The micro-organisms of the soil have been fully discussed in the preceding chapters of this volume. There now remains to be considered the fauna of invertebrate animals, other than protozoa, which inhabit that same medium. In the first place, it is necessary to define what groups of invertebrate animals are to be regarded as coming under the category of soil organisms. The latter expression has rather a wide application and, for the present purpose, is held to mean any organism of its kind which, in some stage or stages of its life-cycle, lives on or below the surface of the soil. It will be obvious that, with so comprehensive a definition, the intimacy of the association of these animals with the soil will vary within very wide limits. Some animals pass their whole life-cycle in the soil; others are only present during a limited phase, and not necessarily in a trophic condition, but since their occurrence is constant, they cannot be entirely omitted from consideration.

Unlike the groups of organisms which have been dealt with in the foregoing pages, the invertebrates of the soil do not admit, as a rule, of investigation in culture media. It is, in consequence, much more difficult to achieve in the laboratory the same control over their environmental conditions. This fact in itself largely explains why the interpretations of field observations in animal ecology have not usually been subjected to the test of laboratory experimentation. The study of animal ecology, in so far as the denizens of the soil are concerned, is of very recent birth. It has not, as yet, passed the preliminary stage of cataloguing empirical data, and much spade work will be necessary before the various factors controlling the phenomena actually observed are understood.

Owing to the paucity of information available, this chapter is essentially based upon observations conducted at Rothamsted. Its object is not so much to attempt to evaluate the invertebrate fauna of the soil, as to suggest a line of ecological work demanding investigation on land of many different types.

Method of Investigating the Soil Fauna.

The method adopted at Rothamsted consists in taking weekly soil samples from a given area for a period of twelve months. Each sample is a cube of soil, with a side dimension of nine inches, and a total content of 729 cubic inches. The samples are taken by means of an apparatus consisting of four iron plates, which are driven into the ground down to the required depth so as to form a kind of box, which encloses a cube of soil (vide Morris, 1922 A). The latter is then removed in layers, each layer being transferred to a separate bag for the purpose. When the complete sample has been extracted, there are five bags containing layers of soil taken from the surface to a depth of 1″, from 1″ to 3″, from 3″ to 5″, from 5″ to 7″, and 7″ to 9″ respectively. Below a depth of 9″ no samples have been taken.

The sample obtained in this manner may be gradually worked into small fragments by hand, and examined whenever necessary under a binocular microscope for the smaller organisms present. This procedure, however, is very tedious and has been replaced by the use of an apparatus consisting of a series of three sieves, with meshes of decreasing size (vide Morris, 1922). The soil is washed through these sieves by means of a stream of water, and the meshes of the final strainer are small enough to retain all except the most minute organisms present, while at the same time they allow the finest soil particles to be carried away. When desirable, the effluent can be passed through a bag or sieve of bolting silk, in order to collect such organisms that may have passed through the third sieve.

In addition to the actual taking and examination of the samples, a botanical survey of the area under investigation is made; chemical and mechanical analyses of the soil are also required. It is further necessary to take soil temperature readings, to determine the moisture content of the samples taken, and the amount of organic matter which they contain.

Groups of Invertebrata Represented in the Soil.

The various groups of invertebrates represented in the soil may be briefly referred to in zoological order.

Nematoda.—The Nematoda or thread-worms are chiefly animal parasites, nevertheless they usually lead an independent existence in the soil in certain stages of their development. The numerous small species belonging to the family Anguillididæ, or eel-worms, form a definite constituent of the soil fauna; they are generally free-living and non-parasitic. Certain members of this family, however, are enemies of cultivated plants.

Annelida.—Terrestrial Annelida are almost entirely confined to the order Oligochæta, the majority of which are earthworms (Terricolæ), whose whole life-cycle is passed within the confines of the soil. The small white worms of the family Enchytræidæ belong to the aquatic section (Limicolæ) of the order, but they have various representatives which are abundant in damp soil containing organic matter.

Mollusca.—The terrestrial Mollusca are included in the sub-order Pulmonata of the Gastropoda. These organisms, which include the snails (Helicidæ) and slugs (Limacidæ), regularly deposit their eggs in moist earth. Slugs adopt the soil as a frequent habitat, only leaving it for feeding purposes in the presence of sufficient moisture. They are frequent consumers of vegetation, with the exception of Testacella, which is carnivorous.

Crustacea.—The few species of Crustacea inhabiting the soil belong to the order Isopoda, family Oniscidæ, which are popularly referred to as “woodlice,” “slaters,” etc.

Myriapoda.—The Diplopoda or millipedes include enemies of various crops and are common denizens of the soil. The Chilopoda or centipedes are usually less abundant and are carnivorous. The minute Symphyla are often evident but are of minor importance.

