Colonization of decomposing deciduous leaf litter by Testacea (Protozoa, Rhizopoda): Species succession, abundance, and biomass

Oecologia (Berl) (1982) 52:381-388 Oecologia © Springer-Verlag 1982

Colonization of Decomposing Deciduous Leaf Litter by Testacea (Protozoa, Rhizopoda): Species Succession, Abundance, and Biomass

J. Daniel Lousier Department of Biology, University of Calgary, Calgary, Alberta, Canada

Summary. The colonization of leaf litter by testate amoebae in a cool temperate deciduous forest was studied over the first 60 months of decomposition. No colonization of fresh leaf litter by Testacea was recorded before the first spring thaw period. Colonization of aspen and balsam leaves was similar in terms of species and numbers of species, with the balsam litter being colonized by slightly fewer species. In the aspen litter bags, all the L-layer species were present after 18 months, and all the species recorded in all soil layers were found after 60 months. The proportion of species which constructed their tests from platelets rather than sediment was 70% of the total number of species for the first 36 months of colonization of both litter types. After 60 months, seven species comprised 70% of the total numbers of Testacea but only 33-38% of the total biomass. Significant, positive correlation existed between the dry weight loss of leaf litter and the total number of active Testacea, the total number of living Testacea, and the total number of species present. The prime limitations to testacean colonization of decomposing leaf litter appeared to be substrate quality, food supply and/or availability of test-building materials.

1 Introduction

The annual autumn leaf fall in cool temperate deciduous forests provides an opportune means for studying several aspects of the ecology of soil and litter organisms, some of which are population dymanics, community succession, colonization theor- ies, and trophic relationships between organisms. Knowledge of microhabitat development and successional changes in populations and communities of organisms during the decomposition of this annual influx of organic matter is essential for a complete understanding of the functioning of northern deciduous forest soils.

Several studies of decomposing leaves have demonstrated the succession of microflora (Marten and Pohlman 1942; Frank- land 1966; Hogg and Hudson 1966; Saito t966; Minderman and Daniels 1967; Hudson 1968; Parkinson and Balasooriya 1969; Jenson 1971 ; Remacle 1971 ; Visser and Parkinson 1975a, b), and fauna (Crossley and Hoglund 1962; Stevanovic 1968; Anderson 1975; Cancela da Fonseca 1975), but there is little information on soil Protozoa colonizing terrestrial leaf litter. There is also little information on relationships between different

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colonizers and on substrate utilization by the various trophic levels colonizing the litter fall (e.g. Anderson 1975).

While Testacea may be a relatively easy group of Protozoa to study via direct observation techniques (Stout et al. 1982), it has been believed that they may not be the most capable of protozoan colonizers. Testacea do not appear to be well- adapted to the surface litter environment. It has also been felt that they reproduce more slowly (Jennings 1916; Heal 1964; Lousier 1974a, b) and have less perfect encystment and excyst- ment mechanisms (Stout and Heal 1967) than do the flagellates, ciliates and small naked amoebae. Some Testacea require sediment materials for test construction and these materials may be limited in amount in fresh litter. Testacea may thus not be able to cope with the environmental uncertainties in the surface litter layer of northern deciduous forest soils, viz., generally much lower and much more rapidly fluctuating moisture contents, and extremely high temperatures (approaching 40 ° C) during various periods of the year.

The intentions of this paper are to: l) record species succession and biomass of Testacea coloniz-

ing aspen (Populus tremuloides Michx.) and balsam (P. balsami- fera L.) leaf litter over 60 months; and

2) discuss the characteristics and growth of colonizing populations, factors affecting colonizing succes, and colonizing mechanisms of litter and soil Testacea.

2 Site Description

The general study area was located at the northern end of the Kananaskis Valley (115°00'-115°06 ~ W, 51°00~-51°04 ' N) in the Fisher Range of the Rocky Mountains of Alberta, Canada, and encompassed about 21 km 2.

