Tuatara: Volume 11, Issue 2, June 1963
The Terrestrial Plankton
The Terrestrial Plankton
‘The term “plankton”, from the Greek planktos meaning drifting, was proposed by Hensen as a collective term for the small organisms which occur suspended or free-swimming in water and whose powers of movement are so restricted that they drift at the mercy of currents.’ It may seem paradoxical to refer to the ‘terrestrial plankton’ but the phrase ‘dry land’ is a misnomer, not even a desert is wholly dry. All terrestrial habitats retain moisture and the total volume of water held in these environments is probably almost equal to that of the volume of the freshwater lakes and rivers, 0.25 Gg. (Hutchinson, 1957, p. 223). Further, the freshwater lakes and rivers are being constantly replenished chiefly by water that has passed over or through terrestrial environments. This annual precipitation on land surfaces is of the order of a geogram (1020g.) or four times the total volume of all inland waters. The annual evaporation from land surfaces is equal to about two-thirds of this figure and the runoff to the sea is equal to about a fifth (Hutchinson, 1957, pp. 221-230). ‘Dry land’ is, therefore, deeply involved in the hydrological cycle and there is ample water to provide a rich variety of niches for aquatic organisms. The peculiarity of these niches is that the moisture is held in small discrete surface films or pore spaces, greatly restricted in volume, and contrasting sharply with the ocean, lakes, and rivers. Secondly, the currents to which this kind of water is subject are those of wetting and drying, of precipitation, drainage and evaporation. Thirdly, these waters tend to be much richer in mineral and organic nutrients than other natural bodies. Indeed the blooms of freshwater and marine plankton are often associated with the influx of fresh runoff carrying not only the major nutrients, page 58 such as phosphate, but also essential growth factors such as vitamin B12 (Hunter et. al., 1956). Fourthly, and perhaps most significantly, there is the close association with higher plants, an organic cycle different to that of most freshwater and marine environments.
In terrestrial environments the variety of the plankton is not as great as that of the marine and freshwater habitats but the structure of the population is very similar. Exceptionally the organic cycle is dependent upon algal photosynthesis (e.g. Antarctica, Flint and Stout, 1960) but generally the vegetation is dominated by the higher plants. Romer has pointed out that the evolution of the higher plants was a necessary prerequisite for the evolution of terrestrial animals and it has also provided a wealth of niches for aquatic microbial life, not only in such bizarre reservoirs as those of the pitcher plant, the bladder wort, or the axils of Astelia but more typically on leaf. stem, and root surface and particularly in the decaying vegetable matter of the forest floor. Here at its richest and in its most typical form may be found the terrestrial plankton.
Algae and phytoflagellates, most commonly unicellular, bacteria, yeasts and protozoa form the nannoplankton. The three latter generally closely associated with fungal mycelium, fine roots, and decaying vegetation. The smaller metazoa include rotifers, nematodes, tardigrades, gastrotrichs. turbellarians, enchytraeids and other aquatic olgichaetes. The Crustacea are represented by copepods, cladocera, and ostracods. There are also insect larvae and minute gastropods. These organisms may attain very great populations. Bacteria may number 109 per ml. of free water, yeasts perhaps 1% of the bacterial total, protozoa several thousands, and so on. Some figures of populations estimated by a dilution technique are given below:—
|Nos. per ml. water:|
|Grassland topsoil||Beech forest litter|
|Protozoa||Rhizopods||26 - 124||545 - 9392|
|Ciliates||63 - 487||545 - 4540|
|Nematodes||59 - 292||700 - 1238|
|Rotifers||Few||204 - 1880|
|Copepods||Absent||62 - 307|
No attempt has been made to estimate the mass of these organisms but it is clear, from the numbers alone, that they form an appreciable part of the terrestrial population.
