Oecologia (Berlin) (1987) 72:597-604 Oecologia �9 Springer-Verlag 1987

Effects of terrestrial isopods on the decomposition of woodland leaf litter M. Hassall 1, J.G. Turner 2, and M.R.W. Rands 1. 1 School of Environmental Sciences and z School of Biological Sciences, University of East Anglia, Norwich, NR4 7T J, UK

Summary. The indirect contribution terrestrial isopods make to decomposition processes by stimulating microbial activites has been quantified in laboratory experiments. The extent to which microbial metabolism is enhanced as a re- sult of the passage of Betula pendula leaf litter through the alimentary system of isopods was measured for both freshly fallen and decayed leaves. Faeces derived from 1 g freshly fallen litter lost 75 mg g 1 D.W. more than did in- tact leaves, as a result of enhanced microbial metabolism. Faeces derived from 1 g of previously decayed leaves, which were shown to be the preferred food of isopods, lost only 17.5 mg g-1 D.W. more than intact decaying leaves. The isopod's direct contribution to soil metabolism was calcu- lated to be 151 mg and 138 mg g-1 litter ingested when fed on freshly fallen and decayed leaves respectively. It is concluded that the physical and chemical changes in the leaf substrate which result from fragmentation and diges- tion by isopods do not necessarily accelerate the subsequent decomposition of the litter very significantly. Fungal propa- gule density was 3.2 • and 3.6 • higher in faeces derived from freshly fallen and decayed leaves respectively than in the intact litter. Numbers of viable bacteria were corre- spondingly 126 x and 34 x higher in faeces than in the freshly fallen and the decayed leaves. Levels of microbial inhibitors were lower in the faeces than in the leaves but levels of free amino acids stayed higher for longer in the faeces than they did in intact litter. In the field the physical removal of litter by the soil macrofauna from surface to deeper and moister microsites may be the most important indirect contribution that they make to decomposition pro- cesses.

Key words: F a u n a - Microbe interactions Decomposi t ion- Communication

A widely accepted principle of soil biology is that members of the soil fauna by enhancing microbial activity, make a much greater indirect contribution to decomposition pro- cesses than the direct contribution they make as a result of their own metabolism. In this paper we question whether this principle applies to terrestrial isopods.

In most ecosystems the soil fauna makes a direct contri- bution of less than 10% to total soil metabolism (Macfa-

* Present address: International Council for Bird Preservation, 219c Huntingdon Road, Cambridge, CB3 0DL, UK

Offprint requests to: M. Hassall

dyen 1968; Reichle 1977; Persson et al. 1980). This is initial- ly difficult to reconcile with the results of exclusion experi- ments such as those conducted by Edwards and Heath (1963) Witkamp and Crossley (1966) and the studies of Coughtrey et al. (1979) which show that in the absence of the soil fauna litter disappearance is greatly retarded. One explanation for these two apparently contradictory sets of observations is that the animal's indirect effect on the mi- croflora is an important factor affecting rates of decomposi- tion.

Members of the saprophagous fauna have relatively low assimilation efficiencies so although their contribution to total soil metabolism may only be small, e.g. 9.7%, Reichle (1977), a far greater proportion of the litter input to the soil system is processed by these animals. By combining Reichle's (1977) data with Heal & MacLean's (1976) esti- mate of 0.12 for the ratio of respiration:consumption for saprophagous invertebrates, and assuming the soil ecosys- tem to be in a steady-state with respect to C input in litter and output resulting from soil metabolism, it follows that 80.8% of incoming litter will be consumed by the soil fauna. Without invoking any indirect stimulation explanations this alone could account for the differences between the results of soil metabolism analyses and those from exclusion exper- iments, noting with Webb (1977) that disappearance of lit- ter from the soil surface does not imply that it has been completely mineralized.

There is however much evidence from laboratory studies to suggest that microbial activities are stimulated by interac- tions with the soil fauna. Visser (1986) suggests that the fauna can influence the microbes in three main ways:

1) by comminution, mixing and channelling of litter and soil,

2) by grazing on the microflora and 3) by dispersal of microbial propagules.

