Reproduction and Life Cycles in Marine Animals
In any comprehensive study of oceanography wherein biological activities are implicated or in the study of any population or individual species in relation to environmental factors, it is necessary to take into consideration the nature of the life cycles of the organisms involved. Only thus can the biological activities and the methods whereby the race is maintained through countless numbers of generations be fully understood. The utility of life-cycle studies in such practical fields as economic entomology, parasitology, and fisheries has been abundantly demonstrated. Through a knowledge of the methods of reproduction and through recognition of the various developmental stages of marine animals the investigator has at hand valuable means of aiding the interpretation
It should be pointed out here that, in dealing with the propagation of any individual species in relation to its distribution, we must distinguish broadly between (1) reproductive distribution and (2) sterile distribution. Reproductive distribution is associated with areas where environmental conditions are favorable to maturation, spawning, and larval development. Such areas may be called areas of reproduction, or nursery areas. Sterile distribution is associated with areas in which the submature or adult individuals may live and some spawning may take place, but in which the eggs fail to hatch or the larvae do not survive, so that the area must be restocked periodically by invasion of postlarval stages produced elsewhere.
In a study of the life cycles of marine animals, one is impressed particularly with three facts: (1) the preponderance of animals which, though sessile, creeping, or burrowing in the adult stage, possess a free-swimming period during the early stages of life; (2) the enormous numbers of young that are produced by both pelagic and benthic animals; and (3) the fundamental similarity of the larvae of different invertebrate groups. We shall be concerned only with the first two.
In a superficial survey of populations, it is mainly the larger, more conspicuous adult animals that are seen, yet, from the standpoint of numbers, vastly more starfish, barnacles, clams, crabs, fish, and so on, are represented in the microscopic, feebly swimming larval stages than in the adult stages. Most of these larvae do not survive to assume the adult habit, but, instead, serve as nourishment for other organisms, swimming or sessile, or are in some manner destroyed through action of the physical or chemical environment.
Types of Reproduction. In reproduction, animals are either oviparous or viviparous. The oviparous forms deposit eggs that develop outside the mother's body, while in the viviparous forms the young are nourished by the mother and are born alive in a postembryonic state. An intermediate condition exists in the ovoviviparous forms, where the eggs are incubated and hatched within the body, as in certain sharks, perch, and blennies. The term larviparous is sometimes used to indicate that larval stages are born. An embryo derives its nourishment from the yolk of the egg or directly from the mother, whereas typically a larva is morphologically adapted with mouth and digestive tract for the purpose of seeking its own nourishment. Later it will be seen how important this fact is in the life of many marine animals.
By far the greater number of animals of the sea are oviparous, and it is among these that the extraordinarily large numbers of eggs are
|American oyster||115,000,000||Pacific halibut||3,500,000|
|Sea hare (Tethys)||478,000,000||Cod||4,400,000|
|Teredo navalis, more than||2,000,000||Sunfish (Mola)||300,000,000|
Parental care of eggs and larvae.
It has long been recognized, however, that the exceedingly great number of eggs produced by some species is not directly correlated with the number of adults that are found. The large numbers of eggs and larvae produced are, instead, a measure of the tremendous toll paid by these species in order to assure survival of enough individuals to carry on the race.
In the marine population as a whole, very little parental protection is given to the offspring in the larval stages, and frequently even the eggs are given no care, yet hundreds of examples can be cited wherein varying degrees of protection are afforded the embryonic stages and sometimes the larvae as well. Many of the larger crustacea retain the developing eggs attached by secretions to hairlike structures on the abdominal appendages. Some annelids produce viscid secretions for attaching the eggs to setae or to the body wall, while others retain the young up to a well-developed larval stage in special brood pouches, as in Spirorbis (fig. 77). Many other invertebrates provide brood pouches—for example,
Some types of egg cases for protection of eggs and larvae.
