THE INVERTEBRATE FAUNA OF THE SOIL (OTHER THAN PROTOZOA).
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.)
+------------------------------+---------------+-------------+
| |Unmanured Plot.|Manured Plot.|
+------------------------------+---------------+-------------+
|Insects | 2,474,700 | 7,727,300 |
+------------------------------+---------------+-------------+
|Larger Nematoda and Oligochæta| | |
| Limicolæ | 794,600 | 3,600,400 |
+------------------------------+---------------+-------------+
|Myriapoda-- | | |
| Diplopoda | 596,000 | 1,367,000 |
| Chilopoda | 215,400 | 208,700 |
| Symphyla | 64,000 | 215,500 |
| +---------------+-------------+
| Total | 875,400 | 1,791,200 |
+------------------------------+---------------+-------------+
|Oligochæta (Terricolæ) | 457,900 | 1,010,100 |
+------------------------------+---------------+-------------+
|Arachnida-- | | |
| Acarina | 215,400 | 531,900 |
| Areinida | 20,200 | 20,200 |
| +---------------+-------------+
| Total | 235,600 | 552,100 |
+------------------------------+---------------+-------------+
|Crustacea (Isopoda) | 33,700 | 80,800 |
+------------------------------+---------------+-------------+
|Mollusca (Pulmonata) | 13,500 | 33,700 |
+------------------------------+---------------+-------------+
| Total Invertebrata | 4,885,400 | 14,795,600 |
+------------------------------+---------------+-------------+
[Illustration: FIG. 20.--Distribution in depth of the more important
groups of soil invertebrates in the manured and unmanured (or control)
plots at Rothamsted. (From Morris, “Annals of Applied Biology,” vol.
ix., nos. 3 and 4, Cambridge University Press.)]
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.
[Illustration:
1, _Collembola_; 2, _Thysanura_; 3, _Orthoptera_; 4, _Thysanoptera_;
5, _Hemiptera_; 6, _Lepidoptera_; 7, _Coleoptera_; 8, _Diptera_; 9,
_Hymenoptera_.
FIG. 21.--Number of individuals in the different orders of insects in
manured and unmanured arable land at Rothamsted. (From Morris, “Annals
of Applied Biology,” vol. ix., nos. 3 and 4, Cambridge University
Press.)]
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).
[Illustration:
1, _Collembola_; 2, _Thysanura_; 3, _Orthoptera_; 4, _Thysanoptera_;
5, _Hemiptera_; 6, _Lepidoptera_; 7, _Coleoptera_; 8, _Diptera_; 9,
_Hymenoptera_; 10, _Diplopoda_; 11, _Chilopoda_; 12, _Areinida_; 13,
_Acarina_.
FIG. 22.--Number of species of different orders of invertebrates
present in the manured and unmanured (or control) plots at Rothamsted.
(From Morris, “Annals of Applied Biology,” vol. ix., nos. 3 and 4,
Cambridge University Press.)]
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.
+---------+-------------+-------------+------------+--------------+
| |Phytophagous.|Saprophagous.|Carnivorous.|Heterophagous.|
+---------+-------------+-------------+------------+--------------+
|Unmanured| | | | |
|plot | 14 | 48 | 13 | 20 |
|Manured | | | | |
|plot | 13 | 58 | 9 | 20 |
+---------+-------------+-------------+------------+--------------+
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.
[Illustration: FIG. 23.--Diagram showing the Relation of the Soil
Invertebrata (other than Protozoa) to the Nitrogen Cycle.]
(_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.
ADAMS, C. C., “An Ecological Study of Prairie and Forest
Invertebrates,” Bull. Illin. St. Lab. Nat. Hist., 1915, xi.
CAMERON, A. E., “General Survey of the Insect Fauna of the Soil,”
Journ. Econ. Biol., 1913, viii. “Insect Association of a Local
Environmental Complex in the District of Holmes Chapel, Cheshire,”
Trans. Roy. Soc. Edin., 1917, lii.
DARWIN, C., “Vegetable Mould and Earthworms,” London, 1881.
HAMILTON, C. C., “The Behaviour of some Soil Insects in Gradients of
Evaporating Power of Air, etc.,” Biol. Bull., 1917, xxxii.
MORRIS, H. M., “Observations on the Insect Fauna of Permanent Pasture
in Cheshire,” Ann. App. Biol., 1921, vii. “On a Method of Separating
Insects and other Arthropods from Soil,” Bull. Entom. Res., 1922,
xiii. “The Insect and Other Invertebrate Fauna of Arable Land at
Rothamsted,” Ann. App. Biol., 1922 A, ix.
REH, L., In Sorauer’s “Pflanzenkrankheiten,” 1913, iii.
RICHARDSON, C. H., “The Attraction of Diptera to Ammonia,” Ann. Ent.
Soc. Amer., 1916, ix.
RUSSELL, E. J., “The Effect of Earthworms on Soil Productiveness,”
Journ. Agric. Sci., 1910, iii.
SHELFORD, V. E., “Animal Communities in Temperate America,” Chicago.
1914, “The Importance of the Measure of Evaporation in Economic
Studies of Insects,” Journ. Econ. Entom., 1912, vii.