These are essentially physical activities, of which fragmenta- tion has been held by many authors (listed by Webb 1977) to be the most important.

Passage of leaf substrate through the alimentary systems of the macrofauna also results in significant chemical chan- ges such as in moisture, nitrogen and inhibitor content and pH (Van der Drift and Witkamp 1960; Bocock 1963; McBrayer 1973 ; Satchell 1974). Van der Drift and Witkamp (1960) showed that CO2 output from Enoicyla pusilla Burn. faeces and from mechanically fragmented litter was up to 7 x greater than the rate from intact oak leaves. Others (e.g. Satchell 1974) have concluded from these results that

598

the increase in surface area which resulted from fragmenta- tion was responsible for promoting the increased microbial activity, although the authors also describe a number of other physical and chemical changes resulting from frag- mentation.

In many British woodlands the most abundant macro- decomposers are terrestrial isopods. Representatives of this group were used in the present study to investigate their influence on decomposition processes, particularly that due to their interactions with the microflora. Hassall and Sutton (1978) have shown that comminution and trituration of leaf litter by three species of terrestrial isopod increases the surface area approximately 3 fold. By combining these data on increase in surface area with the data for the pro- portion of litter production consumed by isopods it was estimated that if the annual litter fall decomposed in 12 months under the influence of micro-organisms alone then it could take only 9.9 months in the presence of isopods at field densities provided two assumptions were valid: these were 1) that microbial densities increased to the same extent as the surface area in comminuted litter and 2) that microbial activity in the faeces was directly proportional to microbial densities.

The present study was undertaken to test these assump- tions in experiments in which both the densities and meta- bolic activities of the microflora on woodlouse faeces were compared with those on their food of woodland leaf litter.

Materials and methods

Selection of test materials

Porcellio scaber Latreille, Oniscus asellus Linnaeus and Ar- madillidium vulgare Latreille were collected from deciduous woodlands in central Norfolk and established separately in large plastic culture tanks with a mixture of damp decay- ing leaf litter for food and pieces of bark for shelter.

To select which species of leaf litter to use in the experi- ments food preference tests were carried out as described by Hassall and Rushton (1984) using both O. asellus and P. scaber with a range of the commonest species of leaf litter found in their natural habitat. Considering both freshly fallen and decayed litter, Betula pendulu Roth ranked overall as the most acceptable food species. There was however a marked difference in preference for freshly fallen and decayed litter. The "freshly fallen" litter had been collected within a few days of leaf fall in October and November, air dried and stored at room temperature and the "decayed" litter collected from the soil surface beneath the same plants in the following April and May and then stored moist at 4 ~ C until used. Both were soaked in distilled water for 4 h before the experiments to ensure that they had comparable moisture contents. To quantify the preferences between these two states of decay further, another series of experiments was carried out in smaller 2 way choice chambers consisting of 8 cm deep and 5.5 cm diameter plastic pots with plastic lids containing a base of 3 cm thick plaster of Paris that rose to a ridge 4.5 cm high across the centre. Freshly fallen and decayed B. pen- dula leaf samples were blotted dry, weighed and then placed on either side of the ridge. The fresh and dry weights of replicate subsamples were determined and the dry weights of the experimental samples then calculated. Three speci-

mens of P. scaber or O. asellus were placed in each of 10 replicate chambers for 48 h at room temperature, after which the leaf remains were dried to constant weight and consumption of each type of litter was calculated.

