Feeding preferences of the collembolan Folsomia candida in relation to microfungal successions on decaying litter

Soil EM. Biochem. Vol. 24, No. 7, pp. 685-692, 1992 Copyright

Printed in Great Britain. All rights reserved

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FEEDING PREFERENCES OF THE COLLEMBOLAN ZWLSOA4Z/l CANDID/l IN RELATION TO MICROFUNGAL SUCCESSIONS ON DECAYING LITTER JOHN N. KLIRONOMOS,*PAUL WIDDENt and ISABELLEDESLANDES Department of Biology, Concordia University, 1455 De Maisonneuve W., Montreal, PQ, Canada H3G 1M8 (Accepted 31 January 1992) Summary-The feeding preferences of two strains of the collembolan, Folsomiu candida, for some common primary and secondary saprophytes of spruce and fir litter were investigated. The fungi were grown on spruce or fir litter, or on cellophane strips that had been placed on top of malt agar. The ability of the animals to survive and reproduce on the fungi was also investigated and a microcosm system was used to examine the effect of collembolan grazing on the microfungal succession on spruce litter. The experiments demonstrated selective feeding. Generally the insects preferred primary saprophytes to secondary saprophytes and selected foods that increased their fecundity. The microcosm study showed that the absence of the grazers slowed down the rate at which primary saprophytes on litter were replaced by secondary saprophytes. These data therefore support the hypothesis that fungal successions observed in the field on decaying litter may result from preferential grazing by microarthropods.

are more or less rapidly colonized by a wave of soil fungi (“secondary saprophytes”), which include species of Penicillium and Trichoderma. This general pattern has been observed on the decaying remains of many plant species in many different habitats (Hudson, 1968; Cooke and Rayner, 1984; Pugh and Boddy, 1988). Garrett (1963) suggested that these successions depended on biochemical changes in the litter during decomposition, the early colonizers using simple sugars and the final stages being dominated by fungi able to use the remaining complex polymers. Park (1955) suggested that the fungi occurring later in the succession were better competitors than the early colonizers. Park (19.55) also suggested that whereas primary saprophytes, such as Cladosporium spp, are well adapted to conditions in the canopy, they may be unable to exist in the soil. There is, however, little evidence in the literature to support these theories. Many of the primary saprophytes have the enzymes to use more complex substrates (Domsch er al., 1980). Some primary saprophytes, such as Cladosporium spp, can persist in the soil for some time (Hudson, 1968) and there is no direct evidence that primary saprophytes are poor competitors; indeed some (e.g. Epicoccum purpurascens) are known to produce antifungal antibiotic compounds (Brown et al 1987). Studies on the feeding preferences of springtails (Collembola) and mites (Atari) have often shown that these common soil fungivores prefer dark pigmented fungi to non-pigmented fungi (Mills and Sinha, 1970; Aitchison, 1983). Visser (1985) suggested on early successional fungi, e.g. that “grazing

INTRODUCTION Grazing by animals can have a profound effect on plant community development and structure. This has been demonstrated in classical studies on the effects of grazing on grasslands (Daubenmire, 1968) and on community structure in the intertidal zone (Connell, 1961; Paine, 1969; Lubchenco, 1983). In decomposer systems, bacteria and fungi form the base of a food web that is just as complex as those found in producer-consumer systems. These are a source of food for “primary decomposers” protozoans, nematodes, annelids, and a wide range of arthropods, including mites and collembolans. In spite of this, little is known concerning the influence that grazing by soil fauna may have on the decomposer community, even though it is recognized that these effects may be important (Parkinson et al., 1979; Newell, 1984a, b; Visser, 1985; Moore, 1988; Moore et al. 1988; Teuben, 1991). The succession of fungi on leaf litter has been described by Kendrick and Burges (1962), Hudson (1968), Widden and Parkinson (1973) and others. The succession begins on senescent leaves on the tree, when they are colonized by “primary saprophytes”, commonly dematiaceous fungi such as species of Alternaria, Cladosporium, Epicoccum, and Phoma. It is thought that the dark pigments of these fungi protect them in the canopy from ultraviolet radiation (Pugh and Boddy, 1988). When the leaves fall they

*Present address:

Department of Biology, University Waterloo, Waterloo, Ontario, Canada N2L 39L. tAuthor for correspondence.