Kirby (1973) has provided a general description of the northern part of the Kananaskis Valley, including descriptions of the climate, physiography, hydrology, geology, soils and forest inventory. Karkansis (1972) surveyed the soils of the entire valley and Lousier (1974a, 1975) described the organic layers of several valley soils, including the aspen woodland soil. The vegetation of the main aspen site has been detailed by Dennis (1970), and various above- and belowground climatic data from the aspen site have been presented in several papers (Dash and Cragg 1972; Lousier 1974a; Lousier and Parkinson 1976, 1978, 1979).

The main study site was at 1,400 In ASL on a well-drained, south-facing slope. The climate is essentially continental, charac- terized by short, dry summers and relatively long, cold winters with intermittent, warm, chinook winds. The soil has been classi- fied in the orthic gray luvisol subgroup and has a surface organic

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Table 1. The changes in active biomass ( × 10-* mg g- 1 dry weight) of species of Testacea colonizing aspen leaf litter

Species Age of litter (months)

5 8 10 12 18 24 36 48 60

Arcella catinus (9.4) a 3.2 4.7 0 9.3 7.4 25.0 Euglypha rotunda (3.5) 1.3 3.8 4.9 26.0 10.0 55.0 E. laevis (3.8) 1.2 1.8 4.5 10.4 21.2 46.6 E. scutigera (7.6) 7.5 I0.0 46.5 E. compressa (24.1) 64.6 71.6 44.3 0 E. compressa forma gtabra (24.1) 30.8 23.9 19.0 7.0 E. cuspidata (I.5) 1.4 0.5 0.8 1.9 4.5 21.3 2.9 E. polylepis (8.8) 8,2 Trinema lineare (2.0) 1.0 2.5 24.3 51.1 168.0 T. enchelys (9.8) 4.9 12.5 38.8 134.2 561.1 Phryganella acropodia (4.2) 2.1 5.4 4.2 10.0 48.9 Difflugiella oviformis (0.05) 0.045 0.017 0.049 0.063 0.15 0.6 0.4 Heleopera petricola (10.7) 31.8 36.6 48.8 Hyalosphenia minuta (0.6) 0.2 H. subflava (6.2) 3.3 6.0 Centropyxis aerophila (10.0) 12.8 39.6 18.4 51.5 C. aerophila var. sphagnicola (12.4) 12.3 13.0 32.5 C. sylvatica (160.0) 54.4 80.0 205.0 317.0 211.0 776.0 C. cassis (12.3) C. plagiostoma (25.1) C. minuta (6.1) C. platystoma (9.4) C. taevigata (16.8) Cyclopyxis eurystoma (12.8) 65.9 C. eurystoma var. gauthieriana (25.I) C. kahli (59.1) C. puteus (157.0) Plagiopyxis callida (25.1)

8.6 10.0 31.0 33.0 30.4 32.0 27.8 23.0 21.9 18.0 11.1 18.0 2.7 2.3

31.1 46.8 62.8 61.0

233.1 140.0 113.4 153.0

1.8 2.l 24.5 16.1

4.4 6.3 28.3 65.0 82.3 91.0 56.7 74.0

366.0 480.0 16.8 27.7 34.4 56.5 2.8 9.2 4.9 8.0 7.7 13.0

99.6 118.0 11.5 38.0 67.3 74.0

118.0 38.0

Total biomass 1.445 60.617 9 9 . 1 4 9 344 .963 621.35

Total number of species 2 6 9 13 15

Number of species with platelet tests 2 5 7 10 11

611.4 1 ,950 .5 1,382.9 1,872.0

16 19 26 28

12 14 14 14

( ) Weight of 106 live cells (mg)

horizon that is easily divided into L, F, H and Ah layers. The tree layer was dominated by trembling aspen, with balsam poplar being less frequent in occurrence. The understory was composed mainly of various grasses and herbs and of wild rose shrubs (Dennis 1970; Lousier 1974a).