Preparation of leaf and faecal substrates

To obtain a series of faecal samples sub-cultures of 200-300 of each species ofisopod were kept in 35 cm diameter 15 cm deep plastic bowls, lined with a 3-4 cm deep base of moist plaster of Paris, covered with a sheet of perforated polyethe- lene and containing an excess of rehydrated B. pendula leaves. A replicate sample of leaves was placed in a control sub-culture bowl without any isopods. After 48 h the faeces were separated from leaf remains and animals by sieving through a 2.5 mm diameter mesh nylon gauze. The faeces were then transferred to a sterile plastic petri dish lined with a piece of sterile glass fibre filter paper that had been soaked with Betula leaf litter leachate. This leachate was made by stirring 20 g of well-decayed and disintegrating B. pendula leaf litter in 100 ml of sterile distilled water for 10 rain and then removing larger particules by filtration through a coarse filter. This was intended to make the mi- crobial propagules that would normally recolonize the faeces or leaves, available during storage. Faeces were spread evenly over the moistened glass fibre disk and the petri dish sealed with 'Parafilm' and stored at 18~ and 100% relative humidity for from 2 to 125 days. The total duration of the experiment would ideally have been until the leaves and faeces had completely decomposed. However as this would take several years they were terminated when CO2 output from the control leaves became so low that it was undetectable. In the experiment with freshly fallen leaves this was after 85 days and in the experiment with previously decayed leaves after 125 days. Samples of un- eaten leaves from the control sub-culture bowls were treated in the same way. Isopods were returned to the sub-culture bowls with fresh supplies of food after the remains of any dead animals had been removed to reduce contamination by carrion feeding.

After samples had been incubated for the required length of time they were removed and sub-sampled for the following analyses:

Microbial metabolism

The rates of total aerobic catabolism due to the combined metabolic activities of all the micro-organisms present in the faecal and leaf samples were monitored by measuring rates of COz output from weighed samples incubated in sealed Conway units. These consisted of a 50 mm diameter 30 mm deep outer chamber with 5 mm wide walls contain- ing an inner glass vial 20 mm in diameter x 20 mm deep, and a lining of glass fibre filter paper moistened with 0.25 ml distilled water on top of which the sample was placed. 3 ml of 0.05 N KOH was pipetted into the inner vial and the unit sealed and incubated for 48 h at 18~ in darkness. Replicate units without either faeces or leaves were used as controls. CO2 output was estimated by back- titration against 0.01 N HC1 using phenolphthalein plus thymolphthalein indicators after precipitating carbonate with barium chloride. The dry weight of substrates was measured and results expressed as CO2 evolved per g 1 dry weight of substrate day- 1.

Moisture content

5 replicate 2(~30 mg sub-samples of each experimental sub- strate were weighed to 0.1 rag, dried to constant weight and reweighed to determine moisture content at the end of the aging periods.

Microbial density

A known weight of faecal or leaf material was finely ground using a sterilized pestle and mortar and suspended in 8 ml of sterile distilled water, to form the base suspension for dilution plate enumeration of viable fungal and bacterial propagules. These were cultured on Rose Bengal and nu- trient agar plates respectively at 18 ~ C for 10 days before counting.

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A bioassay was used to obtain a gross index of overall microbial inhibitor activity in the samples. The technique gives an indication of the combined effects of all metabolic inhibitors of both microbial and plant origin. A suspension 8- of Escherichia coli B was made by harvesting a 24 h culture and suspending it in 0.2% glucose salt solution at a density of 108 cells ml- 1 (Turner and Taha 1984). Particulate mate- rial was removed from a suspension of 100 mg faeces or ~ 6-

o~ leaves in 10 ml of distilled water by centrifugation. 2.0 ml of the supernatant fluid was suspended with 1.0 ml of the E. coli suspension and oxygen consumption measured -~ 20 min later using a Clarke oxygen electrode. Controls con-

4- sisted of 2.0 ml of 0.05 M, phosphate buffer of pH 6.8, incu- 2 bated with 1.0 ml of the E. coli suspension under the same conditions as for the experimental supernatants. Results for oxygen consumption by the test suspensions were ex- a pressed as a percentage of the oxygen consumed by the ~ 2- controls. ~"

The total amino acid (plus ammonium) content of the supernatant solutions, was analysed, using the ninhydrin method (Yem and Cocking 1955) and the availability of 0 reducing sugars by Spiro's modification of the Nelson-So- mogyi copper reduction method (Spiro 1966).

