In the sea, as in the terrestrial environment, the prime relationship between organisms is that associated with nutrition, and, indeed, the relationships leading to the above classification of associations are, in the final analysis, nutritional.
Other relationships are expressed in associations for protection and, within species, for reasons of propagative or social instincts. But the association for protection is only a reaction against rapacious enemies seeking food and is therefore part of a nutritional relationship between predator and prey.
Allen (1934) has reviewed pertinent literature dealing with the microscopic plants as the primary food of the sea. In the sea as on land the nutritional relationships result in a food cycle of producers and consumers in which solar energy and the regeneration of inorganic nutrients utilized by plants in photosynthesis form vital links. But the relation
The Significance of Micro-plants
It has been shown that sea water possesses in solution all of the necessary inorganic elements, phosphorus, nitrogen, iron, and so on, for the manufacture of plant substance with the aid of light. In other words, the sea as a whole possesses the potentialities of sustaining such autotrophic organisms as are capable of capitalizing upon this tremendous supply of nutrient material held in solution. Although the sea offers these possibilities to plant growth, at the same time it also sets up certain serious physical difficulties and barriers by reason of the magnitude, depth, and fluidity of the oceans. We know that it is only the merest rim of the sea that has sufficient light and, at the same time, suitable substratum for attached and other bottom-living plants, and that in the open sea plant life is restricted by the factor of illumination to only the upper few meters represented by the euphotic zone. This relative restriction of living space makes it of vital importance to plants that they overcome or minimize materially the effect of gravity that might lead to their destruction below the euphotic zone. This serious challenge of the pelagic environment has been successfully met by the plants, and the method by which it has been conquered has determined largely also the kind of animal life that the sea can support.
In order that the vast stretches of the ocean may be populated and its nutrient resources used by plants beyond a depth of about 40 m, special types of plants adapted to a floating existence have evolved. To accomplish a pelagic habit, two methods appear to be open. (1) The development of buoyant forms with air bladders or similar features to keep them at the surface. This is the means evolved by the macroscopic alga Sargassum. This method, however, is subject to serious handicaps and can hardly be considered a successful one; moreover, although plants of this nature float in large masses and reproduce vegetatively in restricted places such as the Sargasso Sea, yet their natural home is along the shore attached to rocks from which they have been torn. Such buoyant plants can extract nutrients only from a shallow layer at the immediate surface and unless maintained in large eddies of relatively quiet water, they are subject to being rapidly driven by the wind and currents into coastal areas, there to be destroyed by stranding and by beating of the surf. The contribution of organic material by such plants is relatively small. (2) The really successful method by which plants have been able to
The Significance of Micro-animals
One may ask what influence this type of development of the plants has had on the animal population of the sea. Along what lines has the animal economy evolved to exploit this vast supply of microscopic plant food in the sea? A plant population consisting mainly of scattered individuals that are microscopic in size must impose certain restrictions and requirements upon the animal grazers that depend upon it for nourishment. It is significant that in the sea the chief grazers, representing the main bulk of the zooplankton, are also microscopic or semimicroscopic in size and vast in numbers. Foremost among the grazers of the pelagic region are placed the copepods, the diet of which has been shown by direct analysis to consist mainly of diatoms, dinoflagellates, and other micro-plants, but many other small herbivores, especially protozoans, euphausiids, and larval stages of larger invertebrates also graze directly upon the phytoplankton.
Through all the tiny grazers of the sea nature accomplishes two important ends: first, complete utilization of even the minutest particles of primary food; and, second, transformation of the organic material of these plants into animal substance of size sufficiently large to be caught and utilized by carnivorous forms. The large number of carnivorous animals that occur in the sea is abundant evidence that the numbers of microscopic grazers must indeed be great (p. 896). Much economy would result if the larger animals could feed directly upon the plants in the manner of the large terrestrial animals, but the nature of the environment prohibits the growth of large plants except in a narrow fringe along shore and, except for a small amount in the eel grasses, no seeds with concentrated nutriments are produced as on land for immediate use or as a store to be drawn upon during periods of low vegetative growth. It is true that some fishes, particularly the herrings, feed to some extent directly upon minute plants, especially during their larval stages (Lebour, 1924a), and an exceptional few, such as the menhaden with their notably fine filtering apparatus, feed partly on diatoms and dinoflagellates throughout life (Bigelow, 1926).