3 Methods

The colonization studies were carried simultaneously with the litter bag studies outlined in Lousier and Parkinson (1976, 1978), and those papers should be consulted for the details of the litter bag methodology. At each sampling time (1, 5, 8, 10, 12, 18, 24, 36, 48, 60 months after burial of litter bags), five litter bags of each species of tree litter were removed and returned to the laboratory where four replicate 1 g (wet weight) sub- samples were taken from each bag. Each sub-sample was fixed (Bouin-Hollande), stained (xylidine ponceau), macerated for 10 sec at 3,000 rpm in an Osterizer blender and filtered through a millipore filter. All fields on all filters were examined micro- scopically ( x 250, phase contrast) and the Testacea identified and counted. For further details of the sample preparation and examination, see Lousier and Parkinson (1981 a) and Stout et al. (1982).

4 Results

4.1 Species Succession

No colonization of the litter by Testacea was recorded before the 5-month sample (Tables t and 2); the litter bags were sam- pled after one month hut the winter freeze had occurred, the first permanent winter snow had fallen, and no Testacea were observed in the litter. The 5-month sample was taken less than one week after the initiation of the spring thaw. Colonization of the two types of litter was similar in terms of species and numbers of species, with the balsam litter being colonized by slightly fewer species. The major differences between the testacean communities colonizing aspen and balsam litter were: (1) the failure of E. rotunda and E. laevis, very ubiquitous species and only 45 ~tm in size (Lousier 1976), to colonize balsam litter as readily as they did aspen litter, (2) the more rapid colonization of balsam litter by the spined E. compressa and the non-spined E. compressa forma glabra, rare species and about 90 gm in size (Lousier 1976), and (3) the absence of Cyctopyxis puteus, and Plagiopyxis callida in balsam leaf litter at 60 months.

The family Euglyphidae had more colonizing species present, usually 50% or more of the species observed, during the first 24 months of colonization. After 60 months, two families, Eugly-

Table 2. The changes in active biomass (x 10 r mg g-1 dry weight) of species of Testacea colonizing balsam Ieaf litter

383

Species Age of litter (months)

5 8 10 12 18 24 36 48 60

Arcella catinus 3.2 5.1 15.2 31.4 9.5 13.9 14.0 21.6 Euglypha rotunda 12.7 7.7 22.5 19.9 30.6 E. laevis 5.8 3.5 8.6 15.7 24.4 E. scutigera 7.7 22.5 28.3 26.6 E. compressa 8.2 13.0 39.0 40.2 48.7 23.9 35.9 31.3 E. compressa forma glabra 8.2 13.0 39.0 40.2 24.3 23.9 35,9 31.3 E. cuspidata 1.3 0.5 0.8 2.4 2.5 9.1 2.2 2.9 4.6 E. polylepis 8.4 16.5 26.0 Trinema lineare 1. ! 3.2 16.4 25.7 38.6 43.9 49.2 T. enchelys 5.3 15.9 16.4 39.6 77.2 124.4 174.2 Phryganella acropodia 2.3 6.8 14.0 4.2 39.3 47.0 69.8 Difflugiella oviformis 0.04,l 0.017 0.026 0.079 0.082 0.25 0.27 0.29 0.30 Heleopera petricola 17.3 17.9 10.8 5.2 15.9 24.6 Hyalosphenia minuta 0.6 0.6 1.8 2.1 H. subflava 6.3 15.3 27.8 29.1 Centrophyxis aerophila 3.4 5.4 16.2 33.4 40.4 44.3 44.8 47.0 C. aerophila var. sphagnicola 6.1 18.5 23.6 C. sylvatica 86.4 259.2 267.2 808.0 315.2 238.4 304.0 C. cassis 8.0 C. plagiostoma 16.3 C. minuta 7.9 C. platystoma 3.5 C. laevigata 12.6 I0.9 CyeloFyxis eurystoma 9.6 24.3 C. kahli 24.1 36.8 63.8

Total biomass 1.344 23.517 132.43 414.3 498.2 1,046.4 692.1 790.9 1,055.0

Total number of species 2 6 10 11 �9 13 16 19 21 25

Number of species with platelet tests 2 5 7 8 10 13 14 14 14

phidae, with nine species in each type of litter, and Centropyxi- dae, with 12 species in aspen and 10 species in balsam litter, dominated the species compositiou of the testacean communities in the litter bags. In the aspen litter bags, all the L-layer species recorded in Lousier (1975, 1976) were present after 18 months, and all the species recorded in all the organic layers of the aspen forest soil, i.e., L, F, H, Ah (Lousier 1975, 1976), were found after 60 months. A similar situation was found by S. Visser (pers. comm.) in fungal isolation data from leaves in litter bags.