It is clear that in these instances of parental protection the need for large numbers of eggs is somewhat diminished. Nevertheless, when a relatively long, helpless, pelagic stage follows the protected period of incubation, many larvae must still be produced. Thus, for instance, the blue crab, which, though protecting the eggs till the young are hatched, has pelagic larvae and is said to carry over two million eggs (Truitt, 1939). In contrast, Limnoria produces a maximum of only about-twenty-five eggs, but retains these within a pouch until the young are able to burrow into the wood where they were born. Thus they escape the hazardous pelagic life of larvae. In this animal the hazards of a swimming existence are met not by the very young but by submature specimens which by short migrations attempt to establish themselves in less crowded situations prior to breeding (Johnson, 1935). The fact that some animals produce more eggs than others and at the same time offer more parental care must indicate that factors operate to destroy more developing young in one than in the other.
Finally should be mentioned the common method of depositing eggs in masses or protective capsules of various types (fig. 78), thus diminishing loss from excessive dispersal and other hazards of a floating existence during the period of incubation. The capsules are also sometimes
Types of Development. There are two main types of development: (1) direct and (2) indirect. The direct development in oviparous species is associated with eggs of considerable yolk content, such as are found in the fishes, cephalopods, some nemerteans, crustaceans, and others. The newly hatched young are similar to the parent except for size.
Direct development is common among the deep-sea benthic animals, and this habit appears to be an advantageous adaptation. The slowly moving currents of great depths are of less importance in the dispersal of larvae than are the stronger currents of shallow water. The micro-planktonic life so characteristic of surface layers and from which the pelagic larvae of littoral animals directly derive their food has no counter-part in the deep, and hence it is imperative that the young produced be able to feed directly upon the bottom detritus. The possibility of deep-sea larvae swimming from great depths to the surface, where food is plentiful, and later returning to the bottom appears to be impracticable in nature. The young of some mid-depth pelagic forms—for example, Cyclothone among the fishes and Acanthephyra among the prawns—do however live nearer the surface, where food is more plentiful, than where the adults are commonly to be found (Hjort, 1912).
Benthic animals of Arctic and Antarctic regions also commonly possess no pelagic larval stages. Hjort (1912) and Murray (1913) consider this a probable explanation of the great local concentrations of certain boreal and arctic benthic animals, because the direct development results in the young remaining in the area in which they are born. Brief pelagic larval stages following protection during incubation and absence of dispersing currents lead also to local adult concentrations.
The indirect development is associated with a type of egg with little yolk (that is, alecithal), and hence a self-sustaining larva must develop quickly or the organism dies. This type of development is characteristic of marine invertebrates, which usually cast their eggs free in the water or carry them through the incubative period in special brood pouches. Larval stages appear before the full character of the species to which they belong becomes established. Many of these—for example, the pluteus larvae of the Echinoidea and the Ophuroidea—when first discovered were described as distinct kinds of animal, only to be found later to be the young of already well-known species. The locomotor organs of most of the larvae are cilia (see below for exceptions) which by their rhythmic beating propel the animal slowly through the water at a rate just sufficient to keep them in suspension. The great similarity of structure exhibited by the larvae of some groups suggests a common origin for the groups which as adults are structurally very dissimilar.
Typical Life Cycles. The life cycles of many species have not been investigated, but the principal features in the life history of the major groups have been established. We shall here review only the groups of most immediate interest in general oceanographic studies.
In the protozoa, reproduction is mainly by binary fission, whereby the animals divide to form two separate animals, these in turn dividing after growth. Under favorable conditions, this method makes possible a production of great masses of individuals, as is often witnessed in such forms as Noctiluca. Gametes are also formed in this animal as a result of multiple fission. These unite in pairs, but their further development is unknown. In foraminifera, and possibly also in radiolaria, there is a cyclical alternation of generations in which sexual and asexual phases alternate and give rise to morphologically different individuals (Myers, 1936).
In the tintinnids, in which transverse binary fission occurs, the anterior daughter escapes from the lorica, while the posterior daughter retains the old lorica (Kofoid, 1930).
The sponges reproduce asexually by budding or fragmentation, and sexually by union of gametes, the latter resulting in a free-swimming, flagellated larva, the amphiblastula, which, after a period of swimming, settles to the bottom and grows to form the adult sponge. Asexually produced units, known as gemmules, possessing a heavy protective covering are produced by some sponges as a means of survival during adverse periods. Reproduction by formation of gemmules occurs principally among the fresh-water sponges, but some marine forms also produce gemmules.