The predominance of higher plants has displaced the importance of the algae in the food chain of the terrestrial plankton. Few of the zooplankton are obligate feeders on diatoms or other algae. The majority depend on bacteria, yeasts, or perhaps fungal mycelium. Some are phytophagous and others are micropredators. Ingestion of plant remains is rare among the smallest plankton although some of the nematodes and the larger animals, such as the copepods and aquatic oligochaetes, pass large quantities of plant detritus through their gut. However the greater part of page 59 dead plant material, consisting as it does of cellulose and lignins is inaccessible to most animals, the exceptions, such as the tipulids, termites and ruminants, being those with a specialised cellulolytic enteric fauna and flora. They are dependent therefore, directly or indirectly on the cellulolytic activity of saprophytic fungi and bacteria. It seems possible, indeed probable, that those planktonic animals which do ingest dead plant material, such as the copepods and oligochaetes, derive their nutrients not directly from the vegetable debris but from its associated nannoplankton of bacteria, fungi, and protozoa. If this is true of the plankton, it may also be true of other soil animals, (e.g. Wigglesworth, 1942, p. 281; Engelmann, 1961). It is well known that the plant material that passes through the gut of many soil arthropods is chemically little changed. This suggests a very inefficient method of nutrition but it could well be that these arthropods are not feeding on the plant debris but on its associated fungi and other micro-organisms. Because the restricted distribution of the free water in which the plankton live prohibits the use of such devices as filter feeding terrestrial predators are driven to the only alternative — a complete ingestion of the plankton and its substrate and the separation, by digestive processes, of the edible plankton from its inedible plant substrate. This may well explain the enormous activity of soil animals in plant litter and the failure in most cases to show the presence of significant amounts of cellulolytic enzymes. On the other hand the constant comminution of the dead plant material passing through the gut of soil animals renders it more accessible to microbial attack, and the animal droppings become active centres of microbial proliferation. The relationship may be seen therefore as one of symbiosis. Where larger animals tend to be absent, such as in peats, the process of degradation is slowed down and incompletely decomposed organic material tends to accumulate.
Some figures are available of the activity of the fauna both in the physical comminuation of plant litter and of its chemical degradation. Litter animals such as oribatid mites or amphipods may consume between 25 and 40% of their own weight of litter per day. Of this only about 20% is digested. In the case of mites it is estimated (Engelmann, 1961) that of the digested material by far the greater part is metabolised in the respiration of the animals but Clarke, in his study on the amphipods in a New South Wales podocarp-broadleaf forest, estimated that only about a sixth of the digested material was respired the rest being lost as dead animal tissue in the non-predatory mortality of the amphipod population. Such dead animal tissue, however, represents a far more readily accessible source of nutrients for other soil organisms than the plant tissue and one suspects that it would be rapidly metabolised by other organisms.
Physical comminution by soil animals is illustrated by Nef (1957). ‘If a pine needle 60 mm. long. 1 mm. broad and 0.5 mm. deep page 60 and therefore having an initial surface area of 180 mm.2 is fed to an earthworm which reduces it to fragments of 1 mm. diameter the surface area will be increased to 240 mm.2 but if it is attacked by mites which reduce it to fragments of 1003BC diameter the surface area becomes 1.8 m.2 or 10,000 times the original.’
In Figure 1 an attempt is made to present the relationships of the terrestrial plankton to the larger animals in soil and particularly forest litter. The principal sources of available nutrients are:— (I) soluble nutrients, such as carbohydrates, amino-acids, and soluble proteins initially derived from leaf drip, dead leaves and twigs; and (II) insoluble nutrients, such as cellulose and lignin. The insoluble nutrients are rendered accessible to soil animals only by bacterial and fungal action and they become accessible in one of two ways, either in the form of microbial cell tissue or in solution as autolysed tissue. In the first case they may be eaten either by the microfauna or the macrofauna and in either case contribute to increase of animal tissue and respiratory activity. In the second case they contribute to the sum of soluble nutrients available in the system.
Similarly animals feeding on the microflora suffer either predatory or non-predatory mortality. In the first case their tissues are used in respiration or synthesis by their predators and in the second soluble nutrients may be released by autolysis or they may become centres of microbial proliferation. The relationships are complex but the pattern is uniform. The sum of synthesis and respiration, predatory and non-predatory mortality tends to release at least part of the available energy of the system in the form of soluble nutrients and these soluble nutrients augment the initial source from leaf drip; from frass, honey dew or other products of phytophagous arthropods; and from dead plant litter. It is this pool of soluble nutrients which constitutes the main substrate of microbial proliferation, supports the terrestrial plankton, and which directly or indirectly provides the basic nutrients of the great majority of soil animals. It also seems likely that it is the concentration of these nutrients in the soil profile which determines the rate of respiration rather than the size of population. Measurements on beech leaves have shown the highest rates tend to be in the more freshly fallen leaves — provided they are wet. Here the populations are lowest but it is likely that soluble nutrients, not yet leached away, are at their highest concentration. In beech leaves, which are not readily eaten by soil animals, the greater part of loss of weight of the litter can be accounted for by respiratory metabolism in situ, at least in the early stages of decomposition. It seems very likely that this reflects the predominant role of microbial growth and metabolism, which may well provide the immediate substrate of the associated animal population.page 61
Characteristics of the Plankton
All planktonic organisms are minute but the terrestrial representatives are remarkable even within this range for their relatively small size. Thus the most common of terrestrial copepods are harpacticids, cyclopoids are rare, and the most common of the harpacticid copepods, Epactophanes richardi is only about 0.5 mm. in length. Similarly terrestrial ostracods are relatively small, the New Zealand species, Mesocypris audax, Chapman, 1961, being about 1.1 mm. in length. Of the aquatic oligochaetes the representatives of the Aeolosomatidae occurring in terrestrial habitats are all only about 1 mm. in length, the Naidid worms are larger, up to several mm. long. Phreodrilids and enchytraeids are larger again but in this case the worms possess a thicker body wall, a morphological character shared by the earthworms, which makes them less susceptible to variation in hydrostatic pressure.