The proportion of testacean species which constructed their tests from platelets rather than sediment materials was >70% of the total number of species for the first 36; months of colonization (Tables 1 and 2).

4.2 Numbers and Biomass o f Colonizing Testacea

The changes in total numbers of Testacea (active and encysted) are summarized in Fig. 1). The colonization of aspen litter by Testacea after 60 months was more successful than that of balsam litter in terms of total numbers despite no significant differences in numbers of active forms for the first 12 months and numbers of encysted forms for the first 24 months between aspen and balsam litter.

The total biomass data indicated that while there were stand- ing crops of Testacea at 5 and 8 months, a substantial increase in biomass first occurred during the 8 to 10 month interval (Tables 1 and 2). This lag may be a normal phase of the growth curves of predatory or herbivorous populations (Cairns et al.

1969) allowing development of the diversity and quantity of the food base, in this case, bacteria (Stout 1973).

After 60 months of colonization, seven ubiquitous species (E. rotunda, E. &avis, T. lineare, T. enchelys, P. acropodia, D. oviformis, and C. aerophila) comprised 70% of the total numbers of Testacea in both aspen and balsam but only 33% of the total biomass in aspen and 38% of the total biomass in balsam. When present, C. sylvatica had by far the greatest biomass of all the testacean species, e.g. 90% at 8 months in aspen litter. Although the smaller species (e.g., T. lineare, D. oviforrnis) may have had a very low biomass, their numbers were considerably higher.

5 Discussion

5.1 Growth o f Colonizing Populations

The 5 year study of colonization can be broken up generally into three phases: (I) population growth was rapid, with the rapid immigration of species into the 'sterile ' litter; (2) the rapidly growing, more abundant populations slowed their rate of growth and began to oscillate, and the less abundant and perhaps newer populations continued their slow but steady increase to- ward their own asymptote; and (3) the manifestation of the community of litter-inhabiting testacean populations.

The growth in numbers and biomass of the populations colonizing aspen litter (Fig. 1, Table 1) can be compared to the mean annual abundance and biomass of the species in the soil and litter layers (Table 3). Only aspen litter is used because

7_

b

T v

< w

q ~ t.U F- 1.1_ o 0") r r LI.J nq

Z

384

25000 ASPEN 20000

"~0000 8000 6000 § 4000 ~I

2000

iO00 800 600 400 ~ I i ~

2OO

I, II I I0C

~ A �9 �9 �9

I0 20 AGE

BALSAM

~j"- ~ ~ / 1 ~

I ~ ' ~ " I

I /

I /

/

/ /

[I L I I I / I I L ,30 40 50 60 10 20 30 40 50

OF LITTER IN LITTER BAGS (MONTHS)

Fig. 1. Changes in total numbers of Testacea colonizing aspen and balsam litter, active forms; . . . . . . encysted forms; * denotes significant difference (p=0.05) from previous value along the curve; �9 denotes significant difference (p=0.05) in numbers between species of litter

60

it comprised about 85% of the weight of annual leaf litter fall (Lousier and Parkinson 1976). For most of the species of Testa- cea colonizing the litter, the fluctuations, over time, in numbers and biomass of an individual species reflected the numerical and weight differences for that species between the different soil and litter layers, i.e., either increasing or decreasing in numbers and biomass with profile depth. The only two major exceptions to this general t rend were E. compressa and E. com-

pressa forma glabra, which decreased in numbers and biomass for the first 36 months and then increased.