Results

Microbial metabolism

When freshly fallen B. pendula litter was fed to cultures of A. vulgare and O. asellus CO2 output from the faeces of both species was significantly higher than from the intact leaves during the first l0 days of the experiment (Fig. I a), but as in the experiments conducted by Van der Drift and Witkamp (1960) the difference between faecal and intact leaf substrates decreased until they were at very similar levels 3 weeks after egestion. Averaging results from the two species of isopod, the difference in metabolic rate be- tween faeces and leaves is indicated by shading in Fig. J b.

Graphical summation of this shaded area shows that over the whole 85 day period of this experiment CO2 output from the faeces was 63 ml g- 1 dry wt greater than for the intact leaves. This is equivalent to 91 mg of organic material oxidized per gram of substrate. Thus, the stimulation of microbial activity resulting from comminution and passage through the alimentary canals of isopods resulted in the

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Fig. l a, b. Microbial respiration rates on intact freshly fallen B. pendula leaves and in is�9 faeces, a With is�9 species shown separately (means_+l S.E.s); �9 - � 9 A. vulgare faeces, �9 ..... �9 0. asellus faeces, o - - � 9 intact leaves, b With is�9 results summa- rized and shaded areas indicating the extent to which microbial respiration was stimulated in the faeces; �9 ..... �9 is�9 faeces, . - - . intact leaves

decomposition of an additional 91 mg g-1 faeces, that is 9.1% of this comminuted B. pendula leaf litter during an 85 day period at 18 ~ C. This was mostly due to the burst of microbial activity within the first three weeks after eges- tion.

A superficially similar pattern was observed in the de- composition of faeces of A. vulgare and P. scaber fed de- cayed B. pendula litter (Fig. 2a). However the rates of CO2 output were substantially lower than from faeces derived from freshly fallen litter. Another very important difference is that the microbial metabolism in the intact leaves which had already undergone a substantial amount of microbial decay, was also significantly stimulated during the first three weeks of the experiment (Fig. 2b). This is probably

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Fig. 3a, b. Densities of a fungal propagules in A - - A is�9 faeces and o - - o leaf litter, and b viable bacteria cells in freshly fallen B. penduala leaf litter, intact and in is�9 faeces, s - - - s A. vulgate faeces, �9 ..... �9 O. asellus faeces, �9 �9 intact leaf litter

the result of disturbance stimulating micro-organisms al- ready present and active in and on the leaves. (Macfadyen 1971). F r o m the da ta in Fig. 2b we estimate that for every 1 g of faeces produced from leaf litter eaten by the i s �9 only 21 mg g-~ faeces ( = 2 . 1 % ) was subsequently metabo- lized as a result of enhanced microbial actibity.

Microbial propagule densities

In the field where faecal pellets are egested in shelter sites and amongst the leaf litter, an impor tan t component of the faunal-microbe interactions could be the dispersal o f microbial propagules to fresh substrates. I t was therefore of interest to observe how the numbers of microbial p ropa- gules in the leaf substrate were affected by it being commi-

nuted and par t ly digested by the is �9 During the first 50 days after egestion there are on average 3.2 x as many fungal propagules in the faeces as in the intact freshly fallen litter, and throughout the whole 85 day per iod there are on average 171 • for A. vulgate, and 810 x for O. asellus more bacteria in the faeces than in the intact leaves (Fig. 3 a, b) .

The increase in fungal propagules in faeces derived from decayed leaves was not so consistent (Fig. 4a) but on aver- age slightly higher, 4.2 • more than in intact leaves, than in the faeces derived from freshly fallen litter. However the densities of bacteria are consistently at least an order of magni tude greater in the faeces than in the leaf foods (Fig. 4b) (40x greater for A. vulgare faeces and 28 x greater than in intact leaves for O. asellus faeces)�9

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Age (days) Fig. 4a, b. Densities of a fungal propagules in A - - A isopod faeces and o - - o leaf litter, and b viable bacterial cells on decayed B. pendula leaf litter, intact and in isopod faeces, - - - - m A. vulgare faeces, �9 ..... �9 P. scaber faeces, o - - o leaf litter

Table 1. Effect of trituration on colonization of Betula litter by aerobic bacteria

Sample Viable cells mg ~ f. wt.

