae, which enables them to take advantage of the dispersed phytoplankton food resource. For benthic species, the dispersal of large numbers of larvae also facilitates the colonization of suitable substrate where this substrate is found only in isolated areas. Because this strategy carries a substantial energy cost, many species of oviparous fishes, such as anemone-fishes (Fig. 14-20) and other damselfishes (Fig. 14-28k), lay many fewer eggs on the substrate and protect the eggs from predators until they hatch. Other species, including many sharks, skates, and rays, octopuses and squid (Fig. 14-28i,j) lay only a very few eggs that are protected from predators in tough envelopes or encased in a gel (Fig. 14-28d-h). Finally, ovoviviparous fishes retain fertilized eggs within their reproductive tracts until they hatch. Seahorses (Fig. 14-16h,i) and some pipefishes (Fig. 14-16e) have an unusual incubation mode whereby newly fertilized eggs are deposited in a pouch on the male’s abdomen, where they remain until they hatch. Some cardinalfishes incubate eggs in the male’s mouth (Fig. 14-28n).

Although it would seem to be energy-efficient to produce fewer eggs and protect them until they hatch, energy must be expended to protect the eggs, and this strategy does little to reduce mortality during the larval stage. Larval mortality can be reduced if larvae can evade some predators, but to do so, the larvae must be relatively large. Remember, if larvae are small, they cannot swim effectively, because of the enhanced effect of viscosity (Chap. 5). If larvae must be large when hatched, eggs must have large yolks to provide the energy for growth. This requirement offsets any energy gained by producing fewer eggs.

Viviparous species are at the opposite extreme from the prolific pelagic spawners in the trade-off between egg numbers and protection. In viviparous animals, including mammals, offspring are nurtured inside the mother’s body until they become fully developed and assume adult or nearly adult form. Some shark and ray species are viviparous, as well as all marine mammals. Only one or two offspring are produced at a time because of the large amount of energy needed to nurture the offspring during its prebirth development, but the large live-born offspring have a high rate of survival to reproductive age.

Timing

The timing of reproduction during the life cycle and during the year can be important. Spawning in some species takes place over a period of days or weeks at the same time each year. In other species, individuals may spawn several times a year; and in some species, spawning is almost continuous because at any given time, some individuals in the population are spawning. In middle and low latitudes, most pelagic spawning species spawn only once a year, in spring. This pattern synchronizes the production of larvae with the availability of abundant food supplies from the spring phytoplankton bloom.

In many species, the time of spawning may be determined by variations in light intensity and temperature, which also influence the timing of the phytoplankton bloom. Dramatic year-to-year variations in the reproductive success of many species can and do occur. They are due in part to annual variations in factors controlling the timing of the phytoplankton bloom and of spawning. In some years, spawning may occur at the wrong time or place, in which case larvae miss the phytoplankton bloom and their population incurs massive starvation losses. Omnivores and carnivores suffer in turn, and their populations decline.

In tropical latitudes and certain upwelling areas where plankton food supply varies relatively little during the year, pelagic spawners have a greater tendency to spawn year-round. However, this trend is not universal, because even in these areas, monthly, biannual, or annual synchronous spawning still provides many advantages for larval survival that are not afforded by continuous spawning.

In certain species, spawning is timed to provide the maximum protection of eggs from predators. The best-known users of this method are the small fish called grunion that spawn on southern and Baja California beaches, and the horseshoe crab that spawns along the Atlantic coast. These and other species deposit eggs to incubate in beach sands above the high-tide line. Thus, eggs are protected from the many predators that abound in coastal waters and sediments. Eggs must be placed in sand high enough up the beach to be free from wave action or they would soon be washed out and devoured.

Grunions cannot climb above the high-tide line, and both grunions and horseshoe crabs have pelagic larvae that cannot crawl across the beach to enter the water after they hatch. How do grunions and horseshoe crabs place their eggs in sand above the high-tide line and yet ensure that the sand is covered with water when the larvae hatch? Each species times its spawning to occur at or a little after some of the highest spring tides of the year. In the grunion’s case, the high spring tides that occur on the Pacific coast during summer are perfect because the highest tide of the day (see the discussion of mixed tides in Chapter 10) occurs at night. At high tide in the darkness, when they are safe from air attacks by birds, grunions can move into very shallow water high up on the beach. There they lay eggs during a frenzied spawning that lasts about 30 min, until the tide recedes. After the eggs are laid, tidal ranges diminish as spring tides progress to neap tides, and then build back toward the next set of spring tides. Two weeks after the eggs are laid, the next set of spring tides occurs (Chap. 10). By this time, the eggs have matured. When the overlying sand is resuspended by waves of the high spring tides, eggs are released to the water and the larvae hatch, becoming meroplankton.

The factors that determine the timing of spawning within a given year are relatively simple to understand. It is more difficult to understand why some species reproduce only once and then die while others reproduce repeatedly, and why some species mature rapidly while closely related species may take much longer to reach reproductive age. The average mortality rate of larval and adult stages, energy requirements of spawning, and year-to-year variability in larval mortality rate are believed to be important and interrelated explanatory factors.