In our concept of plant-animal relations, the plants are to be looked upon chiefly as autotrophic organisms capable of converting inorganic material to organic material, thus making it available to animals as particulate food. Lohmann found in the Bay of Kiel that for every multicellular animal there were one thousand protozoan and seven thousand protophytan forms. It is extremely difficult to obtain reliable measurements of the relative volume of plant and animal substance in the sea, but, since only through the endothermic process of photosynthesis can the solar energy be bound and become available for the building of animal substance, it is obvious that the mass of plant material produced must be greater over a long period of time than the mass of animal material. It appears that even at periods of only moderate production the very rapid rate of reproduction in unicellular plants is sufficient to maintain the zooplankton population, even though the bulk of plants actually present at any moment may be less than that of the animals. It should be emphasized that the rapidity of reproduction of the nanno- and microplankton is as important as the bulk present in the water as food at any given time. Lohmann calculated that even though the mass of plants may fall below that of animals in the Bay of Kiel, yet plant production usually exceeds animal consumption during the summer months. The excess may be 29 mm3/100 l of sea water. During winter both production and consumption fall off, but during midwinter, January and February, there is a production deficiency of −0.8 mm3/100 l of sea water.
It must be pointed out that some of the organic material produced by plants is lost to the animals through solution in the sea water; the content of dissolved organic matter in the sea runs as high as six or more milligrams per liter of sea water (up to three milligrams of carbon per liter; p. 250). This represents much more organic material in the sea in solution than exists there as particulate food at any one time, and any organisms that are capable of reclaiming this dissolved organic material have an important role in the economy of the sea. Bacteria doubtless serve this purpose (p. 911), but other saprophytic forms may also play a part. Some dinoflagellates are believed to be saprophytic, but their utilization of dissolved organic matter from the water in such dilute concentrations has not been demonstrated. Attention has already been called to certain “olive-green cells” regularly collected in deep water from the South Atlantic by the Meteor. These have a maximum distribution below the euphotic zone and Hentschel (1936) believes them to live heterotrophically. If this is true, they are important in reclaiming dissolved organic matter and building it into bodies of suitable size for use by filter-feeding animals at mid-depths.
In the following analysis of food relationships our purpose is not so much to learn the habits of individual animals, though to do so is extremely important and indispensable in understanding the biology of
In studying the food relationships of the marine organisms, it is perhaps most convenient for our purpose to group the animals according to the kind or source of food upon which they subsist and according to general methods of feeding, remembering at the same time that the feeding habits of many are unknown and that many have habits not clearly confined to any one of these categories but overlapping more or less into others. The larval and adult stages may also differ both in food required and in the method of procuring it. The first two groups given below are based on the source and kind of food used and, incidentally, on the method of feeding. The last two groups are based mainly on methods of feeding, but this feature itself results largely from the nature of the food.
Plankton and Filter Feeders
Under this heading are included the forms that feed upon microscopic or semimicroscopic organisms and suspended detritus floating or swimming freely in the water. It is here that the uniqueness of the food cycle of the aquatic environment is most clearly manifest. It is not practicable to segregate strictly the true plankton feeders as a group from the feeders on finely divided, suspended organic detritus because most plankton feeders include detritus in their diet, owing in part to the method of gathering food. They may also be designated as “suspension feeders,” after Hirsch. Many of the plankton feeders may be called filter feeders because of the method in which they collect their food. Most of them are provided with some type of screening device through which the water is passed while the small organisms are retained as food. A few examples will serve as illustrations.
In filter-feeding copepods, Calanus finmarchicus for example, the head appendages known as the second maxillae are provided with a number of curved setae or spines each covered by numerous fine hairlike processes. The appendages are paired and together form the main part of a filtering net or chamber just posterior to the mouth. The head appendages lying between the first antennae and the second maxillae,
The filter-feeding apparatus of Calanus finmarchicus: (a) ventral view, anterior portion of animal, distal parts of first and second antennae and mandibles removed; (b) lateral view of entire animal. The lines with arrows indicate the vortices set up. (According to Cannon.)