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Cladosporium spp on leaf litter . could allow accelerated fungal succession. .“. It is possible that selective grazing by the soil fauna could be influencing the succession of microfungi on decaying leaves once they reach the ground. Removal of the pigmented fungi by grazing could allow non-pigmented fungi, such as Trichoderma and Penicillium species, to replace them. In this study we used the collembolan Folsomia candidu and a number of common primary and secondary saprophytes to test the hypothesis that successions of microfungi on decaying litter may be under the control of grazing by fungivorous soil fauna. F. candida is commonly found in the litter layer of coniferous and deciduous soils (Wallwork, 1976; Christiansen and Bellinger, 1980), and occurs in the spruce and fir forests that we have been studying (Widden, 1986; Harney and Widden, 1991). The study employed feeding preference tests, laboratory microcosms, and developmental studies to answer the following questions: Does F. candida show feeding preferences for microfungi that are consistent with the hypothesis that fungal successions on the litter are being controlled by selective feeding? Are the feeding preferences of F. candida for microfungi of adaptive significance to the animals? How important are interactions between the fungus and the substrate in determining feeding preference and reproductive success? Can it be demonstrated that feeding by F. candida can change the course of microfungal succession in a microcosm system?

shown that young individuals rarely move from their release site with or without food (Johnson and Wellington, 1983). Young adults were used because they are beginning oviposition, while still growing at a relatively high rate, and therefore have greater food requirements than younger or older springtails (Johnson and Wellington, 1983). Litter Balsam fir [Abies balsamea (L.) Mill.] litter was collected from Lac a L’epaule. Norway spruce litter [Picea abies (L.) Karst.] was collected from a Norway spruce forest near Lacolle in southern Quebec. described in Widden (1979). Preparation of fungi for feeding tests Agar-grown fungi. The fungi were grown for 1 week on pieces of dialysis tubing (Spectrapor 20) on the surface of 2% malt extract agar. The membranes with the fungus growing on them were then peeled off of the agar surface and cut into 1 cm* squares. These squares were then placed in the test arenas, thus allowing us to present the fungi as food choices in the absence of agar. Litter-grown fungi. Balsam fir or Norway spruce needles were sorted to separate all unwanted debris and 5 g portions were placed in 125 ml Erlenmeyer flasks along with 25 ml distilled water. The flasks were autoclaved for 2 min, left overnight to cool, and inoculated with pure cultures of the microfungi. Using a 5 mm dia cork borer, 2 plugs of fungus were removed from the edge of an actively-growing culture, and placed aseptically into the flasks which were kept at 25°C for 2 weeks.

MATERIALSANDMETHODS

Fungi

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Eight microfungi obtained from coniferous forest soils or litter in Quebec were used. Four were primary saprophytes [Cladosporium cladosporioides (Fres.) de Vries, Epicoccum purpurascens Ehrenb. ex Schlecht., Phoma sp., Sterile dark sp.], three were secondary saprophytes [PeniciIlium thomii Maire (DAOM 167012), Trichoderma koningii Oudem. (DAOM 167074), Trichoderma viride Pers. ex gray (DAOM 167060)], and one was a sugar fungus (Mucor hiemalis Wehmer), present throughout the succession process. Cultures were maintained at 5°C on 1% malt extract agar (MEA) slants and subcultured periodically.

Pairwise tests. 15 g of autoclaved (120°C for 20 min) 25 : 1 mixture of plaster of Paris and charcoal (Booth, 1983) were added to 60 x 20 mm plastic Petri dishes. Excess sterile distilled water was then added, the mixture was well stirred and allowed to settle overnight. The excess water was emptied out and the sides of the dishes were cleaned with a tissue and allowed to dry under U.V. radiation. All plates were kept moist continuously by adding sufficient sterile distilled water. Two squares of each test fungus, or two sets of 5 fir needles infected with each test fungus, were then placed equidistantly around the perimeter of the dishes, alternating each food type. All pairwise combinations of the 8 fungi were tested against each other (28 in total). Twenty adult collembolans that had been starved for 1 week were then placed in the centre of each dish. The dishes were placed in the dark and, 6 h later, the numbers of collembolans feeding at each station were recorded. Both field and lab animals were tested. All combinations were replicated 5 times. Multiple-choice tests. Plaster of Paris-charcoal mixture (50 g) was added to each of five 140 x 15 mm