Insecta.—Insects form the dominant element in the invertebrate fauna. Phytophagous species devour the subterranean parts of plants, and notable examples are afforded by the larvæ of Melolontha, Agriotes and Tipula. Saprophagous forms are abundantly represented by the Collembola, and by numerous larval Diptera and Coleoptera. Predaceous species preying upon other members of the soil fauna are exemplified by the Carabidæ and many larval Diptera. Parasitic species pass their larval stages on or within the bodies of other organisms. The groups of Hymenoptera, and the dipterous family Tachinidæ, which exhibit this habit, constitute, along with predaceous forms, one of the most important natural agencies controlling the multiplication of insect life. There are also insects (ants, and other of the aculeate Hymenoptera) which utilize the soil as a suitable medium wherein to construct their habitations or brood chambers, without necessarily deriving their food from the soil. Lastly, there are many insects, notably Lepidoptera, which only resort to the soil for the purpose of undergoing pupation. The insect fauna is, therefore, a closely inter-connected biological complex; for a discussion and an enumeration of its representatives reference may be made to papers by Cameron (1913, 1917), and Morris (1921, 1922 a).

Arachnida.—The two principal classes represented in the soil are the Areinida, or spiders, and the Acarina, or mites, and ticks. The Areinida, which are well-known to be carnivorous, are an unimportant constituent of the fauna. Acarina, on the other hand, are abundant, and exhibit a wide range of feeding habits; most of the soil forms are probably carnivorous, and either free-living or parasitic.

Number of Organisms Present and their Distribution in Depth.

In computing the number of invertebrates normally present in a given type of soil, the method adopted consists of making individual counts of all such organisms as occur in each sample of a series taken over a period of twelve months. This method considerably reduces errors due to season and to the possible deviation of one or more samples from the average. If the total number of these organisms is known for the samples taken, it becomes a simple procedure to arrive at their approximate numbers per acre.

TABLE XIV.
(Based on Morris, 1922 A.)

Table XIV. represents a numerical estimate of the invertebrate fauna of two plots of arable land at Rothamsted. The soil is clay with flints overlying chalk, and the land in question has been devoted for eighty years to continuous cropping with wheat; one plot (No. 3) receives an annual dressing of farmyard manure at the rate of 14 tons per acre, and the other plot (No. 2) receives no natural or artificial fertilizer. The significant feature in a comparison of the fauna of the two plots is the great numerical increase in organisms due to the addition of manure. From the point of view of distribution in depth, Fig. 20 clearly demonstrates that the bulk of the fauna is concentrated in the first three inches of the soil. With the exception of the Acarina it is evident that the limits of vertical distribution extend below the depth of nine inches investigated, although the numbers of organisms likely to be present are inconsiderable. The Oligochæta, or true earthworms, occur in Rothamsted soil in numbers very much in excess of the figures given by Darwin, who quoted observations by Hensen. The latter authority calculated that there were 53,767 earthworms in an acre of garden soil, and estimated that about half that number would be present in an acre of corn field. In the Rothamsted investigations their numbers exceeded Hensen’s estimate over 16 times in unmanured land, and over 36 times in manured land.

In an area of pasture-land in Cheshire few insects occurred below a depth of 2 inches, and they reached the limit of their vertical distribution at or near 6 inches. Their number (3,586,000 per acre) is considerably in excess of that present in unmanured arable land at Rothamsted.

Dominance of Certain Species and Groups.

In Fig. 21 a numerical analysis is given of the different orders of insects represented in Rothamsted soil. The ascendency of the Hymenoptera and Collembola is almost entirely due to the occurrence of three species in large numbers, viz., the ant Myrmica lævinodis and the Collembola, Onychiurus ambulans and O. fimetarius. In the unmanured plot these two Collembola constituted 13 per cent. of the insects and the species of ant accounted for nearly 28 per cent. In the manured plot they amounted respectively to 27 per cent. and 36 per cent. of the insects present. Next in order of numerical ascendency are larval Diptera, mainly belonging to the families Cecidomyidæ, Chironomidæ, and Mycetophilidæ. The Diptera are followed by the Coleoptera, whose most abundant representatives are larval Elateridæ (wireworms).

In point of view of number of species present (Fig. 22), Coleoptera take the front rank; in the unmanured plot they are very closely approached by Collembola and Diptera.

Passing from the insects, the next assemblage of organisms in point of number of individuals are the smaller worms. The difficulties attending the specific identification of these organisms are great, and, in the present survey, the Nematodes and all the smaller Oligochætes have not been separated.

The abundance of the Myriapoda is mainly due to the prevalence of Diplopoda, which are represented by four species. The Chilopoda almost entirely consist of a single species Geophilus longicornis.