The great abundance of euphausiid crustaceans makes them highly important plankton feeders because they share largely with the copepods the distinction of being grazers upon diatoms and, owing to their habit of living in large swarms below the euphotic zone, they must be of great significance in intercepting and utilizing the slowly sinking plant material produced above in the lighted zone. Euphausiids are known to be quite omnivorous, feeding on a wide variety of floating material, plants, animals, and detritus. This they comb out of the water with their long thoracic limbs which together form a basket through which water is pumped by the swimming legs (Bigelow, 1926, Lebour, 1924b).
The pelagic tunicate Oikopleura is a most remarkable type of filter feeder. Its food consists of the minutest of drifting organisms, the nannoplankton such as coccolithophores, bacteria, small diatoms and dinoflagellates, and other minute forms, which are filtered from the water by means of gratings in the animal's temporary vestments or “houses.” This portion of the plankton may constitute as much as a third or more of the total mass of plankton at some seasons and localities. The house of Oikopleura, in which it lives while drifting about in the plankton (fig. 239), is a gelationous investing structure secreted by the animal. Water is drawn into the house through funnel-like structures guarded by a set of fine mesh gratings (outer filter) capable of excluding organisms of size greater than about 0.127 mm × 0.0345 mm. In the house the water circulates through another set of filters (inner filter) that retain organisms about 0.030 mm in diameter. The water is circulated by undulatory movements of the animal's “tail” and is expelled through a second opening in the house, thus propelling the house through the water. The extremely fine material collected on the inner filter is drawn into the animal's mouth by means of ciliar action. After a few hours the screening devices become clogged and the animal then escapes from the structure through a third separate opening (exit). Having freed itself from the old useless vestment, it secretes a new one with all the complicated structures for gathering the type of food upon which it is dependent.
The filter-feeding apparatus of Oikopleura.
There are also many plankton filter feeders among the sedentary or burrowing animals. Indeed, the permanently attached forms so characteristic of the marine fauna (and by comparison so conspicuously wanting in land fauna) can exist as such only because the water carries to them sufficient nourishment in the form of suspended particulate food,
A familiar example of the filter-feeding habit is that of the simple sponge, wherein flagellated cells lining internal cavities propel the water into the sponge by way of the numerous incurrent pores covering the surface of the body. After passing through the more or less complicated canal system, the water is then expelled through a common opening, the osculum, but enroute the individual flagellated cells select out the fine particles of food carried by the water.
Many plankton feeders may be better classified as preying animals, although in some respects they combine this habit with filter feeding. Any attempt to distinguish between such categories is based largely on the relative degree of selectivity exercised in feeding. Few animals are wholly indiscriminate in feeding, and even filter feeders exercise some degree of selection, either by a mechanical segregation of size dependent upon apertures of the screening apparatus, as in Oikopleura or sponges, or by rejecting through ciliary or other action certain particles unpalatable for chemical or physical reasons.
We have mentioned copepods chiefly as herbivorous plankton filter feeders but not all copepods feed upon diatoms and other phytoplankton organisms. The free-living types like Tortanus and Candace that may be considered largely carnivorous and rapacious have very strongly built mouth appendages for catching and holding their prey.
Jellyfishes and ctenophores are highly predaceous in habit, feeding voraciously upon other plankton animals that drift within their reach. The former paralyzes its prey by means of batteries of nettle cells which cover the tentacles. The latter (Pleurobrachia) when in swarms are very destructive to large numbers of other small organisms, of which they sweep the waters quite clean. The prey is entangled in the trailing tentacles which are provided with sticky adhesive cells. In his study of food relationships in the Gulf of Maine, Bigelow states that “of all the members of the plankton, the most destructive to smaller or weaker animals are the several coelenterates, and especially the ctenophore genus Pleurobrachia, a pirate to which no living creature small enough for it to capture and swallow comes amiss.”
The filter-feeding apparatus of the California sardine: (a) gill cover and gills removed to show one side of branchial sieve formed by gill rakers; (b) enlarged camera lucida drawing of section of branchial sieve; (c) Oithona plumifera, a small copepod drawn to the same scale as (b); d, Calanus finmarchicus, a medium-sized copepod drawn to same scale as (b). Compare with fig. 90, p. 377.
