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AMER. ZOOL., 13:171-176 (1973).
Population Dynamics of Soil and Vegetation Protozoa
STUART S. BAMFORTH
Newcomb College of Tulane University, New Orleans, Louisiana 70118
SYNOPSIS. Many fresh-water protozoa can be found in litters and soils, but the ubiquitous species are those which are able to cope with fluctuating .moisture conditions.
Terrestrial protozoa are more characteristic of bryophyte-soil habitats than aquatic
ecosystems. Nutritionally, two groups have evolved in response to the plant community: naked, predominantly bacterial feeders, whose abundance is determined by the
decomposability of the litter in which they live; and the slow growing, humusassociated testacea, which are more abundant in the litters of slow decomposability.
Ubiquitous species comprise about 90% of the protozoa in soils. More continuous
moisture conditions enhance the appearance of additional species. Hence species diversity indicates higher moisture content of a soil. Protozoa may contribute to the
functioning of the soil ecosystem by inducing fiocculation of bacterial populations and
recycling of minerals through ingestion of bacteria and excretion of soluble products.
The surface of vegetation appears to represent the most terrestrial habitat a protozoan
can exploit, 'because in contrast to the litter-soil ecosystem, only one species, Colpoda
cucullus, dominates the population.
Protozoa are the third most abundant,
but the least understood, group of organisms in the soil. This paper seeks to elucidate their possible role in soils by tracing
their population dynamics, and is based
largely on personal studies of several terrestrial biomes. Previously published work
from this laboratory and the contributions
and ideas of other authors are cited.
METHODS OF STUDY
Ecological studies of terrestrial protozoa
are hard to carry out because of the small
size of the organisms and their dispersed
distribution, thus precluding the respiration, biomass, and turnover rate measurements usually performed when dealing
with more complex animals. Instead, microscopic methods, including dilution
counts and identification of the species
from cultures, are combined with bacteriological studies, chemical determinations of
the soil, data on climate, determination of
the kinds of vegetation, and determination
of the activities of larger animals. The resulting data are then analyzed and interpreted in terms of modern ecological theory
to provide a conceptual framework for unThe preparation of this paper was aided by a
grant from the Tulane University Council on Research.
171
derstanding the role of protozoa in terrestrial habitats.
Quantitative counts describe the "standing crop," but may not always portray the
working of the ecosystem. For example,
the number of ciliates is not always directly
related to the number of bacteria. However, general correlations have been found,
and by comparing the data of several
biomes, insights have been gained into the
dynamics of terrestrial protozoa.
CONDITIONS OF SOIL LIFE
The small size of microorganisms makes
them more sensitive to external factors
than are metazoa. However, their tiny dimensions and short generation time allow
them to evolve quickly to exploit restricted spaces, and their ecology reflects
environmental influences, uncomplicated
by the endogenous factors characteristic of
higher organisms, such as stage in life cycle,
sex ratio, and mating behavior.
Unicellular organisms are aquatic,
hence their presence and activity in terrestrial ecosystems depend upon their
ability to cope with fluctuating moisture
conditions. Successful species must possess
a wide tolerance to fluctuations in humidity and temperature, as well as to the extremes of both; the latter can rise to over
172
STUART S. BAMFORTH
40 C in the upper layers of soils or the
surfaces of leaves at mid-day. These tolerances are achieved through the possession
of a resistant cyst membrane and the ability to pass quickly between active and
latent metabolism. Soil bacteria possess an
additional physiological adaptation for
survival in such habitats; they attain a
higher level of metabolic activity during
the initial growth stages in rewetted soils
compared with that of bacteria maintained
in moist soils. The higher level of metabolism presumably provides the energy
necessary for cell duplication. The most
ubiquitous terrestrial protozoa, Bodo,
Oikomonas, and Colpoda, possess rapid excysting mechanisms to enable them to exploit their bacterial food. Terrestrial protozoa are fresh-water species that invaded
land with varying degrees of success, probably via the moss-sphagnum ecosystem of
stream banks into forest litters, and thence
into soils and onto surface vegetation
(Schonborn, 1964; Stout, 1963).
From a microbial viewpoint, terrestrial
ecosystems are of two kinds: the interstitial
system of litters and soils, and that on the
exposed surfaces of terrestrial vegetation.