In the coelenterates, both sexual and asexual reproduction are important features in the life cycle. The union of germ cells results in a free-swimming, ciliated, planula larva about 1 mm long (fig. 80c). The planulae, though lacking the mouth and enteron of typical larvae, may live for a sufficiently long period on yolk food to bring about dispersal of sessile coelenterates such as the corals and anemones. Vaughan (1919) found the pelagic period of corals to be from one day to two or three weeks. Upon settling to a hard bottom the planulae of corals and other Anthozoa develop a mouth and tentacles for feeding, and later the reproductive organs are formed. In some there is also active asexual reproduction by fission and budding. Large coral colonies are thus initiated from a single individual. It is the skeletons of these asexually produced individuals which form the large coral heads, some of which are 3 m or more in diameter and contain many thousands of individual polyps. The length of time required for formation of such colonies has been investigated by Vaughan (1919), who found that a coral colony (Porites asteroides) 50 mm in diameter may be formed in four years.
The remarkable life histories of many jellyfish of the class Hydrozoa offer the examples of alternation of generations that are used in all zoological texts. The jellyfish, or medusa, stage (fig. 79) of such forms as Obelia is either male or female, and the eggs are cast free in the water, where they are fertilized and develop into planula larvae. The planula soon settles on the bottom to form the sessile polyp, or hydroid, stage. From special structures on the polyp, asexually produced buds become separated as swimming medusae, thus completing the cycle. The alternation of sessile and pelagic generations is a factor of great significance in the distribution not only of the hydrozoa such as Obelia, but also of other forms—for instance, the large scyphozoan Aurelia, which, though varying in details of life history, possesses stages similar to those in Obelia. The sessile generation is the chief link instrumental in restricting all stages of such animals to the neritic waters, generally to the proximity of shores and shoals with a suitable substratum of rocks, shells, or larger plants for attachment of the planula larvae. Bigelow (1938) found that in the open sea off Bermuda only about 3 per cent of the medusae caught at a distance of 10 miles from shore were of the type with a fixed stage in their life history. The degree of dispersal is, of course, dependent upon the speed and direction of the water currents prevailing. Some swimming jellyfish—for example, Aglantha digitalis and other members of the order Trachylina—are not dependent upon a sessile stage because daughter medusae develop directly from the pelagic stages.
The life cycle of a typical hydrozoan jellyfish, Obelia.
Open-sea colonial coelenterates—for example, Velella or Physalia—are representatives of the “blue-sea fauna.” Their life cycle is adapted to offshore life by elimination of the sessile stage. The planula larva gives rise to a medusiform stage from which the complicated colony arises.
The Ctenophores are all hermaphroditic, and the eggs are usually shed into the water, where, upon fertilization, they grow by direct development into free-swimming larvae. Gastrodes, a parasite in Salpa, produces a typical planula larva.
The great importance of annelids, especially in the littoral benthic fauna, warrants their inclusion in this brief study of life histories. At certain seasons the voracious swimming larvae of annelids are a major
Some characteristic marine larvae. a, nauplius larva of the copepod Labidocera; b, trochophore larva of the annelid Nereis agassizi; c, planula larva of coelenterates; d, zoea larva of the crab Pachygrapsus; e, veliger larva of the clam; f, bipinnaria larva of starfish; g, the cod larva with yolk sac.
The larvae of many benthic annelids enter the plankton only after they have completed their early stages under some means of special protection. For example, in the little tube worm, Spirorbis, and related forms, they develop in a special brood pouch beneath the operculum, while in some Polynoe, or scale worms, they are sheltered by the dorsal, flaplike elytra, and in yet other instances the eggs are deposited in attached or demersal gelatinoid masses (fig. 78), where the developing embryos and larvae enjoy some degree of protection. In Spirorbis the trochophore stage is passed in the brood pouch and the older larvae may assume the sessile habit after only twenty-four to thirty-six hours in the plankton. If a suitable substratum is not available, the pelagic stage is somewhat prolonged. Nereis agassizi spawns the eggs free
The chaetognaths, or arrow worms, are hermaphroditic but not self-fertilizing. The eggs, which are fertilized internally, are shed into the water, where they develop directly into free-swimming larvae not unlike the adults.