In the undis turbed decomposit ion cycle in the aspen woodland, the residence times per organic layer for the annual litter fall increment were determined to be: L1 (fresh litter), 1 year; Lz layer, 3 years; F layer, 3 years; and H /Ah layers, 18 years (Lousier and Parkinson 1976). The litter bags settled into the profile at the following rate: after 1 year, the bag occupied the L2 layer; after 3 years the bags were entering the F layer; and after 5 years, they were at the F-H layer interface. The colonizing species usually reached the mean annual L-layer abundance and biomass levels in the 12-36 mon th interval, while the F- and H-layer mean annual levels were achieved during the 18- 36 mon th and 36-60 mon th intervals respectively. Some species, most of which occurred in the F and H layers only (Table 3), had not reached the mean annual abundance and biomass levels even after the litter bags had been in place for 60 months. This

Table 3. Mean annual numbers (D) (g-1 dry weight) and biomass (B) ( • 10-4 mg g-1) of Testacea in the organic layers of the aspen woodland soil

Species L F H Ah

D B D B D B D B

Arcella catinus 319 29 318 30 83 8 0 0 Euglypha rotunda a 177 6 1,129 42 687 22 19 1 E. laevis a 416 16 765 31 556 20 10 0.5 E. scutigera a 159 12 134 10 376 29 100 8 E. compressa 115 28 97 23 0 0 0 0 E. compressa f. glabra 274 66 138 33 0 0 0 0 E. cuspidata a 1,106 17 332 5 178 3 0 0 E. polylepis 0 0 0 0 343 30 0 0 Trinema lineare a 1,628 34 6,558 131 8,930 179 595 12 T. enchelys ~ 1,690 166 2,203 216 2,080 203 251 24 Phryganella acropodia a 354 14 1,180 50 1,952 82 190 8 Difflugiella oviformis ~ 9,089 5 14,442 7 21,792 9 3,190 2 Heleopera petricola ~ 80 9 249 26 206 20 0 0 Hyalosphenia minuta ~ 142 1 253 2 436 3 81 0.5 H. subflava ~ 80 5 184 t 2 368 22 0 0 Centropyxis aerophila" 177 17 608 60 1,015 102 109 10 C. aerophila vat. sphagnieola a 89 10 304 38 291 36 64 8 C. sylvatiea 327 523 392 627 125 203 0 0 C. eassis 0 0 249 31 195 24 0 0 C. plagiostoma 0 0 309 78 271 68 0 0 C. minuta 0 0 290 18 226 14 0 0 C. platystoma 0 0 166 16 125 12 0 0 C. laevigata 0 0 0 0 125 21 0 0 Cyclopyxis eurystoma a 80 10 244 32 331 42 90 12 C. eurystorna var. gauthieriana 0 0 97 24 83 21 62 16 C. kahli 0 0 212 125 133 78 62 37 C. puteus 0 0 0 0 83 131 0 0 Plagiopyxis callida 0 0 249 63 233 56 43 11

Totals 16,302 968 31,102 1,730 41,213 1,438 4,866 150

Constant species (sensu Cofiteaux 1976)

385

w ~

TIME

{:3

TIME

TIME TIME

C.I

TIME

A. Ubiquitous species of Testacea, colonizing the litter after 5-'12 months in the field.

B. Litter species of Tesfacea, colonizing the litter after 5-18 months in the field.

C.

I7 / - TIME

TIME

Humus species of Testacea, colonizing the litter after 24-56 months in the field (I) or 18-60 months in the field (11",): I: Tests made of platelets; n: Tests made of sediment.

Fig. 2. Population growth curve patterns for testacean species colonizing fresh aspen and balsam leaf litter

f f

>- BACTERIA

.~xl ~ / J ~TESTACEA

TIME

A.

TH z @ ~ l/ cuRvE ,-

TIME

Fig. 3. A Growth of total numbers of bacteria and Testacea colonizing leaf litter. B Probable growth curve of soil organisms with rapid turnover rates colonizing fresh leaf litter

could be attributed to the artificiality of lhe litter bag environment, other limiting environmental conditions, slow testacean colonizing capabilities and population growth or to seasonal effects on abundance. The unpublished results of population dynamics studies of testaceans in the litter and soil layers indicated: (1) substantial seasonal fluctuations in testacean numbers, biomass and productivity; and (2) a necessity for frequent sampling (at least twice a week) because of fast generation times for Testacea. The infrequent sampling regime for this colonization study limits the assessment of population growth and productivity of colonizing testacean species.