The interstitial system will be discussed
first, since vegetation is a special system
that only a few species have successfully
invaded.
flagellates and amoebae have adapted so
well to the interstitial milieu that several
edaphic species have evolved. Among ciliates, the genus Colpoda has exploited the
terrestrial environment most successfully
and furnishes 50-95% of the ciliates in litters and soils. Testacea have adjusted structurally to the soil milieu through the evolution of globose shells, slit-like apertures,
and inner diaphragms in terricolous forms.
The edaphic adaptations of flagellates
and amoebae, together with their small
size and difficulty in identification, render
them less useful in quantitative studies
than ciliates which encompass a wide range
of aquatic to edaphic species. Thus, ciliates
can serve as indicators of the microphagous
group, and their comparison with the nutritionally different testacea (which also
exhibit a range of aquatic to edaphic
forms) furnishes information about the dynamics of terrestrial protozoa.
In litters of easily decomposable leaves,
typical of tropical and deciduous forests
and grasslands, the ratio of testacea to
ciliates is often less than 1:1, and ciliates
may number over 5,000/g (wet weight) of
material. In mixed forests, where litters
also contain some less easily decomposable
leaves, such as those of Fagaceae and conifers, the testacea:ciliate ratio increases up
to 10:1, and ciliates vary from 1,0002,000/g. In coniferous litters and bryophyte
vegetation, the testacea:ciliate ratio exTHE LITTER-SOIL ECOSYSTEM
ceeds 10:1, and ciliates number only a few
In litters and soils, water occurs in films 100/g, whereas testacea may reach 70,000/g
around particles and is thus discontinuous (Bamforth, 1971a). In arid habitats, cilmuch of the time, except after a rainfall. iates are more prominent (up to 3,000/g),
Organic nutrients are more concentrated reflecting their ability to respond quickly
(than in fresh waters), and are derived to brief periods of moisture, but again,
from decomposing litter (and animals to a the testacea, though reduced in numbers,
lesser extent) and plant leachates. The are more prominent in coniferous than
atmosphere of the pore spaces imparts angiosperm litters.
high concentrations of carbon dioxide into
The soil populations of both testacea
the water films.
and ciliates are considerably smaller than
Nutritionally, terrestrial protozoa may those in the overlying litters, but the probe divided into two groups, the naked, fast- portions of the two protozoan groups corgrowing, predominantly microphagous bac- respond to those in the overlying vegetateria-feeders (flagellates, amoebae, and tion. This influence of vegetation on prociliates), and the slow-growing testacea, tozoan populations is shown graphically
which are dependent upon humus and in Figure 1.
similar materials (Stout, 1965). Small
The distribution of these protozoans is
173
DYNAMICS OF SOIL-VEGETATION PROTOZOA
E
0)
a.
Easily
<t>
•o
c
D e c o m p o s a bl e
CO
0)
3-
O
Vegetation
x:
»i
(0
o
Evap.>
P r e c i p.
Mixed
Vegetation
Bryophytes
Evap.<
Precip.
and
Conifers
10
20
Testacea-
Thousands
30
per
40
gram
FIG. 1. The relationship o£ the number of ciliates
and testacea in litters to the type of vegetation.
Region to the left of the broken line denotes arid
habitats.
also related to the carbon:nitrogen ratio
of the litter and soil (due to the plant material in them). Bacterial protoplasm has
a C:N ratio of about 10:1, compared to the
range of 20:1-35:1 for more easily decomposable litters, and the ratios exceed 35:1
for Fagaceae and conifer litters. The latter
types of leaves are rich in compounds such
as celluloses and lignins which are more
resistant to decay. As a result, the conversion of litter material into microbial protoplasm is slower, and microbial populations and activity are inversely proportional to the C:N ratio of litters.
The greater bacterial and protozoan
populations of forest litters are aided primarily by more stable moisture conditions
provided by the tree canopy, drippings of
plant leachates (as additional energy
sources), and mechanical breakdown of litter by invertebrates. Temperature plays a
secondary role by restricting the availability of moisture in warm regions through
excessive evaporation (drought), and in
cold regions by making moisture unavailable through freezing
(physiological
drought) (Bamforth, 1972).