Most crustaceans, in which we are particularly interested because of their prominence in some phases of oceanographic studies, pass through several distinct pelagic larval stages. The common initial crustacean larva is the nauplius (fig. 80a), bearing three pairs of appendages used for both swimming and feeding.
In copepods the sexes are separate, in some species the ratio of adult males to females being strikingly unequal at all times, while in other species the inequalities are seasonal, the males being more abundant at the onset of breeding but later diminishing in numbers more rapidly than the females after the breeding season (Damas, 1905, Farran, 1927, Campbell, 1934). The most important of the planktonic copepods spawn the fertilized eggs free in the water, yet many littoral species and some important pelagic species—for instance, Oithona, Paraeuchaeta, and others—carry the eggs in brood sacs through the period of incubation (fig. 77). In both cases the eggs hatch to typical self-sustaining nauplii. Paraeuchaeta is somewhat of an exception, for it develops from a heavily yolked egg and does not feed in the naupliar stage (Nicholls, 1934). In copepods there are normally six successive naupliar stages separated by definite moulting of the chitinous skin. The hard exoskeleton of crustaceans does not grow, and must therefore be shed or moulted periodically as the animal becomes too large for the encasement. In many crustaceans the number of moults may be variable, but in copepods there are a fixed number of stages, each separated by a moult. At the termination of the sixth naupliar stage a complete metamorphosis occurs from which emerges Stage I of six successive copepodid (copepodite) stages. Copepodid Stage VI is the adult, and, during spring reproduction in waters of the latitude of the British Isles, maturity may be reached in a period of about twenty-eight days in Calanus finmarchicus, but it is much delayed in the autumn-winter generation or in populations of more northern waters.
In Calanus finmarchicus, by far the most thoroughly investigated of all pelagic copepods, it has long been known (Gran, 1902, and others) that the animals spend the winter months in the deeper water layers. The breeding of this species occurs in spring and summer in boreal waters, and there are two or more successive generations, each of which, apparently, may bear more than one brood. The generation arising from the first spring spawning appears to mature quickly, spawn, and die. The last generation produced in autumn is a relatively long-lived
The life cycle of Calanus finmarchicus appears to be quite characteristic of other members of that important genus and perhaps of other related genera as well, but very few pelagic copepods have been adequately investigated, and considerable variation can be expected. We shall not enter into the remarkable life histories of the parasitic copepods, but an example of a typically free-living littoral form—that is, Tisbe furcata—is instructive for comparison with Calanus. Tisbe furcata carries the eggs through the incubative period in brood sacs. There are six naupliar and six copepodid stages, as in Calanus but the time required for development from egg to mating maturity may be as little as ten days, and filled egg sacs are carried by females of the new generation in fourteen days after hatching. During maximum production, one female may produce at least seven or eight broods at about five- to eight-day intervals.
Successive generations of Calanus finmarchicus (from Nicholls).
In the euphasiids, another group of outstanding importance in the economy of the sea, the method of reproduction is not unlike that occurring in many copepods, in that usually the eggs are shed in the water, but the succession of generations is not rapid and the life span is of greater length. For Euphausia superba, in Antarctic waters, the time required to reach sexual maturity is estimated by Ruud (1932) to be two years. Some investigations indicate that normally the animals live in the immediate vicinity of the bottom and that during spawning they congregate in swarms and ascend to deposit the eggs in surface-water layers. Here, while slowly sinking, the eggs hatch to typical naupliar larvae, which are followed by successive stages of distinctive larvae, the older of which may return for a time to the surface layers. In
Among most other crustaceans the eggs are carried through incubation attached to appendages or in brood pouches of various types. In heavily yolked eggs, as in the common crab and related forms, the nauplius stage is passed within the egg, and the developmental stage emerging from the egg is known as a zoea larva (fig. 80d), of which there may be several separate stages. The weakly swimming zoea may drift in the plankton for several weeks before changing to the megalopa stage and settling on the bottom. The lobster produces a special type of pelagic larva. the phyllosoma, which, with its leaflike body, is especially adapted to float in the plankton (fig. 229g). In barnacles, the larvae escaping from the mantle cavity within the shell of the sessile adult are typical nauplii which, after living a pelagic existence for a few weeks, are transformed into what are called cypris larvae (fig. 2241). The cypris larvae soon settle to the bottom and, upon attachment to a solid surface, metamorphose to assume the adult state.