The formidable jaws of the arrow worm Sagitta attest that it is also a highly rapacious plankton feeder; being able to snatch individual organisms like Calanus and larval fish despite the fact that it possesses only light-sensitive “eye spots” instead of true eyes (fig. 228a).
Among smaller important plankton forms, mention should also be made of the tintinnids, radiolarians, foraminifera, Noctiluca, and other planktonic Protozoa that engulf such small organisms as chance carries within their reah. These are plankton feeders but not filter feeders. That some may exercise a degree of selective feeding is indicated by the tintinnids, some of which are found regularly to contain only the shells of silicoflagellates, while others select certain coccolithophores, the coccoliths or armor of which they use in building their shells.
Among the more or less obvious preying plankton feeders may be placed many fishes, notably herring, mackerel, sardines, and others of this type (p. 896) which either select out individual animals of the plankton or filter quite indiscriminately by the aid of the gill rakers, which form a net through which water entering the mouth must pass in its course over the gills and out under the gill coverings (fig. 240). The fineness of the net or branchial sieves formed by the gill rakers varies with different types of fishes, and in unclogged condition determines the minimum size of the planktonic organisms that can be sieved out for food. Even the menhaden, Brevoortia tyrannus, with a notably fine branchial sieve, is unable to retain organisms as minute as coccolithophores and small diatoms and infusoria. In the herring the sieve is much coarser, and though these fish are known to select out organisms individually the gill rakers must assist materially in retaining many of the smaller Crustacea. The stomach of a single herring has been found to contain more than 60,000 copepods. It should be noted that though much of plankton feeding may appear indiscriminate, yet a good deal of selection does occur, since swarms of specific prey may be selected and followed, as is evidenced in the herring and in the filter-feeding whalebone whales. The plankton-feeding fishes are swift swimmers but the usefulness of this ability must be in large measure to escape their enemies, the typical large predators (see below), although most plankton feeders do in part also prey upon other smaller fishes.
A portion of the frayed baleen plates forming the filter-feeding apparatus of the whalebone whale.
It is a strange fact that the largest animals, that is, certain of the whales, are plankton feeders, living upon great masses of very small animals. These are the Mystacoceti or whalebone whales, of which the blue whale or sulphur bottom, the largest of all living animals, is an example (fig. 76 a, p. 314). In the mouth of this type of whale are suspended the closely set plates of whalebone (fig. 241) through the frayed ends of which water is passed while the planktonic euphausiids, copepods, pteropods, and so forth, which make up the principal diet, are filtered out. Whales are most abundant in waters rich in planktonic life and, as indicated in fig. 244, p. 904, their numbers may be correlated with the abundance of planktonic food of their preference.
Numerous other examples could be given from diverse animal groups to illustrate the manner in which nature exploits the supply of microscopic but vastly numerous and scattered particulate food floating freely in the water. Any considerable fluctuations in the abundance or distribution of the planktonic food must quickly affect the plankton feeders and, in due time of course, other types of feeders as well.
More will be said later (p. 901) about general problems involving filter feeding, production, and population density.
Detritus Feeders and Scavengers
We have learned that much of the organic material produced in the pelagic zone is precipitated to the bottom in the form of living or dead bodies of the planktonic and nektonic organisms and their excreta. Added to this is detrital material resulting from disintegration of benthic plants and animals and also from influx of terrestrial material. In
The organic material available in this mixture on the bottom is fed upon by bacteria and other microorganisms such as Protozoa, nematodes, and rotifers, and the whole mixture in turn is consumed by larger detritus feeders. Bottom organic detritus is sometimes considered the main source of nourishment for most benthic invertebrates. In a survey of Danish waters Blegvad (1914) concluded that of 90 or more species of invertebrates investigated, 69 (the most common animals) were some form of detritus eaters, while 5 were herbivorous and carnivorous and 16 were purely carnivorous. In the strictest sense only those organisms subsisting solely on detrital organic remains are detritus feeders, but it is not practicable in a general survey to draw the line so closely. So in a broader sense, we see that some detritus feeders may be nourished in part by living organisms and are not necessarily entirely scavengers in habit. In the littoral zone, especially in the eulittoral zone, part of the detrital mixture consists of photosynthetic organisms such as littoral diatoms growing naturally on the bottom and thus contributing to the organic material available in the detritus.