Animals Two cultures of F. candidu (Willem) were used in these experiments. The first had been isolated from agricultural soil at Macdonald College of McGill University by Dr S. Hill, referred to in this study as the lab animals. The second was isolated from a Balsam fir forest at Lac a L’epaule (Harney and Widden, 1991), and is referred to as the field animals. Only adult collembolans were used, since it has been

Feeding preferences for F. cundida glass Petri dishes and the base was prepared as described above. The 8 test fungi were then added to these large arenas, spaced equidistantly around the perimeter of the arenas. The order of the food placement was chosen randomly in each replicate. Eighty starved adult collembolans were then placed in the centre of each dish. Dishes were placed in the dark at room temperature. After 6 h the numbers of collembolans feeding at each station were recorded. No animal was used more than once during the feeding tests. To prevent animals from being influenced by possible pheromonal cues left by animals from previous experiments, all plastic dishes were discarded after use, and the glass dishes were cleaned and sterilized before reuse. Developmental study Development on agar-grown fungus. Twenty animals (1 week old), which had been starved from birth, were put into each of 8 separate glass jars (80mm deep x 45 mm wide) filled with 30 g of the base mixture. Each jar was provided with a constant excess supply of one of the test fungi, grown on agar as described in the feeding tests. The jars were aerated and humidified weekly. Body size and fecundity (number of young produced) were recorded after 28 days. This period was calculated as the time it took for the collembolans to mature from the first day of feeding to the first day of egg laying plus 7 days. This experiment was replicated 5 times. Development on litter-grown fungi. Batches of sterile litter were colonized separately by each of the 8 saprophytic fungi. Portions (3 g) of colonized litter were placed in separate 25 x 150 mm test tubes. Batches of 20 starved l-week old animals were added to each of the tubes. Five replicate sets of tubes for each fungus were prepared. After 6 weeks the animals were extracted with a Tullgren funnel and the numbers of adult and juvenile animals were recorded.

dishes, 300 collembolans were added, and 6 were left without animals (control). The dishes were then kept at 20°C for 6 weeks at 100% r.h. Every 2 weeks, 5 needles were removed from each flask and surface sterilized with 0.1% HgCl, for 3 min (Kendrick and Burges, 1962). The needles were then cut into 5 fragments, plated on MEA, and incubated for a period of 10 days, after which the fungi growing from the needle fragments were recorded. This experiment was terminated after 6 weeks because contaminants started to appear. Statistical methods The pairwise feeding tests were analyzed using a Pearson chi-square goodness-of-fit test to a 50: 50 ratio (Zar, 1984). The recorded data were pooled for all replicates. The 8-choice feeding tests were analyzed using a multivariate ANOVA to detect effects due to the foods. For the developmental study, a one-way ANOVA was used to analyze fecundity and body size as a function of different foods. In the microcosm experiment, a one-way ANOVA was used to detect differences between the number of litter fragments colonized by primary and secondary saprophytes as a function of the presence of collembolans.

RESULTS

In the majority of tests, F. candida showed significant feeding preferences (Figs 1 and 2). When comparing the feeding preferences of the two collembolan populations, few differences were observed. Both the feeding preferences (Fig. 2) and the % animals feeding (Fig. 3) were almost identical when the two collembolan populations fed on the same substrate. However, different preferences were seen when the fungi grew on different substrates. When grown on

Microcosm study A, horizon soil was collected from the Norway spruce forest, air-dried, and sterilized by autoclaving. Sterile soil (15 g) was added to each of six 60 x 20mm plastic Petri dishes. A total of 1 x lo6 conidia of each of three secondary saprophytes (P. thomii, T. viride and T. koningii) in 4 ml sterile distilled water were added to the soil and mixed well. Portions of litter (5 g) were placed in 125 ml Erlenmeyer flasks, along with 25 ml water. The flasks were autoclaved for 20min and left overnight to cool. They were then separately inoculated with one of the following primary saprophytes (C. cladosporioides, E. purpurastens or Phoma sp.) as described in the previous experiments. All flasks were left at 25°C for 2 weeks to allow the fungi to penetrate the needles. Twenty needles of each fungus (a total of 60 needles) were then placed on top of the moist soil in the dishes which had been colonized with secondary saprophytes. To 6 of these

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Fig. 1. Summary of chi-square analyses of pairwise feeding tests on the lab animal population using fungi grown on MEA. Comparisons are defined by letters in bold on the left and upper margins. EP = E. purpurascens, CC = C. cladosporioides,SD = Sterile dark sp., PH = Phoma sp., MH = Mucor hiemalis, PT = P. &mii, TV = T. vi&, TK = T. koninnii. Where significant preferences occurred the letters denoting the preferred fungus are entered, ns signifies a non-significant preference, X denotes that the comparison was not tested. Significant differences using Pearson chi-square at P < 0.05.