In most bivalve (pelecypod) molluscs the sexes are separate, although some are hermaphroditic, and others—for example, certain species of oysters—are unisexual but change their sex alternately from one to the other. This phenomenon is also observed in other marine animals (Coe, 1940). Fertilization of the eggs frequently takes place after the eggs have been shed into the water, but commonly the eggs are retained within the brood pouch formed by the gills, in which case the spermatozoa are taken in through the inhalant siphon with the stream of water that is kept flowing over the gills. A modified trochophore larva is first formed, and from this a later larva, the veliger, results (fig. 80e). After a period of swimming the veliger settles to the bottom.
Gastropods are often hermaphroditic. Fertilization among them is commonly internal, and their eggs are frequently deposited in gelatinous or membranous cases attached to rocks or sea weed. Tiny floating cases containing several eggs are sometimes formed, as in Littorina (fig. 78). The trochophore and part of the veliger stage are passed within the egg case.
Among the echinoderms the sexes are separate and the eggs are usually spawned into the water, where fertilization occurs. Some (Asterina) lay demersal eggs which, because of their viscid nature, adhere to rocks and other objects. In other echinoderms, especially deep-sea and polar species, the eggs are fertilized and retained in brood pouches, where they undergo early development. Development is indirect in all cases, but the forms with most heavily yolked eggs do not have pelagic
The metamorphosis resulting in the adult state is as complete as that experienced by the butterfly, and it is not surprising that, before the parentage of the pelagic larvae was known, they were considered as distinct animals unrelated to the adult (figs. 80f and 224f and j). The characteristic larvae are bipinnaria (sea stars), echinopluteus (sea urchins), ophiopluteus (brittle stars), auricularia (sea cucumbers). The echinoderm larvae are of only moderate interest in the economy of the sea, but great biological interest is attached to the probable significance of some in showing a relationship to the most primitive chordates.
Many fishes—for example the cod, mackerel, halibut, and sardine—shed their eggs into the water, where fertilization takes place and the developing larvae are nourished by the yolk of the floating eggs (fig. 80g). The herring deposits viscid eggs which, upon sinking to the bottom in shallow water, become attached to solid objects. The gobies, blennies, sculpins, and others attach their eggs to solid objects or lay them on the bottom, where the male may stand guard over them until hatched. The grunion buries its eggs in the sand of wave-washed beaches during periods of high spring tide. Here the eggs remain for a period of about two weeks, when the next series of high tides washes them out and stimulates their hatching (Thompson, 1919, Clark, 1925). In sharks and rays, fertilization is internal, and either the young are born alive or the nonbuoyant eggs are deposited in leathery cases known as “mermaids, purses” (fig. 78, p. 317).
The eggs of fishes fall roughly into two groups, depending upon buoyancy: (1) pelagic and (2) demersal. The demersal eggs sink to the bottom or are deposited there; pelagic eggs float freely in the water and hence greater numbers are produced to overcome the losses inherent with this group. Many fisheries investigations are concerned with the occurrence and dispersal of pelagic eggs and the resulting larvae, for from such studies much information is gleaned regarding the spawning habits and areas of many commercially important fishes (p. 861). In general, the development of fishes can be considered as being direct, there being no general metamorphosis of form to the adult morphology. There is frequently, nonetheless, a marked degree of dissimilarity between larvae and adult, and in some there is a distinct metamorphosis. The Leptocephalus larva of the eel, for instance, was once considered a separate species. Many fishes have definite spawning grounds far removed from their feeding habitat, and the remarkable migrations of such fishes as the eel and the salmon are directly associated with reproductive instincts (pp. 811 and 861).
The reproductive habits of certain deep-sea fishes are of special interest as an indication of adaptation to the environment. In the lightless,
The mammals of the sea bring forth living young, which are nursed for a period by the mother. Like those of some fishes, the great migratory movements of whales and seals are associated with wanderings to and from favorable breeding grounds. Growth in whales is extremely rapid; sexual maturity may be reached in two years, and one calf may be produced every other year.