Decayed Betula litter 6.2 x 10'* Triturated a decayed Betula litter 1.8 x 105 Faeces from Oniscus asellus a feeding 8.9 X 1 0 6

on decayed Betula litter

" Samples were 36 h old

In order to investigate whether the increase in numbers of bacteria could be a t t r ibuted to the mechanical fragmen- tat ion of the litter by isopods, a compar ison was made of the numbers of aerobic bacteria in a) intact decayed leaves, b) decayed leaves that were mechanical ly f ragmented by grinding in a sterilized pestle and mor ta r to fragments of a size comparable with those in i sopod faecal pellets, and c) in leaves that had been c o � 9 by isopods and egested as faeces. The results (Table 1), indicate that the mechanical f ragmenta t ion did increase numbers of bacteria approximate ly 3-fold but that O. asellus faeces at a compa- rable time after f ragmenta t ion (36 h) contained over 144 x more bacteria than the intact leaves.

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Table 2. Densities of viable aerobic bacteria in the food, gut con- tents and faeces of Oniscus asellus fed B. pendula litter in different states of decay. Data represent numbers of cells g- t substrate

Substrate Food

Freshly fallen Decayed leaves leaves

Litter 3.0 x 10 3 4.3 x 10 3 Hindgut contents 5.0 x 10 5 7.5 x 10 4 Faeces 10 h after egestion 1.0 x 10 5 8.9 x 10 6

Table 3. Effect of leachate from Armadillidium vulgate faeces and Betula litter on oxygen consumption by Escherichia coli (means 4-1 S.E.)

Sample age Sample (days)

A. vulgare Decayed Freshly dead faeces Betula Betula

2 9 1 + 9 a 114__.11 86_+8 21 96+3 73___8 57_+7 50 88_+6 77_+9 63_+6

a Oxygen consumption by E. coli in presence of leachate is ex- pressed as a percentage of the control value of 10.1 nmole O2 ml- lmin -1, at 30 ~ C

Clearly something other than simple f ragmenta t ion o f tissues in the leaves st imulated the reproduct ion of bacteria during, or soon after, passage through the al imentary sys- tems of isopods. To determine more precisely when this increase occurs samples were taken from within the hindgut of O. asellus which was dissected out using sterile instru- ments. The results (Table 2) indicate that the number o f bacteria increased by 17 x within the hindgut of animals fed decayed B. pendu la leaves and up to 2070 x in recently egested faeces. In animals fed freshly fallen litter the numbers of bacteria increased by 167 x during passage through the gut but decreased slightly from this peak in recently egested faeces.

These results suggest that the a l imentary canal is a very suitable environment for mult ipl icat ion of the bacteria in- gested with the food and/or that it contains a high density reservoir of microorganisms which invade the food as it is passing through. Evidence to suppor t the suggestion that mater ial might be inoculated with certain species o f bacteria during passage through the gut was obtained from quali ta- tive analysis of the bacterial popula t ions which showed that a species of C y t o p h a g a not found at all in the food consti- tuted approximate ly 10% of the bacterial popula t ion in the faeces.

Chemica l analyses

Given that physical f ragmenta t ion alone could not explain the increased numbers of micro-organisms in the faeces, prel iminary observations of chemical changes in the sub- strata were made. I t was found that levels o f respiratory inhibi tors of E. coli are generally higher in the decayed, and even higher in the freshly fallen leaf lit ter than in the faeces of A. vulgare (Table 3). This assay does not distin- guish between inhibitors of p lant origin such as polyphen-

602

ols, which may acocunt for the higher levels of inhibition in the freshly fallen litter, and inhibitors of microbial origin, which could account for the 21 and 50 day samples having more of an inhibitory effect than the 2 day old ones.