In species with high adult mortality and relatively low larval mortality, natural selection will favor early and one-time reproduction. Because adult mortality is high, individuals that mature late will be selectively removed from the population because they are more likely to die before they produce offspring. Individuals that spawn more than once will also be selectively removed because they are likely to die before reaching a second or subsequent spawning cycle. Thus, for many species it is a successful strategy to reach maturity quickly, spawn only once, and then die. Salmon and eels are prime examples of species that use this strategy. Also, these fishes make long-distance migrations to spawn during which they stop feeding and deplete their own body tissues for fuel. This metabolic cost makes it evolutionarily more efficient to invest all remaining energy in a single reproductive event rather than attempting a return journey.

If egg or larval mortality is high in relation to adult mortality, natural selection will favor individuals that mature late and spawn more than once. Individuals that mature early and divert a large fraction of their food energy resources to reproduction, but relatively little to growth and predator avoidance, will be more likely to die early. An individual that matures late, devotes most of its energy to growth and survival, and diverts only a small amount each reproductive year or cycle to reproduction will produce more eggs in its lifetime. The late maturer is larger when reaching reproductive age, and thus it is capable of producing more eggs than a younger-maturing individual could, while expending the same amount of energy as a percentage of body weight. If this late maturer invests a relatively small proportion of its food energy in reproduction during each year, it can survive to spawn repeatedly, further increasing its lifetime egg production.

Selection for late maturity and multiple spawning cycles is further enhanced by great year-to-year variability in the survival of eggs and larvae. Survival through multiple spawning cycles enables a species collectively to outlast excessive variations in egg production or survival in successive spawnings. Because adults of several ages contribute to each year’s total egg production, the effect of a small or missing year class (resulting, for example, from a poor year for larval survival) is minimized. Pelagic eggs and larvae are subject to intense predation and to ocean current and climate variations. Many fishes and benthic invertebrates with pelagic eggs and larvae have the relatively late-maturity and multiple-cycle reproduction that is associated with high and variable mortality of eggs and larvae.

Even closely related species can have very different reproductive timing. For example, the common mussel (Mytilus edulis) and California mussel (Mytilus californianus) are closely related and coexist in some areas. Because M. edulis has high mortality due to predation, it is outcompeted by M. californianus for living space in places where the larvae of both species settle. M. edulis invests a very large amount of energy in reproduction in comparison with M. californianus and spawns once a year in winter, whereas M. californianus spawns throughout the year.

Migration

Many marine animals migrate between different regions during their life cycles. The migrations can cross tens of thousands of kilometers, but typically they are much shorter in distance. Generally, one area on the species’ migration route is its reproductive site, where eggs are fertilized, released, or deposited. The other end of the migration route (or other points on a complex migration pathway) is the main feeding ground for adults and/or juveniles. Hence, for most species, migration can be viewed as a strategy for ensuring appropriate habitat and food supply for each life stage of the species.

Migration may place larvae where appropriate food supplies are abundant and adults in another region where their different food supply is plentiful. However, migration is often not this simple, because adequate food supplies for each stage often are present throughout the migration route or at only a single location.

Why then do species not avoid the energy expenditure imposed by migration? There may be several answers. For example, the species might deplete available food in a specific region if it did not migrate to allow recovery of the food species populations. Migration may also place eggs, larvae, and/or the adult populations in locations where they are less subject to predation. Alternatively, migrations may enable species that are usually scattered widely across large ocean areas to congregate in one or more breeding areas, thus improving the chances of finding a mate and enhancing genetic mixing and diversity. Finally, adult migration to a spawning ground may ensure that pelagic eggs and drifting or weakly swimming larvae are carried by ocean currents to locations where food suitable for young adult stages is abundant. After drifting to such feeding grounds, larvae can metamorphose to the adult stage. Each of these possible advantages of migration and probably others are important for some species.

The North Sea herring has a migration–reproduction pattern typical of many abundant coastal pelagic fishes. Adults feed for much of the year in areas of rich plankton production off Norway (Fig. 14-29). In spring, herring migrate across the North Sea to spawning grounds near the Scottish coast. There they breed and lay eggs, which attach to stones or gravel on the seafloor. After they hatch, the larvae are transported eastward by currents to the adult feeding grounds, where they assume adult form.

Figure 14-29. North Sea herring migrate from feeding areas off the coast of Norway to a number of localized areas off the Scottish coast to spawn.

Anadromous and catadromous fish species have perhaps the most amazing migrations. For example, the catadromous Atlantic eel, Anguilla, spends its approximately decade-long adult life in freshwater rivers of North America, Europe, and the Mediterranean Sea. At the end of this period, the eels undergo changes that include exchanging their dull gray color for a silver hue and growing enlarged eyes typical of pelagic fish species that live below the photic zone. The eels then migrate down their home rivers and thousands of kilometers across the oceans to the southeastern part of the Sargasso Sea (Fig. 14-30a). There, the eels breed and then presumably die. Their leaf-shaped larvae (called leptocephali) are a few millimeters long when they begin their journey to the streams that will become their adult homes.

