DECOMPOSITION AND COLONISATION BY INVERTEBRATES OF NATIVE AND EXOTIC LEAF MATERIAL IN A SMALL STREAM IN NEW ENGLAND (AUSTRALIA) R. W. J. PIDGEON & S. C. CAIRNS Division of Ecology, Department of Zoology, University of New England, Armidale, N.S.W., 235I, Australia Received April 8, 1980 Keywords: Streams, allochthonous detritus, riparian vegetation, decomposition, colonisation, benthic invertebrates
Abstract In many parts of south-eastern Australia, native riparian vegetation has been cleared and exotic willows planted. In order to evaluate some of the possible effects of this practice, the decomposition and colonisation by invertebrates of the leaves of three native plant species along with those of willow were examined. Decomposition of leaves of the willow Salix babylonica L. and the indigenous macrophyte Myriophyllum propinquum A. Cunn. was much faster than for leaves of the indigenous trees Eucalyptus blakelyi Maiden and Casuarina cunninghamiana Miq. Both macroinvertebrates and current were found to have a significant influence upon decomposition. The pattern of preferential colonisation suggested that plant detritus represented a primary food source for invertebrates and not simply a refuge. Colonisation was found to be a function of the stage of decomposition, regardless of plant species. The lower temporal availability of willow leaves compared to the native evergreen tree leaves appears to be insufficient to enhance the production of the benthic macroinvertebrates.
minimum level of microbial colonisation ('conditioning') has taken place. Differences among plant species in the rates of conditioning, rates of breakdown and, as a consequence, rates a colonisation by invertebrates have been
Introduction
demonstrated (Petersen & Cummins, 1974). Reice (1974, 1977) has also shown differences in the breakdown rates resulting from differences in both the size of leaf aggregations and the substrate composition (and hence composition of benthic fauna). The consequence for benthic fauna of such variation in breakdown rates is an increase in the temporal availability of food, particularly when most leaf ipput occurs in a short period of time such as autumn in many northern hemisphere locations (Petersen & Cummins, 1974). However, where the riparian vegetation is evergreen and leaf fall is continuous such advantages of tree diversity and substrate patchiness are probably of much less significance. Further, the life cycles of benthic detritivores are less likely to be adapted to optimising the utilisation of seasonally abundant fallen leaves as suggested for some northern hardwood forest streams (Hynes,
Stream ecosystems are currently regarded as heterotrophic detritus-based systems which are dependent upon allochthonous organic matter for the majority of energy inputs. Allochthonous detritus has also been shown to be extremely important to the trophic dynamics of the benthic fauna in streams (Hynes, 1970; Cummins, 1974; Mann, 1975; Wetzel, 1975; Anderson & Sedell, 1979). Riparian trees, through their input of allochthonous detritus and the reduction of autochthonous primary production by shading streams, can have a considerable influence on energy flow patterns, particularly of small streams. Because of this many workers have examined the breakdown of terrestrial tree leaves in streams and their utilisation by benthic invertebrates. This work has been extensively reviewed by Anderson & Sedell (979). Invertebrates colonise leaf material in streams after a
I970; Cummins, 974). The natural riparian vegetation in Australia consists almost entirely of evergreen angiosperms. Their pattern of litter fall is similar to northern hemisphere gymnosperms in being continuous but with a maximum in spring and summer. The magnitude of litter fall in Australian forests is similar to many northern hemisphere forests but the litter differs in composition by containing a larger proportion of branches and bark (Maggs &Pearson, 1977; Blackburn & Petr, 1979). The importance of this detritus to Australian stream biota has been demonstrated by selective colonisation of leaves and bark by some benthic invertebrates in a forested mountain stream in Victoria (Blackburn & Petr, op. cit.). In agricultural areas of south-eastern Australia the natural riparian vegetation has been almost totally removed in many places and frequently exotic deciduous willows II3
Hydrobiologia 77, 113-127 (1981).
ooi8-8158/81/o772-o113$o3.oo.
© Dr. W. Junk b.v. Publishers, The Hague. Printed in the Netherlands.