Stability in a terrestrial system depends
upon a continuity of moisture, and is reflected in the species diversity of organisms,
that is, more species of protozoa occur in
damper regions. Although the genus Colpoda comprises most of the ciliates in terrestrial habitats, about a dozen other species are frequent: Chaenia sp., Enchelys sp.,
Keronopsis sp., Pleurotricha sp., Oxytricha
minor, Leptopharynx sphagnetorum, Vorticella microstoma, Cyrtolophosis mucicola,
Cyclidium glaucoma, Chilodonella cucullus, and C. uncinata. These last five, together with Colpoda cucullus and C. steini,
are ubiquitous in swamps and mosses and
possess higher temperature (and often carbon dioxide) tolerances than any of the
other species of limnetic ciliates among 72
studied by Bick and Kunze (1971). This
observation emphasizes some of the adaptations necessary for edaphic life. Several
of these dozen species can be expected in
any litter or soil. Additional species must
be more aquatic, hence ciliate species diversity not only reflects the amount of
moisture in the habitat, but also indicates
a more stable situation, that is, water flue-
174
STUART S. BAMFORTH
tuations will be less extreme. An increase
in ciliate diversity often results in the inclusion of one or two predaceous forms
such as Litonotus, Dileptus, Bursaridium,
Breslaua, and Sphaerophyra, and is usually
accompanied by the appearance of other
aquatic microphages such as colorless
euglenoids and heliozoa.
Testacea likewise show greater diversity
in moist litters and soils with the appearance of bryophyte and aquatic "Aufwuchs"
spine-bearing Euglypha species and flattened forms such as Arcella discoides and
Microchlamys patella.
Increase in species diversity accompanies
increasing stability of the ecosystem and
its division into smaller habitats or niches.
Litters and soils contain many microhabitats within their own communities. For
example, the upper more exposed litter
layers contain fewer numbers and species
of ciliates than moister lower layers. Species
diversity usually accompanies, but does not
always correlate with, increased numbers
of microphagous protozoa. The moist
leaves of mosses, which decompose slowly,
often contain as many or more species of
microphagous, as well as testate, protozoa
than the more rapidly decomposing litters
of adjacent angiosperms, which contain
greater numbers.
SURFACES OF VEGETATION
The ecosystem of the surface of vegetation (leaves, stems) presents more of a challenge to microorganisms because the moisture film, deposited by rain, dew, mist, or
fog, is easily removed, and temperature
extremes are greater than in the interstitial
milieu of litters and soils. The atmosphere,
however, is more favorable in containing
less carbon dioxide. The mere wetting of
leaves leaches nutrients from the plant surface (despite a waxy cuticle) and these are
exploited by a varied microflora.
One protozoan, Colpoda cucullus, has
successfully invaded this extreme habitat
and may be considered a vegetation species
(Mueller and Mueller, 1970). It is able
to excyst and encyst rapidly, feed upon the
bacteria in moisture drops on leaves, and
reproduce in the encysted state. This species comprises over 70% of the protozoan
population on living leaves and can be
found in concentrations as high as 800 individuals/g. Colpoda steini and occasionally a few other ubiquitous soil ciliates such
as Chilodonella curullus and Vorticclla
microstoma may be present in low numbers (Bamforth, 1971ft).
When leaves die, protozoan populations
increase to several thousand per gram. Colpoda steini becomes more prominent, and
small flagellates invade (Fig. 2). Thus, the
senescent leaf may be considered an ecotone between the living phyllosphere and
the ground litter.
ROLE OF TERRESTRIAL PROTOZOA
All naturally occurring organisms in an
ecosystem contribute to the utilization of
energy and recycling of minerals by the
system, and their biologies fit them into
their particular niches. The presence of
large numbers of microphagous protozoa
in the soil encouraged several studies of
predator-prey relationships, but several
decades of investigation have failed to
show that protozoa exercise a controlling
influence on the number and diversity of
bacteria. In fact, some studies have suggested protozoa benefit rather than control the bacterial population (Hutchinson,
1914).