The dominant group of the Arachnida is the Acarine family Gamascidæ, which are represented by about a dozen species.

Classification of Soil Invertebrates According to Feeding Habits.

From the point of view of the fauna as a whole, the zoological classification of the soil invertebrates is only significant when the various groups are analysed according to the feeding habits of their members. All animals are directly or indirectly dependent upon plant life for their nutrition. For the present purpose they are divided into four categories, and the position of each class of animals in the scheme is based upon the habits of its chief representatives in the soil. Definite information on this subject, however, is not always forthcoming, and it is only possible to achieve approximate estimates. In the table above the percentages in number of individuals present in the two plots investigated at Rothamsted are given under each type of feeding habit.

It must be borne in mind that these estimates only apply to average conditions; the outbreak of a plant pest in any one year must naturally materially alter the proportions given. The phytophagous organisms are represented by a certain number of the Insecta together with the pulmonate Mollusca. Carnivorous forms which are mainly beneficial from the agricultural standpoint, include Insecta, together with the Chilopoda, many Acarina and the Areinida. Saprophagous forms constitute the dominant element of the soil fauna. More than 30 per cent. of the Insecta exhibit this habit, which is also the dominant one in the Oligochæta, Symphyla, and in many of the soil Nematodes. Heterophagous species include all those of somewhat plastic habits; for the most part they are saprophagous, but, on the other hand, a considerable proportion of the species attack growing plants or exhibit both habits. Under this category are included a certain number of the Insecta, the Diplopoda, Isopoda, and some Acarina.

The Influence of Environmental Factors upon The Invertebrates of the Soil.

Since animals are endowed with powers of independent locomotion: they are not necessarily tied to their environment to the same extent that plants are. The investigation of the influence of environmental factors sooner or later involves a study of the tropisms of the animals concerned. Until these are adequately understood it is scarcely possible to arrive at any exact conclusions relative to their behaviour in the soil. Insects, for example, respond to the stimuli of various, and often apparently insignificant forces, acting upon their sensory organs. Such responses are known as chemotropism, phototropism, hydrotropism, thermotropism, and so forth according to the nature of the stimuli. Tropisms are automatic and, so far as they distinguish sensations, are independent of any choice, and consequently of psychic phenomena. Animal automatism, however, does not present the rigidity of mechanical automatism. Differential sensibility, vital rhythms, or periodicity, etc., are other important aspects of animal behaviour.

The environmental factors, affecting more especially the insect population of the soil, have been discussed by Cameron (1917) and Hamilton (1917), and certain broader aspects of animal ecology by Adams (1915) and Shelford (1912). These factors are so numerous and so inter-connected, that it is only possible to refer to them briefly in the space available. As might be expected, soils that are of a light and open texture are the ones most frequented by soil insects, nutritional and other factors being equal. Furthermore, it has already been shown that in arable land insects and other animals penetrate to a greater depth than in pastures. This fact is primarily due to the greater looseness of the soil occasioned by agricultural operations, which ensure at the same time better drainage aeration, and greater facilities for penetration. Hamilton found that soil insect larvæ are very sensitive to evaporation, and especially so if the temperature is 20° C. or over. In their natural habitat the relative humidity of the air, in moist or wet soil, is not far below saturation, and the temperature of the soil rarely goes above 20°-23°C., and then only in exposed, dry, hard soil in which these larvæ do not occur.

The significance of the rate of evaporation as an environmental factor was first emphasised by Shelford. According to him the best and more accurate index of the varying physical conditions affecting land animals, wholly or in part exposed to the atmosphere, is the evaporating power of air. By means of a porous cup-atmometer, as devised by Livingston, Shelford has carried out an important series of experiments on the reactions of various animals to atmospheres of different evaporation capacities, and reference should be made to his text-book.

The importance of the organic matter present in the soil is well illustrated in the table on p. 152. The great increase in the number of insects and other animals is partly due to their direct introduction along with the manure, and partly to their entry into the soil in response to chemotropic stimuli exerted by fermentation. Organic matter influences the fauna in other ways also; it increases the moisture content of the soil, and it provides many species with an abundance of food material. Also, the amount of carbon dioxide present in the soil is partly dependent upon decaying organic matter. Hamilton conducted experiments on the behaviour of certain soil insects in relation to varying amounts of carbon dioxide. Although his work is of too limited a nature to be accepted without reserve, it lends support to the conclusions of Adams who says: “The animals which thrive in the soil are likely to be those which tolerate a large amount of carbon dioxide, and are able to use a relatively small amount of oxygen, at least for considerable intervals, as when the soil is wet during prolonged rains. The optimum soil habitat is therefore determined, to a very important degree, by the proper ratio or balance between the amount of available oxygen and the amount of carbon dioxide which can be endured without injury.”