(Salix spp.) have been planted along these streams. Such qualitative and quantitative changes in the allochthonous inputs of these streams could well have adverse consequences for the indigenous stream biota. In a study of energy flow in a small stream under different forms of riparian vegetation Pidgeon (1978) found that the production of the benthic fauna was directly related to the level of autochthonous primary production. Further, it appeared that increased inputs of particulate organic matter from exotic willows (Salix spp.) did not provide an alternative fod source for the benthic fauna when autochthonous primary production was reduced through shading. This suggested that willow leaves were either unpalatable or in some other way unavailable to the indigenous benthic fauna. Following upon these findings the aim of the present study was to examine the decomposition and colonisation of willow leaves under these conditions and to make a comparison with these processes for some indigenous sources of both allochthonous and autochthonous detritus.
nated by the perennials Myriophyllum propinquum A. Cunn. and Cladophoraspp., was well developed in this section of the stream except in the deeper parts of pools and where willows cause intense shading. The density of the aquatic vegetation is greatly affected by spates but it could almost completely cover the stream bed after prolonged dry periods. These macrophytes are a significant source of detritus in this stream. In 1974-1975 the annual gross primary production (macrophytes + periphyton) in the experimental pool was 19.0 x I 3 kJ m- 2 , while the annual input of terrestrial plant material was .2 x 103 kJ m- 2 (Pidgeon, 1978). The benthic fauna was numerically dominated by fine particle feeders: oligochaetes, bivalve molluscs (Corbiculina sp.) and caenid mayflies (Tasmanocoenisscotti Till.). Pidgeon (1978) found a mean annual density of benthic fauna of 14 x 104 m- 2 and mean annual biomass of 9.o3 g ash-free dry weight m- 2 in the experimental pool.
Methods Study Area The study was carried out in Commissioners Waters, a small third-order tributary of the Macleay River system on the New England tablelands of northern N.S.W., Australia (20°31'S, 151 39'E). Typical of many streams in this region, most of the catchment of this stream is cleared grazing land. The original riparian trees (Eucalyptus spp.) have largely been cleared and exotic willows, most commonly Salix babylonica L. and S. rubens Schrank, have been planted in many places along the stream. However, at the study site the original riparian vegetation (Eucalyptus blakelyi Maiden and E. viminalis Labill) remained. This section of the stream was at an altitude of 950 m and consisted of a series of long shallow sandy-bottomed pools 5I5 m wide and 0.2 m deep separated by very short riffles I-2 m wide. The experiment was conducted in one such pool. Discharge of the stream at normal levels was o.1-0.2 m3 sec-' (Pidgeon, 1978) and during the present study water velocity in the experimental pool was 1.4-8.3 cm sec The stream was eutrophic and apparently unpolluted. Mean water temperatures ranged from 8C in winter to 23°C in summer (Pidgeon, 1978) while pH was in the range 7.3-9.2 (Baker, 1976). The bottom substrate of the experimental pool consisted mainly of medium to coarse sand with some gravel and pebbles. Aquatic vegetation, domi114
The plant material used in the present study consisted of preabscission leaves of the trees S. babylonica, E. blakelyi and Casuarinacunninghamiana Miq. and whole stems plus leaves of M. propinquum collected from the stream area in September 1978. C. cunninghamiana was included because it is the dominant riparian tree species at altitudes below 9oo m. The tree leaf material was oven dried at 400 C to constant weight. This procedure could not be carried out with M. propinquum because of the fragmentation of the material during handling when dry. Dry weight of this material was estimated from that of IO samples, each of 20 g wet weight. Further, the M. propinquum had to be killed to prevent continued growth after submersion. This was done by exposing it to a temperature of go°C for one hour. Because of the small size of most of the material the use of leaf packs was impractical. However, it was desired to simulate natural conditions as much as possible. For this purpose the material was enclosed in nylon bags measuring IO cm x 20 cm with a o mm mesh. This gave access to the largest invertebrates and allowed the current to act on the material causing loss through abrasion and transport. The size of leaf aggregations has been shown to have a considerable affect on rates of breakdown of leaf packs (Reice, 1974; Benfield et al., 1979). It has also been sug-
gested that colonisable leaf area can be a more important factor than total dry weight in determining the density of
invertebrate populations on decomposing leaves (Davis & Winterbourn, I977). With this in mind and because the plant material used in the present study differed in shape and density, the bags were filled with equivalent volumes rather than equivalent weights of material. This resulted in different initial dry weights for each species: S. babylonica (6.9 g), E. blakelyi (Io.o g), C. cunninghamiana(Io.o g), M. propinquum (4.o0 g). Animals will colonise most suitable structures on a stream bed either for shelter or grazing on Aufwuchs. In order to determine whether the observed colonisation of plant material was simply a result of this effect or whether it was influenced by the type of material and rate of decomposition, extra bags were filled with strips (5 cm x cm) of black plastic (PVC) sheeting. By providing an approximately equivalent surface area for colonisation these bags served as initial controls.