All of the Centropyxidae (Centropyxis, Cyclopyxis and Pla- giopyxis spp.), with the exception of Cen tropyxis sylvatica, increased in mean relative abundance (RA) and relative biomass (RB) with litter age and soil profile depth. These species generally had lower RA and RB in the litter bags than in the soil layers,

perhaps indicating a lack of test-building materials in the litter bags. This does not appear to be a limitation for C. sylvatica which dominates the total testacean biomass in the litter.

Two Euglyphidae (Euglypha polylepis, Trinema lineare), both Hyalosphenia spp., Phryganella acropodia and Difflugiella oviformis also increased in RA and RB with profile depth and with litter age, but in this instance, all but D. oviJbrmis had greater RA and RB in the litter bags than in the soil layers. For Euglypha scutigera and Trinema enchelys, RA decreased after an initial increase and RB increased with litter age and soil profile depth; both parameters were again greater in the litter bags than in the soil layers. The remaining seven species showed decreases in RA and RB with soil profile depth and litter age, and all had higher RA and RB values in the litter bags.

Species having higher RA and RB values in the litter layers could again be a consequence of excellent environmental conditions resulting from the artificiality of the litter bag environment; it could perhaps indicate a preference by these species for the litter environment or an ability to better exploit the available resources in the litter environment.

Soil Testacea are now known to have relatively rapid reproductive capabilities (Hedley and Ogden 1973, 1974; Hedley et al. 1974; Lousier 1979; Sch6nborn 1975, 1977) and are thus able to reproduce to exploit a resource fairly quickly. If a testacean population is not growing on leaf litter, the prime limitations could be any or all of the following: substrate quality, food supply, or availability of test building materials.

The species population curves differed somewhat for the various testacean species. These have been categorized and are illus- trated in Fig. 2. The growth patterns of the individual populations, as well as the total testacean community, appeared generally to follow the principles of logarithmic or logistic growth. The patterns in Fig. 2A are those of ubiquitous species of Testa- cea, which colonize the litter after 5-12 months in the field and which usually numerically dominate the community. Figure 2B represents those species of Testacea which colonize the litter after 5-18 months in the field and which, despite peaking in density in the litter, are present in low numbers. Figure 2 C char- acterizes the two patterns of population growth of humus Testa- cea which are colonizing the leaf litter. The first is for those species which colonize the litter after 24-36 months in the field; these species all have tests composed of platelets. The second pattern is for the remainder of the humus species, which have

386

tests made of sediment particles and which colonize the litter after 18-60 months in the field.

5.2 Characteristics of Colonizing Testacean Populations

The leaf litter represents a habitat that can be considered unpredictable in terms of micro-climate and its effects on substrate quality. It would appear that the best strategy for a testate amoeba to succeed in colonizing such an unpredictable environment would be high reproductive rate, high growth rate and high dispersal rate in order to make best use of available resources before competition becomes more intense. Such species have often been called fugitive (Hutchinson 1951), opportunistic (MacArthur 1960; Hutchinson 1967), or r-strategists (MacAr- thur and Wilson 1967). Grassle and Grassle (1974) expanded the definition of opportunistic habit from the more narrowly defined processes of r-selection and K-selection and have charac- terized opportunistic species as those species relying on high reproductive rates, short life spans, large population sizes, wide physiological tolerances, broad dispersal abilities, density independent mortalities, and poor competitive abilities. MacArthur and Wilson (1967) predicted r-selection in species in climates which are rigourously seasonal and in which recolonization in the spring is by winter survivors responding to a proliferation of food supply. It is difficult to categorize the testacean community because of a lack of basic biological information on each species relative to physiological tolerances and competitive abi- lites. However, the climate was rigourously seasonal, a spring flush in activity has been recorded for other organisims (Dash 1972; Visser and Parkinson 1975; Visser and Whittaker 1977), and Testacea do meet some of the criteria of opportunistic species: high reproductive rates, short life spans, large population sizes, and density-independent mortalities (Lousier 1979) and broad (if not relatively high) dispersal abilities, and thus, as colonizers may be considered r-stategists. Compared to other protozoan groups, the Testacea may not have as high a dispersal ability (Bamforth 1980). However, in terms of exploiting the resources available to them, it appears as if the Testacea are capable of employing r-strategy processes during colonization of fresh litter and during periods of response to dramatically improving environmental conditions.