 

Figure 14-30. Migration routes. (a) Adult Atlantic eels migrate from their river homes in Europe and North America to the southwestern corner of the Sargasso Sea, where they spawn and die. Their larval offspring travel back to North America and Europe via the North Atlantic subtropical gyre currents and enter rivers (generally the home rivers of their parents), where they grow to maturity. (b) There are several species of North Pacific salmon, each of which has a somewhat different migration pattern. This figure shows a typical pattern in which the juvenile salmon migrate from their home streams to sea to spend 3 or more years migrating and feeding in the North Pacific Ocean between Alaska and Russia. The adults then return to rivers (usually to their home streams) to spawn and die.

The American population drifts north with the Gulf Stream for 1 or 2 years before somehow sensing the proximity of the rivers of their ancestors, at which point the eels swim upstream to reach their new freshwater homes. European eels take 2 to 3 years to drift to their European homes. Mediterranean eels take an additional year to drift north with the Gulf Stream and then back to the south with the eastern boundary current of the North Atlantic Gyre until they can enter the Mediterranean. Although all Atlantic eels are considered the same species, the American, European, and Mediterranean eels are genetically distinct. These distinct populations may breed in slightly different areas of the Sargasso Sea so that larvae can join the Gulf Stream at the best point for the most efficient ride home.

In the Pacific Ocean, a similar species of catadromous eel that has adult populations in North America and Asia migrates to a spawning region in the southwestern part of the North Pacific Gyre that corresponds to the southwestern corner of the Sargasso Sea. Many details of the eel’s migration, breeding behavior, and spawning locations are still unknown. In addition, as with all migrations, the chemical, magnetic, visual, or other clues that eels use to guide their migration to appropriate locations are unknown and subject to much research.

Pacific salmon are anadromous species that use a migration pattern almost opposite that of the eel (Fig. 14-30b). Salmon start life as eggs laid by the parent in gravel beds of rivers along the North Pacific coast. The eggs hatch 1 to 4 months later, and the resulting plankton-eating larvae grow quickly. During either their first or second year, juvenile salmon swim down the river to the ocean. By the time they reach the ocean, they are small but voracious predatory fishes. The salmon grow into adults and migrate across the Pacific Ocean to their selected feeding grounds, which range throughout the North Pacific Ocean. After remaining in the ocean up to about 5 years, they return to their home streams to breed and then die.

Salmon usually lay only several thousand eggs, far fewer than many other fish species. However, the eggs and larvae have relatively low mortality because they are protected from the abundant ocean predators through the spawning migration. Hence, the features of the salmon reproductive cycle are comparatively low egg and larval mortality, a single relatively early reproductive cycle followed by death, enormous energy costs of spawning migration, and production of a relatively small number of eggs in a favorable habitat. These features constitute a stable and successful reproductive strategy, as described earlier.

Almost all salmon return to the stream in which they hatched. They are thought to achieve this feat by “smelling” the distinctive chemical compositions of their home streams. However, contrary to popular misconception, not all salmon successfully migrate back to their home streams. As many as 10% to 20% are known to lose their way and migrate to streams other than their original home. Such “mistakes” are probably important to the maintenance of genetic diversity in the species and to the recolonization of streams where catastrophic events may have destroyed the spawning population.

The longest known ocean migrations are those of sea turtles and marine mammals, particularly the California gray whale. Sea turtles range far and wide throughout the oceans and return with great reliability to the beaches where they hatched.

All baleen whales, which, with the exception of the gray whale, are filter feeders, migrate seasonally. They feed in plankton-rich, high-latitude waters during spring and summer, and they return to warm tropical waters to breed in winter. California gray whales are unique among baleen whales because they feed by sifting sediment to eat small sediment-dwelling crustaceans called amphipods and they undertake one of the longest known seasonal migrations. In summer, they feed in the Bering and Chukchi Seas (Fig. 14-31a). When winter approaches, they migrate south along the North American coast, generally staying within sight of land. Their migration takes them some 11,000 km south to the shallow coastal lagoons of Baja California, where food is extremely limited and where adults must live off the fat reserves built up during summer. In the warm lagoon water, gray whales breed and females give birth 1 year later. Although young whales weigh about 2 tonnes, they have relatively thin layers of blubber, the fat that protects these warm-blooded mammals from losing body heat. If they were born in colder waters where the amphipod food supply is abundant, their mortality rate would be very high. The annual 22,000-km migration is therefore undertaken to ensure both adequate food for adults in summer and the high survival rate of offspring necessary to this species, which, like all other mammals, produces few young during its lifetime. Other whales, such as the humpback, also make long annual migrations (Fig. 14-31b).

 

Figure 14-31. Some whale migrations. (a) California gray whales migrate annually between feeding areas in the Beaufort and Chukchi seas and breeding areas off the coast of Baja California. (b) Humpback whales feed in the far North Pacific Ocean and Bering Sea and migrate to breeding areas around Hawaii and Baja California.