The concentration of detritus feeders is, of course, dependent upon the extent of production of plants and nonscavenger animals. Where this production is great, there also the scavengers must be numerous. With increasing depth, the detrital food on the bottom becomes less. The plant material diminishes until in the great depths not even sinking pelagic plants produced in the euphotic zone above ever reach the bottom, being disintegrated through bacterial action or autolysis, or eaten and converted into bodies of animals. Such mid-depth and abyssal pelagic animals serve as links in a series of changes that convey sufficient organic material, as animal detritus, from the euphotic zone downward to the bottom to support at least a sparse benthic population of detritus-feeders, and the animals that in turn live upon them. It is hardly conceivable that any plant material as such ever reaches the bottom to enrich the detritus of abyssal depths. The rate of sinking of Chaetoceros diatoms in still water is only about 1 m in 4 3/4 hours. Plankton animals such as salps sink at the rate of 4000 m in 2 days 7 hours (Hesse, Allee, and Schmidt, 1937). The low temperature of great depths is important in delaying bacterial action, thus allowing more time for sinking before complete disintegration takes place, while the rate of sinking must
Various types of animals may be mentioned as detritus feeders. Their habits of feeding are varied and may combine several methods. Such burrowing worms as the lugworm Arenicola and others, and the protochordate Balanoglossus, swallow the mud indiscriminately in the process of digging and are nourished by whatever digestible material may be present in the mud and sand.
The clam Macoma nasuta, lying buried in the mud and sand of shallow water, extends its long inhalant siphon to suck up slime that has accumulated on the surface of the mud. The digestible material thus taken in is entangled in mucus and propelled by cilia to the labial palps and the mouth. The bivalves Nacula and Yoldia gather detrital material by directly extending the unusually long labial palps to pick up the food.
Among the echinoderm detrital feeders the sea cucumbers, illustrated by Stichopus, suck up large quantities of mud and detritus that has come to rest on the bottom. It has been calculated (Crozier, 1918) that in certain shallow coastal areas of Bermuda, these animals pass 6 or 7 kg (dry weight) of mud per square meter per year through their digestive tracts; in a certain enclosed area of 1.7 mi2 the mud eaten annually may be from 500 to 1000 tons. The stomach fluids are somewhat acid and may dissolve calcium carbonate. Feeding of this type is important in the biological “working over” of bottom deposits. The sea urchins, Strongylocentrotus spp., also subsist on plant and animal detritus. The mud-dwelling brittle star lies buried below the surface of the mud with several arms extended out over the surface in contact with the top slime which they collect and carry to the mouth.
Mud-dwelling tube worms collect the nutrient-rich detritus by means of extended cirri along which food material can be carried in ciliated grooves. Detritus feeders living in the mud also have their quota of filter and mucus feeders, although the material consumed doubtless also consists of typical planktonic organisms as well as suspended organic detritus stirred off the immediate bottom by currents or, in some instances, purposely stirred into suspension by the animals, for example, by Callianassa and other Crustacea.
The echiuroid worm Urechis, which inhabits U-shaped burrows in muddy sand, has a remarkable method of obtaining food through a combination of mucus secretion and filtration. Mucous glands at the anterior end of the worm secrete a funnel-shaped mass of mucus 5 to 20 cm long lining the upper end of the burrow in front of the animal. The broad end of the funnel fits against the walls of the burrow, while the narrow end fits as a snug collar around the anterior end of the animal. Water is then forcibly pumped through the burrow from front to back and in its passage through the mucous tube small particles of detritus,
An interesting method of detrital feeding is shown by the sand crab Emerita, which inhabits wave-washed sandy beaches especially in tropical and subtropical waters. Living in sand burrows in the lower part of the intertidal region, the animals face seaward while their long feathery antennae protrude from the sand to intercept fine detrital material that is washed out with the receding waves.
In the littoral zone where large quantities of attached benthic plants are produced, many herbivorous or omnivorous animals also are found that feed directly upon the growing plants and are therefore to be considered a complement to the small but numerous planktonic grazers and the plant detrital feeders so vital in converting plants into animal substance. The large benthic algae have their greatest significance as a source of animal food in the temperate and boreal regions (p. 293).