Little is known concerning the occurrence of ammonia in the soil atmosphere, but its presence in minute quantities is probably an important chemotropic factor in relation to saprophagous organisms which are the largest constituent of the fauna. A great increase in Dipterous larvæ occurs on the addition of farmyard manure, and this is noteworthy in the light of Richardson’s experiments (1916), which indicate that ammonia exercises a marked attraction for Diptera, which spend some part of their existence in animal excrement in some form or another.

The nature of the vegetation supported by the soil is of paramount importance in relation to phytophagous organisms, and examples need scarcely be instanced of certain species of soil insects being dependent upon the presence of their specific food plants.

The Relation of Soil Invertebrates to Agriculture.

The relation of these organisms to agriculture may be considered from three points of view: (a) their influence upon the soil itself; (b) their relation to the nitrogen cycle; and (c), their direct influence upon economic plants.

(a) The behaviour of earthworms as a factor inducing soil fertility is discussed by Darwin in his well-known work on the subject, and their action may be briefly summarised as follows. In feeding habits they are very largely saprophagous, and consume decaying vegetable matter including humus, which they swallow, together with large quantities of soil. Earthworms come to the surface to discharge their fæces (“worm casts”), and in this process they are continually bringing up some of the deeper soil to the air. Darwin estimated that earthworms annually brought to the surface of the soil in their “casts” sufficient earth to form a layer ·2 inch in depth, or 10 tons per acre. Their action, along with the atmosphere, are the chief agencies which produce the uniformity and looseness of texture of the surface soil. By means of their burrows earthworms facilitate the penetration of air and water into the soil, while their habit of dragging leaves and other vegetable material into these burrows increases the organic matter present below the surface. These facts are generally agreed upon, but it is a disputed point whether earthworms, by devouring organic matter, aid the conversion of the latter into plant food more rapidly than takes place solely through the activities of micro-organisms.

Soil insects and other arthropods, by their burrowing activities, are also instrumental in loosening the soil texture and thereby facilitating soil aeration and the percolation of water. The action of termites in warmer countries is discussed by Drummond in his “Tropical Africa,” who compares the rôle of subterranean termites to that of earthworms. The great abundance of ants renders them also significant in this same respect, and very few species are direct enemies of the agriculturist.

(b) In their relation to the nitrogen cycle (vide p. 174), the activities of the soil invertebrates may be expressed diagrammatically, as a side-chain in the process (Fig. 23). The proteins, elaborated by plants, are utilised as nitrogenous food by the phytophagous animals present. The waste products of the latter, which contain the nitrogen not used for growth or the replacement of loss by wear and tear, are returned to the soil. Here they disintegrate, and are ultimately converted into ammonium salts, mainly by bacterial action. The dead bodies of these animals are also broken down by various means, becoming eventually chemically dissociated and available as plant food. Animal (and plant) residues serve, however, as food for the large number of saprophagous invertebrates present in the soil. In this event the nitrogen contained in such residues becomes “locked up,” as it were, for the time being in their bodies. Both saprophagous and phytophagous animals are preyed upon by carnivorous species, but ultimately the nitrogen is returned to the soil upon the death of those organisms. The amount present in the bodies of the whole invertebrate fauna has been calculated by Morris (1922) upon analyses furnished by chemists at Rothamsted. It is estimated that the fauna of manured land contains about 7349 grm., or 16·2 lb. of nitrogen per acre, and that of untreated land, 3490 grm., or 7·5 lb. per acre. These amounts are equal respectively to the nitrogen content of 103·6 lb. and 48 lb. of nitrate of soda.

The primary question affecting agriculture is, whether any notable loss of nitrogen is occasioned by the presence of these organisms in the soil. It has been mentioned that their nitrogenous waste material, and their dead bodies, ultimately undergo disintegration; any loss, if any, takes place during the latter process. With the more complex compounds it probably consists in the production of amino-acids and their subsequent hydrolysis or oxidation. During this process an appreciable loss of nitrogen in the gaseous form occurs. This loss, which is discussed on p. 173 would represent the net deficit occasioned by the incidence of invertebrates in the soil. Against this loss must be placed the beneficial action of such organisms as earthworms, which, in all probability, more than counterbalances it.

(c) Many soil insects, on account of their phytophagous habits, are well-known to be some of the most serious enemies of agriculture. Certain of these, and also other classes of invertebrates, which are likewise directly injurious, have been instanced in the earlier pages of this chapter. Detailed information on this subject will be found in textbooks of economic zoology, notably the volume by Reh (1913).

LITERATURE REFERRED TO.