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Fig. 2. Summary of chi-square analyses of pairwise feeding tests, using fungi grown on two different litter substrates (balsam fir and Norway spruce) and coilembolan populations (lab and field). Data are expressed as in Fig. 1 except that LI = Sterile Litter.

agar, C. cladosporioides and the sterile dark fungus were the preferred foods (Fig. 1). When grown on Norway spruce litter, E. purpurascens, C. cludosporiaides, and Phoma sp. were the preferred foods [Fig 2(c),(d)], and, when grown on balsam fir litter, 7’. koningii was preferred over Phoma sp. [Fig 2(a),(b)]. The secondary saprophytes, P. thomii and T. viride, were never preferred foods when growing on litter. During the pairwise tests, more animals fed on fungi grown on litter than fungi grown on MEA (Fig. 3). Also, when a primary saprophyte was present, more animals were found feeding than when only secondary saprophytes were provided. In the case of balsam fir, even when only secondary saprophytes were introduced, a relatively high number of animals were seen feeding. This may be explained by the high preference for T. kon~gii when grown on balsam fir litter. The results of the multiple-choice feeding tests were consistent with those of the pairwise feeding tests [Fig. 4(a),(b)]. Again C. cladosporioides was a preferred food when grown on any substrate, whereas E.

purpurascens was preferred when grown on Norway

spruce litter, but not when grown on balsam fir litter or on agar. Tri~hoder~~zakoningii, however, was a preferred food when grown on balsam fir litter, but not when grown on Norway spruce litter (P < 0.05) or on agar. No differences were seen between preferences for the other fungi. P. thomii and T. riride were the least preferred foods, along with Phoma sp. when grown on balsam fir and T. koningii when grown on Norway spruce litter, The major inconsistency in these data was the behavior of the field population of animals, fed on agar-grown fungi. The field population showed a marked preference for the sterile dark fungus in the multiple choice tests, whereas the lab animals did not (Fig. 4). There was a significant effect (P < 0.001) of food type on total body size reached when the collembolans were raised to maturity on a single fungal diet. The diet permitting most growth was E. purpuruscens and the one permitting least growth was T. koningii (Fig. 5). There was also a significant effect of diet on fecundity (P < 0.01). E. purpurascens produced the

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Fig. 3. Percentage of animals actively feeding in the pairwise feeding tests. SVSS: feeding tests between two secondary saprophytes; SVSL: feeding tests between secondary saprophytes and sterile litter; PVSS: feeding tests between primary and secondary saprophytes; PVSL: feeding tests between primary saprophytes and sterile litter; PVSP: feeding tests between two primary saprophytes. LFIR: lab animals, fungi grown on fir litter; FFIR: field animals, fungi grown on fir litter; LSPRUCE: lab animals, fungi grown on spruce litter; FSPRUCE: field animals, fungi grown on spruce litter; LMEA: lab animals, fungi grown on malt extract agar. Error bars represent 95% confidence limits for the mean.

highest fecundity, whereas T. koningii gave the lowest (0) (Fig. 5). Generally the animals feeding on primary saprophytes grew larger, and produced more young than those growing on secondary saprophytes (Fig. 5). Similar results were obtained when the fungi were grown on litter and fed to the animals. The primary saprophytes yielded more young than the secondary saprophytes when grown on either balsam fir or Norway spruce (Fig. 6). Again, there was a major anomaly in the data, in that the animals reared on T. viride yielded as many young as any other fungus when grown on Norway spruce litter [Fig. 6(b)]. Grazing by F. candida was seen to significantly (P < 0.05) affect the microfungal succession during the 6 week period of the microcosm experiment (Fig. 7). Colonization of the litter fragments by primary saprophytes did not change very much in the absence of the collembolans, although litter fragments were also being colonized by secondary saprophytes. In the presence of the collembolans, primary saprophytes were almost totally eliminated after the second week, allowing for more colonization by secondary saprophytes. After the second week, the total number of litter fragments colonized by fungi (primary and secondary saprophytes combined) was slightly higher in the presence of the collembolans.

