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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 habitat. J. Protozool. 19 (Suppl.):32-33. Bick, H., and S. Kunze. 1971. Eine Zusammenstellung von autokologischen und saprobiologischen Befunden an Siisswasserciliaten. Int. Rev. Gesamten Hydrobiol. 56:337-384. Hardin, G. 1943. Flocculation of bacteria by protozoa. Nature 151:642. Hutchinson, C. M. 1913-1914. Report of the Agricultural Institute and College, Pusa, 81. Mueller, J. A., and W. P. Mueller. 1970. Colpoda cucullus, a terrestrial aquatic. Amer. Midland Natur. 83:1-12. Pomeroy, L. R. 1970. The strategy of mineral cycling. Annu. Rev. Ecol. Syst. 1:171-190. Schonborn, W. 1964. Lebensformtypen und Lebensraumwechsel der Testaceen. Limnologica 2:321335. Schonborn, W. 1965. Untersuchungen iiber die Ernahrung bodenbeuohnder Testaceen. Pcdobiologia 5:205-210. Stout, J. D. 1963. The terrestrial plankton. Tuatara 11:57-64. Stout, J. D. 1965. The relation between protozoan populations and biological activity in soils, p. 119. In Excerpta Med. Int. Cong. Ser. No. 91, 2nd Int. Conf. Protozool., London, July-August 1965, Progress in Protozoology. Viswanath, G. K., and S. C. Pillai. 1968. Occurrence and activity of protozoa in soil. J. Sci. Ind. Res. 27:187-195.