5.3 Factors Affecting the Establishment and Growth of Populations

The colonization behaviour of a consumer population is determined by the spatial and temperoal availability of substrate and food supply, and the dispersion, behaviour and abundance of competing and predatory populations. Soil Testacea also require available test-building materials. Based on the information gath- ered for this study, comments can be made only on the spatial and temporal availability of substrate and food supply, and the availability of test-building materials.

5.3.1 Substrate

While the substrate is always decreasing in quantity because of decomposition, it is improving in quality (as habitat for soil organisms) through chemical, physical and biological alteration (Lousier and Parkinson 1976, 1978). In other words, as litter age and depth in the soil profile increase, availability of substrate for colonizing Testacea increases. The initial substrate, i.e., the litter layer, is replenished annually through litter fall, while the other layers (F, H) are replenished through the accumulation

of decomposing organic matter. The relationship of spatial and temporal availability of substrate to testacean colonizers can be quantified to the extent that significant (p<0.05) positive correlation (r2>0.90) existed between the dry weight loss in aspen and balsam leaf litter and the total number of active Testacea, the total number of living Testacea, and the total number of species of testate amoebae present. As substrate quality improved because of the leaf litter losing its integrity and beginning to mineralize, environmental variability (e.g., fluctuations in microclimate) decreased and became more predictable, thus favouring greater activity and productivity of colonizing populations.

5.3.2 Food Supply

The discussion of the spatial and temporal availability of food supply can consider two sources of nutrition for testacean populations: the first is soluble organic substances, while the second and more important source is bacteria (Stout 1973). The organic substances have two major origins, the decomposing plant litter and the above- and belowground organisms. The availability to Testacea of dissolved organic nutrients from both sources is directly and indirectly affected by the temporal and spatial variation in substrate quantity and quality discussed above. Bac- terial use of soluble organic matter has been well-documented and is affected directly and indirectly in a fashion similar to that of Testacea. There is no documentation as to quality and quantity of competition for soluble organic foodstuffs between bacteria and Testacea and, indeed, other Protozoa.

Bacteria have been suggested as the major food source of Testacea (Stout 1973; Stout and Heal 1967) and as such should have a profound influence on several aspects of testacean ecology, in particular, colonization behaviour and success, and population ecology. The results of a 12 month study of bacteria colonizing aspen and balsam litter showed that the numbers of bacteria colonizing both aspen and balsam litter were similar (Lousier and Elliott 1975). Further analysis of these data showed that each sampling time after 0 months produced counts and biomass estimates that were significantly greater than those recorded at the previous sampling time. The initial rapid increase over the winter could have provided a substantial food base for primary consumer populations capable of colonization of the leaf litter and utilizing the bacteria as a food source. Gray et al. (1974) have shown that bacterial numbers continue to increase during decomposition but do not fluctuate widely.

The organisms isolated were, on the whole, active in the utilization of one or more of the following compounds : glucose, casein, gelatin, starch, citrate and urea (Lousier and Elliott 1975). This may have indicated a zymogenous flora which was present in larger numbers on litter containing easily utilizable compounds. The concentration of proteolytic, amylolytic, cellulolytic and nitrogen-fixing bacteria is often higher in litter than in soil (Remacle 1971).