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Fig. 5. Body length and eggs laid (as a measure of fecundity) by F. candida when feeding on pure cultures of fungi grown on MEA. Symbols for fungal taxa are as in Fig. I. Error bars represent 95% confidence limits for the mean.

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et al

on litter by favoring colonization by secondary saprophytes. That these preferences are of adaptive significance to the animals is indicated by the growth rates and fecundity, which ranked closely with the feeding preferences, whether the fungi were agar-grown (Figs 1 and 5) or litter grown (Figs 2 and 6). There were two exceptions; T. koningii, which was a preferred food when grown on balsam fir [Fig. 2(a),(b), Fig. 41, but gave poor fecundity [Fig. 6(a)], and T. viride which, when grown on Norway spruce, gave a high fecundity [Fig. 6(b)] and yet was never a preferred food source [Figs 1, 2(c),(d) and Fig. 41. Onychiurus armatus also exhibited a feeding preference hierarchy for basidiomycetous fungi which was consistent with survival, growth and reproductive rates (Shaw, 1988). Shaw’s data, however, also show an anomaly, with Lactarius rufus being preferred to Marasmius androsaceus, even though the animals had a lower survival when feeding on it. These anomalies in the data could result from the evolution by the fungi of strategies to avoid grazers, much as plants have evolved both physical and chemical defences to avoid being eaten. Such interactions between the fungus, the substrate, and the animals, and the possible evolution by fungi of defence systems aimed at grazers are always likely to complicate the interpretation of laboratory data on the relationships between feeding preferences and fitness. Our data also show that the substrate on which the fungus is growing has an effect on the food preferences of the animals. This was particularly noticeable in the case of T. koningii, which, when grown on balsam fir, became a preferred food. even though it was avoided when grown on agar or on Norway

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E. purpurascens and C. cladosporioides, were normally preferred when tested against other fungi. Whereas it is dangerous to generalize from simple feeding experiments in the laboratory to succession processes in the field, a survey of the literature suggests that these results form part of a general pattern. Thus, Addison (1977) demonstrated that the arctic collembolan, Hypogastrura tullbergii, preferred C. cladosporioides and Phoma herbarum over Penicillium notatum and a species of Cylindrocarpon. Aitchison (1983), working with Isotoma uiridis, Orchesella ainslei, Tomocerus flavescens, Onychiurus sp., and Xenylla sp. demonstrated feeding preferences for dematiaceous fungi, as did the study of Parkinson et al. (1979), using Onychiurus subtenuis. Dash and Cragg (1972) showed that not only Collembolans, but Enchytraeid worms, Nematodes and mites showed preferences for dematiaceous fungi rather than Paecilomyces and Penicillium species. These observations, therefore, lend support to the hypothesis that, by preferentially feeding on pigmented fungi, the soil fauna may be controlling successions

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Fig. 7. The abundance of primary or secondary saprophytes on Norway spruce litter previously colonized by primary saprophytes, as affected by grazing by F. candida. Bars

represent the percentage of plated needle fragments colonized by either primary saprophytes (P) or secondary saprophytes (S) in grazed (GRAZERS) or control (CONTROL) microcosms. Error bars represent 95% confidence limits for the mean.