Analyses of 21 and 50 day leaf samples showed that total amino acids had decreased to undetectable levels, whereas 1.2 4- 0.4 and 0.9 +_ 0.2 gg leucine equivalents rag- a fresh weight of faeces were found in the 21 and 50 day A. vulgare faecal samples respectively. This suggests that the increased density of microbes in the faeces leads to more efficient retention of nitrogen in comminuted litter.

Results for the reducing sugar analyses did not show any consistently significant differences between faecal and leaf substrates but did indicate that freshly fallen leaves contained more (0.96-t- 0.13 g, glucose equivalents rag- 1 fresh weight) than decayed leaves (0.63+0.20 g glucose equivalents mg- 1) which could partly account for the high- er rates of microbial metabolism observed on fresh litter (Fig. 1) than on decayed litter (Fig. 2).

Discuss ion

In a critical review of the effects of soil fauna on the activi- ties of the soil microflora Satchell (1974) summarized the view, then widely accepted, in the statement that " the main effect of arthropods is one of comminution, exposing a greater surface area to microbial attack". I f limited surface area for colonization is the primary factor limiting micro- bial activity then it can be predicted that 1) microbial activi- ty will increase in proportion to the increase in surface area, 2) the increase in activity will be the same regardless of the initial condition of the leaf substrate, and 3) the enhanced activity should persist as long as the increased surface area remains available.

Non of these predictions are supported by the above data. Firstly during neither experiment were mean levels of CO2 output throughout the experiment consistently en- hanced by as much as the surface area in the faeces had been increased (3 x ); secondly the effect was much more pronounced in freshly fallen litter than in decayed leaves and thirdly the stimulation lasted in both experiment for less than three weeks, but there was no evidence of a decline in surface area. Clearly these observations do not support the hypothesis that the increase in surface area is primarily responsible for increased microbial activity in the faeces.

The results in Fig. 1 and 2 do give an opportunity to compare the indirect contribution isopods make by enhanc- ing microbial metabolic activity as a result of the total phys- ical and chemical changes they make to the leaf substrate, with the direct contribution that they make to decomposi- tion processes by virtue of their own carbon metabolism. When the food consists of freshly fallen B. pendula leaves, on average 18.1% of ingested material is assimilated by P. scaber and 81.9% is egested (Hassall and Rushton 1982). Of the 181 mg g-1 assimilated, only 16.6% is channelled into production of isopod tissue (Hassall and Sutton 1978), so 83.4% is metabolized and eventually respired as CO2. Thus the direct contribution made by the isopod to the min- eralization of 1 g leaf litter is 151 mg lost as CO2 due to the isopods own metabolism.

Of the 819 mg g-1 of food egested as faeces 9.1% is lost as a result of enhanced microbial respiration, that is 75 mg are mineralized as a result of the isopods indirect effects on microbial metabolism (Fig. 5a).

181 mg ~1o~ assimilate

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microbial respiration Contribution

Fig. 5. A comparison of the direct and indirect contributions made by isopods to decomposition processes

Table 4. Consumption rates of terrestrial isopods given a choice of Betula litter in different states of decay

Isopod species State of decay

Decayed Freshly t.values dead

Porcellio scaber 2.26 0.42 t = 6. t 7 _+0.38 +0.37 P<0 .00 t

Oniseus asellus 3.55 1.15 t = 2.34 4-1.90 -+0.60 P<0.05

Consumption rates in mg dry wt indiv- 1 day- 1

When given a choice, all terrestrial isopods yet studied, have been shown to selectively ingest decayed rather than freshly dead tree leaf litter (Hassall and Rushton 1984). Table 4 shows the results of the simple two way choice experiments which illustrate how strongly both P. scaber and O. asellus prefer to eat decaying rather than freshly fallen B. pendula. On the decayed substrate (Fig. 5b) the comparison between direct and indirect contributions is even more striking with only 17.5 mg g-1 mineralized due to the enhancement of microbial metabolism but 8 x as much metabolized by the animals themselves. I f some of the faeces were to be recycled, then the overall indirect effect might be larger.