The terrestrial nannoplankton, such as the protozoa, is similarly remarkable for its small size. Thus terrestrial species are almost invariably smaller than freshwater or marine representatives of the same genus and where more than one species is present it is typically the smallest which is the most common. Thus while a catch of terrestrial plankton has many similarities to a catch of fresh water or marine plankton the most striking difference is that it will need to be studied under a higher magnification and it is reasonable to associate this distinction with the confined character of their aquatic habitat which restricts moisture to thin films and narrow pore spaces.
A second feature of the terrestrial plankton is the relative simplicity of form and life history. Most groups are capable of asexual reproduction and the life cycle tends to be short and direct. Again it seems reasonable to associate these characters with the necessity of accommodating an aquatic mode of life to an environment capable of frequent desiccation. The formation of cysts or, in the case of copepods, eggs capable of enduring periods of drought is also typical.
Apart from the nannoplankton — the bacteria, the yeasts, and protozoa — little is known of the physiology of the terrestrial plankton. Many of the larger forms, such as the copepods, appear to be sensitive to high carbon dioxide concentrations or low oxygen tensions such as are associated with rapid decomposition under conditions of poor aeration. Most seem tolerant of acid pH, being common in sphagnum and forest litter with a pH below 5.0 and sometimes below 4.0. However from the few observations that have been made there is a suggestion that mull forest soils, such as those under puriri, may have a different copepod fauna to mor forest soils, such as those under beech, and this may imply physiological and ecological distinctions at the species or genus level. Little is known of the rate of reproduction or of any page 63 nutritional peculiarities in the larger plankton. Amongst the small oligochetes remarkable powers of regeneration have been demonstrated (Stout, 1958). Powers of food selection and even range of movement within a soil or a forest litter are at present little known. Clearly, however, their physiological properties are of the greatest interest for it is these associated with their simple morphology that have favoured exploitation of the third great reservoir of aquatic life.
It is this aspect, the successful colonisation of ‘dry land’ that has aroused speculative interest in the soil fauna generally (Ghilarov, 1956). How have animals evolved from strictly aquatic to strictly non-aquatic organisms? The fauna of the terrestrial environment, part rock, part water, part air, offers the most suggestive evidence on this problem. Three evolutionary pathways have been suggested. One, proposed by Hurley (1959) as the evolutionary pathway of terrestrial amphipods, suggests that a supralittoral fauna penetrated directly into the forest floor. A second possibility is the slow evolutionary adaptation of a fresh water pond fauna to increasing periods of desiccation until finally a true soil fauna enjoying brief periods of aquatic life is attained. The Tubificidate have been suggested as an example of this process. A third possibility is the evolution of a fauna originating in fresh water streams, extending through moist mossy banks and sphagnum bogs to the forest floor and so to mineral soil. This seems in the majority of cases to be the most convincing explanation. Thus with the naidid worms the closest relatives of one of the New Zealand species were recorded from shallow streams and adjoining moss carpets. The copepods and ostracods tend to occur in sphagnum as well as in forest litter (Harding, 1953, 1955), and this seems also the most convincing pattern of protozoan evolution. On the other hand the evolutionary trend is not solely towards greater emancipation from a permanently aquatic environment. The reverse trend is also evident. The occurrence of earthworms and pulmonate gastropods in fresh water lakes, and perhaps more dramatically the suggested evolution of hydracarines from terrestrial mites are cases in point.