Feeding preferences for F. cundida spruce litter. Bengtsson et al. (1988) have shown that fungi produce a number of volatile compounds which may be attractive or repellant to collembolans. They demonstrated the movement of two fungi on the ranking scale when a different substrate was used, and showed that fewer compounds released from one of the fungi in agar were more attractive than the greater number released from the fungus in soil. This variation of the ranking of food items from one environment to another, due to changes in fungal chemistry, is consistent with our data showing different preferences when different litter substrates were used. These shifts in ranking make it dangerous to extrapolate from feeding preference tests of agargrown fungi to the field situation. There are obvious advantages to using agar-grown fungi for feeding experiments, in that one can be sure that the only food-source is the fungus, and that there is excess fungus available. When the fungi are grown on the litter, it is not possible to ensure that the animals are only feeding on fungus, and one cannot see how much fungus is present. In our experiments with litter-grown fungi, C. cladosporioides was the fungus that showed the least visible mycelium when grown on litter, even though it was the favored food, so we are reasonably sure that the animals were not just responding to the quantity of food available. That the litter itself was not attractive as a food is demonstrated by the fact that sterile litter was never preferred to litter infected with a fungus (Figs 2 and 3) and, alone, could not support the survival of these animals (Fig. 6). We have shown that F. candida can successfully exist and reproduce on a wide range of fungi (Figs 5 and 6). According to optimal foraging theory, food specialization is only an advantage when the food concentration is high. In nature it is unlikely that a homogeneously high abundance of one fungal species is common, so one would expect to find a significant number of generalist grazers. The data indicate that F. candida is a generalist, which is capable of selecting the optimal food from a range of fungi. This ability may explain why an insect which is parthenogenic (Marshall and Kevan, 1962) and therefore should have low genetic diversity within the population, has such a wide distribution in North America (Christiansen and Bellinger, 1980). It may also explain why the two populations from quite different habitats exhibit very similar feeding preferences under the varied experimental conditions to which they were exposed. In the microcosms the frequency with which the primary saprophytes were isolated from the litter remained fairly constant with time in the absence of collembolans. When the collembolans were present, the secondary saprophytes had almost completely eliminated the primary saprophytes within 2 weeks (Fig. 7). Thus, grazing by F. candida had altered the rate of replacement of primary saprophytes by secondary saprophytes.

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The data from the microcosms, in combination with those from the feeding tests support the hypothesis that grazing effects could cause the replacement of dark pigmented primary saprophytes by light pigmented secondary saprophytes. They do not, however, confirm that this happens in nature. Field studies, using methods to exclude grazers from decaying litter would be useful to confirm this hypothesis. That collembolan grazing can profoundly influence fungal community composition has been demonstrated by other researchers. Parkinson et al. (1979) used microcosms to show that collembolan grazing stimulated the colonization of a basidiomycete fungus over a sterile dark fungus on litter by reinforcing or switching an existing competitive relationship. Newell (1984a, b) used a combination of laboratory experiments and field observations, to show that grazing by the collembolan, Onychiurus latus, could change the fungal community and possibly affect rates of cellulose decomposition in Norway-spruce litter. In this paper we have shown that F. candida displays fungal food preferences in vitro which are usually consistent with the ability of the food to support growth and reproduction. These preferences are dependent on the substrate that the fungus is grown on. Evidence is presented that preferential grazing may be an important driving force in the succession of microfungi on coniferous leaf litter. Our data show that the interactions between fungivorous microarthropods, the fungi, their substrates, and the structure of the fungal community are extremely complex. These interactions deserve more thorough investigation than they have so far been exposed to. Acknowledgements-This study was supported by a grant to Paul Widden by the Natural Sciences and Engineering Research Council of Canada. We also wish to thank Vilma Scattolin and Maria Troli for technical assistance.

REFERENCES

Addison J. A. (1977) Population dynamics and biology of Collembola on Truelove Lowland. In Truelove Lowland, Devon Island, Canada: A High Arctic Ecosystem (L. C. Bliss Ed.), pp. 3633382. University of Alberta Press, Edmonton. Aitchison C. W. (1983) Low temperature and preferred feeding by winter active Collembola (Insecta, Apterygota). Pedobiologia 25, 27-36. Bengtsson G., Erlandsson A. and Rundgren R. (1988) Fungal odour attracts soil Collembola. Soil Biology & Biochemistry 20, 25-30. Booth R. G. (1983) Effects of plaster-charcoal substrate variation on the growth and fecundity of Folsomio condida (Collembola, Isotomidae). Pedobiologia 25, 187-195. Brown A. E., Findlay R. and Ward J. S. (1987) Antifungal compounds produced by Epicoccum purpurascens against soil-borne plant pathogenic fungi. Soil Biology & Biochemistry 19, 657464. Christiansen K. and Bellinger P. (1980) The Collembola of North America, Part 2, Families Onychiuridae and Isotomidue. Grinnell College, Iowa.