In microcosm experiments described by Hanlon and An- derson (1980) Oniscus asellus was able to recycle its faeces and the stimulated microbial activity persisted at some den- sities for as long as 40 days. Only one g of food was initially provided in these microcosms so there was probably consid- erable recycling of the faeces over the 40 day period. When the animals are feeding on previously decayed litter in the field, it is likely that coprophagy accounts for less than 8% of total consumption (Hassall and Rushton 1982). Thus the stimulatory effects in the field would probably be some- what greater than those observed here but less than those observed in the microcosm experiments described by Han- lon and Anderson (1980).

If f ragmentat ion and the chemical changes resulting from a single passage through the al imentary canal have so limited an effect on the subsequent b reakdown of the litter how is it possible to account for the dramat ic inhibi- tion of decomposi t ion when the soil fauna is experimental ly excluded from leaf lit ter?

Other physical activities of the animals might be impor- tant. I f as seems likely, the general biostasis in the soil litter system is caused pr imari ly by lack of available nutr ient the movement of animals within the litter soil matr ix could be an impor tan t physical factor a) in moving litter from the surface to be deposi ted as faeces in shelter sites with higher relative humidi ty and b) in dispersing the microbial propagules to new sites where the substrate may be more suitable. The filter paper on which the faeces were placed in this experiment is not representat ive of field condit ions and thus may have led to considerabe underes t imat ion of the indirect effect of the isopods resulting f rom their dis- persal of microbial spores. This is especially likely as the compar ison of viable microbial propagule densities in leaves and faeces showed that for the bacter ia part icular ly, passage through the guts of the isopods led to substantial increases in density as found for Oniscus asellus by Ineson and Ander - son (1985).

The reason for these increases in the microbial popula- tions are not immediate ly apparen t and may be related to chemical changes such as in p H or C : N rat io which were not measured in this study. The leachate from faeces inhib- ited oxygen consumpt ion by E. coli to a smaller extent than that from intact leaves which may indicate that some inhibi- tory plant chemicals such as polyphenols are reduced as the mater ial passes through the a l imentary canal. There were higher levels of amino acids in older samples o f faeces than in the intact leaves which may be impor tan t for the continued replication of the microbes. Even if this is not so, the persistence of higher levels of amino acids in the faeces than in the leaves is still interesting in that it suggests that faeces retain nitrogen within the litter system better than do the unfragmented leaves.

A further possible indirect effect of the fauna on the microf lora is due to their grazing on the fungal hyphae. The impor tance of the mesofauna in this respect has been demonst ra ted e.g. by Parkinson et al. (1979), Mitchell and Parkinson (1976), and Han lon and Anderson (1979), while Hanlon and Anderson (1980) clearly show that Oniscus asellus and Glomeris marginatus Villers reduce the standing crop of fungi on fragmented and ground oak litter while increasing the densities of bacterial populat ions.

In conclusion it is clear that leaf litter eaten and egested by isopods, differs both physically and chemically from in- tact leaves and that the microf lora is al tered in both density and species composi t ion by passage through their al imenta- ry system. However, as in the studies of Nicholson et al. (1966) and Webb (1977) on the faeces of millepedes, we find no evidence that these changes significantly accelerate the decomposi t ion of faeces, compared with intact leaves, in the field. Thus the most impor tan t contr ibut ion these a r th ropod macrodecomposers make to the decomposi t ion of leaf litter may be in physically t ranspor t ing it to more humid posit ions lower in the profile. By foraging in surface litter layers, usually at night, and then t ranspor t ing and deposi t ing 80% or more of what they have eaten as faeces in their sheltered resting sites, they make a visually obvious contr ibut ion to litter d isappearance but this does not neces-

603

sarily accelerate the subsequent microbial metabol ism other than as a result of moving the substrate into more favour- able microcl imatic conditions.

Acknowledgements. We are very grateful to Mrs. Jill Debbage for technical assistance with the microbiological and chemical analyses, to Dr. B. Ausmus for discussion of data and to Drs. I. and L. Thompson for comments on the manuscript. We also thank several anonymous referees who suggested ways of clarifying an earlier draft of this paper.

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Received December 22, 1986