The mobility of the fauna varies greatly. Some, such as protozoa, although very strictly aquatic are able to exploit the smallest and most transitory pockets of moisture; others, such as enchytraeids and ostracods, although requiring a high relative humidity, are able to move freely within such an atmosphere. These latter have close affinities both taxonomically and ecologically with earthworms and terrestrial amphipods and isopods. Their respiration is dependent upon relatively large moist exposed surfaces and they lack the cuticular waxes which are of such great value to the insects in their emancipation from water to air (Beament, 1961). Consequently they are susceptible to excessive transpiration losses. Such animals are always happier in a wholly aquatic medium than page 64 in an atmosphere of low relative humidity. Their ability to move freely in forest litter is conditioned by the high humidities which prevail in this environment. This is readily illustrated by the most common method of extraction — the Berlese funnel. Copepods, ostracods, and amphipods may all be extracted from forest litter by this means but as the litter dries out many will perish before they can escape. Such powers of movement enable these organisms to retire in dry weathers to deeper layers of the soil profile. They have acquired therefore a certain measure of independence from the currents of precipitation, drainage, and evaporation. To this degree they are no longer planktonic animasl. But it remains a matter of degree and their affinities are still more with the copepods and naidid worms than with the mites, arachnids and insects which differ so greatly physiologically and in their mode of life.
Still the best and most readily accessible account of the forest fauna is that of Birch and Clark (1953). A more recent work is the new English translation by Norman Walker of Kuhnelt's Soil Biology (Faber). A number of papers have been published in recent years on the microfauna of New Zealand soils and these are also listed below.
Beament, J. W. L., (1961). The role of physiology in adaptation and competition between animals. Symposia Soc. Exp. Biol. XV: 62-71.
Birch, L. C., and D. P. Clark (1953). Forest soil as an ecological community with special reference to the fauna. Quart. Rev. Biol. 28: 13-36.
Chapman, Ann (1960). Terrestrial Ostracoda of New Zealand. Nature, Land. 185 (4706) : 121.
Chapman, Ann (1961). The terrestrial ostracod of New Zealand, Mesocypris audax sp. nov. Crustaceana 2(4): 255-261.
Clark, W. C. (1960-61). The Mononchidae (Enoplida, Nematoda) of New Zealand. I-IV. Nematologica 5 (1960) : 199-214; 260-274; 275-284; Nematologica 6 (1961) : 1-6.
Engelmann, M. D., 1961. The role of soil arthropods in the energetics of an old field community. Ecol. Monogr. 31 (3); 221-238.
Flint, E. A., and Stout, J. D., (1960). Microbiology of some soils from Antarctica. Nature 188 (4752) : 767-768.
Ghilarov, M. S., (1956). Soil as the environment of the invertebrate transition from the aquatic to the terrestrial life — Sixth Intern. Congr. Soil Sci., Paris, 1956, Commission III. 51. pp. 307-313.
Harding, J. P., (1953). The first known example of a terrestrial ostracod, Mesocypris terrestris sp. nov. Ann. Natal Mus. 12, 359-365.
Harding, J. P., (1955). The evolution of terrestrial habits in an ostracod. Bull. VII, Symposium on Organic Evolution, National Institute of Sciences of India, New Delhi, pp. 104-106.
Harding, J. P., (1958). Bryocamptus stouti and Goniocyclops sylvestris, two new species of copepod crustacean from forest in New Zealand. Ann Mag. Nat. Hist. 13 (1), 309-314.
Hurley, D. E., (1959). Notes on the ecology and environmental adaptations of the terrestrial amphipoda. Pacific Science XIII (2): 107-109.
Hutchinson, G. E. (1957). A Treatise on Limnology. Vol I. Geography, Physics, and Chemistry. New York. John Wiley and Sons, Inc., 1015 pp.
Hutner, S. H. L., Provasoli, J. J. A. McLaughlin and I. J. Pinter (1956), Biochemical geography: some aspects of recent vitamin research. The Geographical Review 46 (3): 404-407.
Nef, L. (1957). Etat actuel des connaissances sur le role des animaux dans la decomposition des litieres de forets. Extrait de Agriculture, Vol. 5, ser. 3: 245-316.
Stout, J. D., (1956 and 1958). Aquatic oligochaetes occurring in forest litter. I and II. Trans. Roy. Soc. N.Z. 84: 97-102; 85; 289-299.
Stout, J. D., (1961). Biological and chemical changes following scrub burning on a New Zealand hill soil. 3. Microbiological changes. N.Z. J. Sci 4(4): 740-752.
Wigglesworth, V. B., (1942). The Principles of Insect Physiology. Methuen & Co., London, 434 pp.