692

JOHN N. KLIRI3NOMOS et

Connell J. H. (1961) The influence of interspecific cotnpetition and other factors on the distribution of the barnacle Cthamalus stellarus. Ecolonv 42, 710-123. Cooke R. C. and Rayner A. D. M. (1984) Ecolog.~ qf Saprotrophic Fungi. Longman, New York. Dash M. and Cragg J. B. (1972) Selection of microfungi by Enchytraeidae (Oligochaeta) and other members of the soil fauna. Pedobiologia 12, 282-286. Daubenmire R. (1968) Plant Communities. Harper & Row, New York. Domsch K. H., Gams W. and Anderson T-H. (1980) Compendium of Soil Fungi, Vol. I. Academic Press, New York. Garret S. D. (1963) Soil Fungi and Soil Ferti1it.y. Pergamon Press, Oxford. Harney S. and Widden P. (1991) The ecology of Paecilomyces farinosus in two balsam fir forests infested with spruce-budworm. Canadian Journal of Botany 69, 512-515. Hudson H. (1968) The ecology of fungi on plant remains above the soil. New Phytologist 67, 837-874. Johnson D. L. and Wellington W. G. (1983) Dispersal of the Collembolan Folsomia candida Willem, as a function of age. Canadian Journal of Zoology 61, 25342538. Kendrick W. B. and Burges A. (1962) Biological aspects of the decay of Pinus sylvestris leaf litter. Nova Hedwigia 4, 313-342. Lubchenco J. (1983) Littorina and Fucus: effects of herbivores, substratum heterogeneity, and plant escapes during succession. Ecology 64, 1116-l 123. Marshall V. G. and Kevan K. M. (1962) Preliminary observations on the biology of Folsomia candida Willem, 1902 (Collembola: Isotomidae). ‘The Canadian Entomologist 94, 575-586. Mills J. T. and Sinha R. N. (1970) Interactions between a springtail, Hypogastrura tullbergi, and soil-borne fungi. Journal of Economic Entomology 64, 398401. Moore J. C. (1988) The influence of microarthropods on symbiotic and non-symbiotic mutualism in detrital based belowground food webs. Agriculture, Ecosystems and Environment 24, 147-1.59. Moore J. C., Walter D. E. and Hunt H. W. (1988) Arthropod regulation of micro- and mesobiota in belowground detrital food webs. Annual Review of Entomology 33, 419439.

al

Newell K. (1984a) Interactions between two decomposer basidiomycetes and a Collembolan under Sitka spruce. Soil Biology & Biochemistry 16. 221-233. Newell K. &984b) Interactions between two decomposer basidiomycetes and a Collembolan under Sitka spruce: grazing and its potential effects on fungal distribution and litter decomposition. Soil Biology & Biochemistry 16, 2355239. Paine R. T. (1969) The Pisaster-Tegula interaction: prey patches, predator food preference and intertidal community structure. Ecology 50, 950-961. Park D. (1955) Experimental studies of the ecology of fungi in the soil. Transactions of the British Mycological Society 38, 130-142. Parkinson D., Visser S. and Whittaker J. B. (1979) Feeding preferences for certain litter fungi by Onychiurus subtenuis. Soil Biology & Biochemistry 11, 529-535. Pugh G. J. F. and Boddy L. (1988) A view of disturbance and life strategies in fungi. Proceedings of the Royal Society of Edinburgh 94B, 3 -11. Shaw P. J. A. (1988) A consistent hierarchy in the fungal feeding preferences of the Collembola Onychiurus armatus. Pedobiologia 31, 179-187. Teuben A. (1991) Nutrient availability and interactions between soil arthropods and microorganisms during decomposition of coniferous litter: a mesocosm study. Biology and Fertility of Soils 10, 256-266. Visser S. (1985) Role of soil invertebrates in determining the composition of soil microbial communities. In Ecological Interactions in Soil (A. H. Fitter, D. Atkinson, D. J. Read, M. B. Usher, Eds), pp. 297-317. Blackwell, Oxford. Wallwork J. A. (1976) The Distribution and Diversity of Soil Fauna. Academic Press. London. Widden P. (1979) Fungal populations from forest soils in southern Quebec. Canadian Journal of Botany 57, 1324 1331. Widden P. (1986) Microfungal community structure from forest soils in southern Quebec, using discriminant function and factor analysis. Canadian Journal of Botany 64, 140221412. Widden P. and Parkinson D. (1973) Fungi from Canadian coniferous forest soils. Canadian Journal of Botany 51, 2275 2290. Zar J. H. (1984) Biostatistical Analysis. Prentice-Hall, New Jersey.