The growth curve for the increase in bacterial numbers showed an exponential increase over the winter and stabilized during the following spring, summer and fall, perhaps oscillating about a mean level. Total testacean numbers also increased ex- ponentially, but only after a 6 month time lag, and appeared to begin to oscillate once approaching an asymptote. The relationship between the logistic curves of both groups of organisms is approximated in Fig. 3A. However, these curves are suscepti- ble to the criticism offered by Pielou (1969) ; the fit of the logistic curve to observed growth curves is more apparent than real. The curves should probably be a variation of the curves shown

387

in Fig. 3 B, with the oscillations caused by fluctuating environmental conditions decreasing with time as the litter environment improves by moving down the profile. The oscillations may be regular or irregular, depending on flucutations in seasonal and annual environmental conditions.

A diverse and abundant bacterial flora must be available for successful invasion by Testacea. It seems likely that the quality and diversity of the food base may determine the succession of testacean species, whereas the quantky of the food base, in conjunction with micro-climate factors, may influence reproduction rates and population growth of testacean species.

Laminger (1978) concluded that Trinema enchelys, in a subal- pine mull humus type during periods of lower soil moisture contents, fed primarily on detritus partMes, but during periods of better to good soil moisture conditions, fed upon bacteria and smaller Testacea as well. Freshly J~allen litter would not appear to provide an appreciable opportunity for Testacea to ingest detrital material and it could be assmned that the effects of food supply on testacean colonization success would be related primarily to the status of the litter bacteria. Unfortunately, several aspects of the ecology of soil and litter Testacea are not fully explainable primarily because of the lack of basic knowledge with regard to nutrition.

5.3.3 Availability o f Test-Building Materials

The proportion of testacean species which constructed their tests from platelets rather than sediment particles was > 70% of the total number of species present during the first 36 months of the colonization study. This may have indicated an unavailability of sediment particles for test construction, and, consequently, lower reproductive rates and slower population growth amongst those Testacea with sediment-based tests. The evidence of population studies (Lousier 1979) indicated that Testacea with sediment tests can reproduce as quickly as any other species of Testacea. However, it was found that these empty tests decom- pose more slowly (Lousier and Parkinson 1981 b), thus indicating possibly a greater demand on the available sediment materials. These sediment materials become more available with time and with depth of litter in the profile through several physical, chemical and biological processes and are thus not as abundant in freshly fallen litter (Lousier and Parkinson 1976, 1978).

5.4 Testacean Colonization Mechanisms

It is interesting to speculate how a testate amoeba, a relatively immobile organism, manages to colonize a new substrate such as leaf litter. High dispersal abilities, often thought as prerequisite for opportunistic colonization, are usually characteristic of highly mobile soil organisms (e.g., collembola, mites). Testacea require a water continuum in which to move, a continuum not readily available in newly fallen litter. However, after the first winter and spring thaw, the new litter had been readily flattened on the soil surface and featured improved moisture holding capabilities. Soil amoebae are thought to have very limited movement, in the order of 1-2 cm day-1 (Stout and Heal 1967). Despite this low mobility and other hurdles (such as discontinuity of moisture), soil Protozoa do colonize a diversity of substrates on the soil surface with some degree of success.

The following are possible colonization mechanisms used, passiveIy or actively, by soil and litter Testacea in the aspen woodland:

(1) immigration by movement onto and into the new substrate;

(2) redistribution of individuals and species by rainfall and water movements in the litter and soil;

(3) transport of encysted and active cells by metazoans; and (4) redistribution of litter, litter fragments, soil, and testacean

cells by the strong prevailing winds. Each mechanism may be used differently in scope and magni-

tude within the same site depending on the position of litter increment in the soil profile, or between sites depending on ecosystem/habitat type, vegetation/litter type, soil type, environmental conditions and species of Testacea available.

Acknowledgements. Financial support for the study was provided by an NSERC Operating Grant (No. A2257) to Dr. Dennis Parkinson and an NRCC Postgraduate Scholarship to the author.

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Documents

Colonization of decomposing deciduous leaf litter by Testacea (Protozoa, Rhizopoda): Species succession, abundance, and biomass