Numbered among these littoral algal grazers are many gastropods, crabs, shrimps, and amphipod and isopod crustaceans. The devices used in mincing the plants consist of horny rasplike radulae in the gastropods, and claws, pinchers, and mandibles of heavy chitin in the crustaceans. A number of fishes, for example the rudder fish (Kyphosus) and the butterfly fish (Chaetodon) as well as other reef and littoral fishes, also browse on the attached algae.
It is not feasible to separate sharply the browsers from the detritus feeders and scavengers, since they perhaps all feed more or less indiscriminately upon growing plants or upon living or dead fragments, some of which may be washed far to sea. Indeed, most plants are eaten after they have become detached from their moorings and while in the process of breaking up mechanically or through decay. This was also the conclusion of Hewatt (1937) in special observations on food relations of intertidal animals at Monterey Bay. Petersen (1918) reports that eel grass is utilized mainly as detritus and that it may either be spread over the bottom or carried as fine particles in the water.
The relation of marine wood-boring organisms to their food supply constitutes an unusual one in the sea and may be arbitrarily mentioned under this presnent heading.
Much organic material is washed or blown into the sea from land which incidentally becomes available as food for marine life. Few instances can be cited wherein typical organisms of the sea are directly dependent upon organic products from the land. Such dependence is
On the whole, it is animals of this type that are best known to the layman, for they are usually relatively large and their feeding habits tend towards the spectacular. We have already had occasion to mention a few of the preying animals such as the jellyfish, arrow worm, certain copepods, plankton-feeding fishes, and whalebone whales because of their role in utilizing the food offered by the micro- and macroplankton. The fishes and whales of this type were considered, in part, also as filter feeders.
Fast-swimming predators, among which are the surface fishes tuna, barracuda, and salmon, are provided with well-developed eyes and efficient teeth to aid in capture of their prey, which consists largely of plankton-feeding fishes. It should be noted here that such plankton-feeding fishes as the herring, sardine, menhaden, mackerel, anchovy, and alewife are fishes of exceptionally great abundance and are eagerly sought as food by the larger preying animals of the pelagic region. Some idea of their numbers may be gleaned from the fact that over 500,000 tons of sardines have been taken in in one year from California waters alone (Scofield, 1937), and the menhaden yield of the east American coast may reach 400,000 tons in a year (Tressler, 1923). Such fishes must therefore stand as an important link between the animal plankton and the larger piscine predators unprovided with direct means of gaining sustenance from the small planktonic life. High in this complex food pyramid are also the toothed whales and other marine mammals.
The pelagic fishes of great depths are also predators but they are of relatively small size, usually ranging upward to only a few centimeters. This small size may well be correlated with the scarcity of food at these depths. The diminutive sizes not only represent a conservation of organic material in growth, but also, owing to the increased ratio of
Among the nonplankton-feeding predator mammals of the sea are the toothed whales, for example the sperm whale (fig. 76b, p. 314), which is provided with teeth only in the lower jaw and which dives to great depths for its favorite food the squids, including the giant squid, the largest of all invertebrates. Other cetacean predators are the killer whales, porpoises, and dolphins, animals adapted to swimming with incredible speed and provided with teeth in both upper and lower jaws. To these must be added the seals, the sea lions, and the walruses. The first two catch their prey (fish and crustaceans) with very well-developed but ordinary teeth, while the last are specialized with long tusks with which to dig shellfish from the bottom.
Many benthic animals are predaceous, living upon each other and upon other bottom animals already discussed as users of detrital and finely divided food occurring on the bottom. The list includes many bottom-living fish called “bottom feeders” or “ground fish.” The best known among these are the plaice, flounders, halibut, croakers, cods, and rays which live on the crustaceans, shellfish, worms, and coelenterates of the bottom community.
Sea stars are notably voracious feeders on bivalve molluscs, a single specimen having been known to devour five or six clams in a day. Predaceous snails, distinguished by their long siphons, are also enemies of bivalves and other molluscs, drilling a neat hole through the shell and eating the soft contents.
The interrelations of the organisms of the sea are diagrammatically summarized in fig. 242. The volumes indicated are not based on computations and should be considered as being only very roughly proportional
The marine bacteria are a vital link in the nutritional relationships of all marine organisms, but it is more convenient to discuss these later under a special heading (p. 908).
The main features of the interrelations of marine organisms.