One explanation has been offered by
Viswanath and Pillai (1968) as a result
of their studies on activated sludge and
sewage purification processes, which may
be compared functionally to processes in
the soil. They have experimentally shown
that microphagous protozoa, especially
peritrichs, are largely responsible for the
formation of the bacterial floes which are
necessary for the efficient degradation of
organic matter. With the exception of Vorticella microstoma, peritrichs are not common in natural soils, and their ecological
equivalent may be found in bdelloid rotifers (e.g., Philodina), which are more motile, capable of more powerful ciliary currents, and very resistant to desiccation.
Since the majority of soil macrophages
DYNAMICS OF SOIL-VEGETATION PROTOZOA
175
Living
Leaves
Dead
L i t t e r
Leaves
0 oooo \\\
Colpoda
C. steini
cucu 11 us
Bodo
FIG. 2. Protozoan succession on leaves. The difference between the two kinds of leaf populations
may be scon even on a partly senescent leaf: the
living proximal portion containing principally Colpoda cuculhis, the dead distal portion supporting a
more diverse protozoan community.
are small flagellates and Colpoda, flocculation activity would have to depend on
these protozoa. Viswanath and Pillai (1968)
have described flocculation activity of Colpoda spp. in experiments where bits of bacteria-laden debris collect on the ciliates.
Hardin (1943) had previously found that
floes formed in pure cultures of several
kinds of bacteria only when the flagellate
Oikomonas termo was introduced. Hence,
the dominant soil protozoa are capable of
flocculation activity and might function on
a microbial level in the same capacity as
earthworms and soil arthropods on the
metazoan level, to aid bacterial decomposition through mechanical activity.
An additional function of protozoa in
soil is suggested by studies on recycling of
minerals in aquatic ecosystems, where most
of the elements are contained in the bodies
of algae (Pomeroy, 1970). Bacteria accumulate elements through decomposing
activities and recycle elements only
through autolysis or as a result of being
ingested by protozoa, small detritus eaters,
and coprophagous forms. The digestive
products of these particulate feeders include compounds in soluble form which
can be readily absorbed by the algal community. Thus, protozoa and their metazoan analogues serve to recycle elements.
Litters and soils constitute a modified
176
STUART S. BAMFORTH
aquatic ecosystem in which most of the
elements are contained in the biomass of
higher plants. Recycling consists of litter
formation from the plants, conversion into bacterial protoplasm, and perhaps
transformation through protozoan and
meiofaunal metabolism into soluble products than can be absorbed by plant root
systems.
The operation of the litter-soil ecosystem can be better understood through comparison with infusion succession. When
organic matter decays, the developing bacterial population depletes oxygen and produces large amounts of carbon dioxide,
thereby providing an environment favorable to invasion by soil protozoa, that is,
small flagellates and Colpoda. These protozoa enhance populations (which increase
in numbers) and prepare the ecosystem for
hymenostomes and hypotrichs which in
turn reduce the bacterial populations for
the succeeding peritrichs. Such succession
appears spatially in a stream receiving
sewage. The soil ecosystem can be considered the first stage in this succession,
which is maintained due to the continual
input of organic matter by the litter, despite interruptions by drought. As material
in the litter migrates from the upper to
lower layers it becomes more degraded,
and the protozoan population diversifies
to include the more complex ciliates of
the second stage of succession (Bamforth,
1970). The protozoa could enhance bacterial functioning by flocculation and mineral recycling through bacterial feeding
and excretion of soluble products, which
are then removed from the soil by the
roots of plants.
Schonborn's (1965) nutritional studies
suggest that many testacea can subsist on
highly resistant plant materials such as
lignin. Thus, they might contribute to
mineral recycling in a manner similar to
microphagous protozoa. Their slow metabolism is integrated into the slow rate
of decomposition characteristic of evergreen vegetations of temperate to cold
climates, to maintain a continuous recycling of nutrients.
REFERENCES
Bamforth, S. S. 1970. Distribution of ciliates in
deciduous litters. J. Protozool. 17 (Suppl.) :15.
Bamforth, S. S. 1971a. The numbers and proportions of testacea and ciliates in litters and soils.
J. Protozool. 18:24-28.
Bamforth, S. S. 19716. Population dynamics of leafinhabiting protozoa. J. Protozool. 18 (Suppl.):
75.
Bamforth, S. S. 1972. Protozoa from an alpine
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