The spawning of many marine animals, especially in boreal waters, is of a spontaneous nature, and vast numbers of individuals spawn within a period of a few days, with the result that in such cases the main spawning period is easily ascertained, since great swarms of eggs or larvae appear suddenly in the plankton and are gradually dispersed by water movements. This feature is especially well illustrated by the oyster, certain sea cucumbers (Cucumaria), nereid worms, and barnacles.
The degree of success of (1) spawning or (2) survival of larvae of successive spawning seasons gives rise to an inequality in numerical strength of year classes of adult or juvenile forms constituting any given population. This inequality is best demonstrated by studies of commercial fishes, investigations of which have been most ardently pursued. However, the same inequality must also occur in the populations of any animals with a normal life span sufficiently long for individuals to live through several reproductive seasons as juveniles and adults.
For purposes of illustration we may consider a species with a life span of several years in which the age of individuals can be accurately determined and in which adequately large and inclusive samples are obtainable for comparison. Now, assume a highly successful spawning and larval survival in a moderate population of this species in the breeding season of 1930, a very poor spawning season in 1931, an average degree of spawning and survival of larvae in 1932, and then another highly successful year in 1933. The 1930 year class will, upon investigation of the whole population in 1931, show up as a disproportionately great number of small, one-year-old individuals in relation to the other age groups in the population. In the next year (1932) the two-year-old individuals of the 1930 spawning are still conspicuous in the population, but the smaller number of one-year-old individuals is evidence of a poor spawning or survival for the 1931 reproductive season. Thus, in 1933 and subsequent years the downward trend of numerical strength of the 1930 and 1931 classes can be traced and compared with other year classes—for example, that of the average year 1932 and of the successful year 1933
From such comparative studies of year classes and with a knowledge of the spawning habits and age groups, means are provided for analysis of probable environmental factors that determine the degree of success of spawning or survival of larvae, because the relative number of individuals entering into any year class must depend mainly on these critical periods. In subsequent years within the normal life span of the species, the reduction of numbers in year classes is not so likely to be of catastrophic nature. It has been pointed out by Hjort et al (1933) that for a given region the average rate of growth of individuals within the different year classes of Norwegian herring is the same for each year class regardless of the relative numerical strength of the classes. This seems to indicate that, in the sea, nature each year provides a sufficiency of food for the survival and growth of the older stages of this fish as represented in the composite commercial catch. The numbers of individuals belonging to the separate year classes may be widely different (as much as 1 to 30), and this difference must then result from some factor or multiplicity of factors operating to destroy the animals during the very early stages of their existence.
Schematic illustration of changes in year class composition of a population.
Studies of commercially important fish, shellfish, and whales are deeply concerned with analysis of the year classes. For example, in nature there is an equilibrium between the rate at which fish enter the accumulated stock or supply and the rate at which they are withdrawn through natural mortality. Additional removal through fishing exploitation disturbs this equilibrium and may constitute so serious a drain upon the stock that the drain becomes greater than the rate of replenishment and the stock subsequently becomes so depleted that it is no longer
Year-class analyses of the fish population are also utilized as a basis in arriving at forecasts of the most probable abundance of fish in the next year's catch. Illustrative of this are the investigations of the U. S. Bureau of Fisheries into the fluctuations so characteristic of commercial catches of mackerel. Sette (1931et seq) studied the relative abundance of these fish caught with reference to each year class of the population. The numerical strength of the younger year classes entering into the catch provided a basis for calculating the probable yields that these classes would give in the following year under similar conditions of fishing. Such calculations can be significant only when the downward trend in numbers of the dominant year classes is rather regular. In dealing with migratory fishes, the occurrence of sporadic invasions of populations produced elsewhere or with a different range and whose year-class composition is not known must give rise to unexpected changes in the ratio of the year classes occurring in any one range or locality under investigation. The continued success of such commercial fisheries as the mackerel is determined mainly by the numerical strength of the dominant year classes of the population native to the fishing area. In the above investigation it was found that the big year class of 1923 constituted the main bulk of a declining fisheries yield for a period of years until the industry again experienced a sharp upward incline as the contingents of the 1928 successful spawning entered the catch.