Forty bags were used for each of the five different material types. The bags were numbered and attached at randomised locations to one of five Io m lengths of fine steel wire. The wires were then tethered in the centre of the pool in rows i m apart and parallel to the banks on 8 September 1978. Six to eight bags of each type were sampled at intervals of I, 2, 4, 8 and 6 weeks after immersion. Each bag was gently lifted from the substrate with a 0.25 mm mesh sieve. In the laboratory the contents of the bags and any material retained on the sieve were placed onto a .o mm mesh sieve and gently washed, with the filtrate being passed through a 0.25 mm mesh sieve. Animals were then removed from the plant material on both sieves by hand sorting at Iox under a dissecting microscope. The plant material from both sieve fractions was then combined and oven dried at 40°C to constant weight. Animals from the
C Ankvin-irn
MAdnrnninnllm
80
40
E
E Ca
0
E a,
3: >1 _0
F l nC l i
r r*ni
b,.~i;~
80
40
n u 0
1
2
4
8
16
01
2
4
8
16
Time (weeks) Fig. . Mean (± standard deviation) weight loss by four different
species of plant material from coarse mesh (o) and fine mesh () litter bags. 115
two sieve fractions of the samples were identified and counted separately. In order to evaluate the role of macroinvertebrates and current in the breakdown processes of detritus, samples of dried S. babylonica, E. blakelyi and wet M. propinquum, the same weight as in the coarse (o mm) mesh bags, were enclosed in nylon bags with a mesh of.0.15 mm. These bags effectively excluded all macroinvertebrates. Ten such bags were used for each of three different plant species. These were placed in the stream on a separate three wire grid, immediately downstream from the coarse mesh bags. Five bags of each species were removed after 4 and 16 weeks. The fauna in the substrate under the litter bags was sampled at 4, 8 and 6 weeks after immersion of the bags. Ten core samples, 177 cm2 in area and 5 cm deep, were taken on each occasion from random coordinates within the grid of bags. Animals were removed by elutriation onto .o mm and 0.25 mm mesh sieves and the two fractions counted separately. To detect any qualitative changes in the plant material contained in the litter bags, measurements were made of the relative ash, organic nitrogen and phosphorus contents of the pooled material of each species collected at each sample time. To determine ash contents, 0.4-0.5 g of milled and homogenized dry material was ignited for 24 h at 450o°C in a Gallenkamp muffle furnace. Nitrogen contents were determined by a micro-Kjeldahl procedure (Beutz, 974) using samples of 0.4-0.5 g of prepared material with colorimetric determinations being made with a Technicon auto-analyzer. For phosphorus contents, 0o.4-
o.5 g of prepared material was digested with a mixture of nitric, perchloric and sulphuric acids (Walkeley, 1942). Colorimetric determinations were made by the method of Williams & Twine (1967) using a Technicon auto-analyzer. All determinations were made on two sub-samples of each type of prepared material. Where values differed by > 5% a third sub-sample was taken and the procedure repeated.
Results Weight Loss of Detritus Changes in the dry weights of the four different plant species are shown in Fig. . Weight loss of M. propinquumand S. babylonica from the coarse mesh bags was much more rapid than that of E. blakelyi and C. cunninghamiana.M. propinquum and S. babylonica had declined to 5% and I2%, respectively, of their initial weights by 4 weeks and had completely disappeared by 8 weeks. In contrast, with E. blakelyi and C. cunninghamianathere was still 58% and 43%, respectively, remaining after 8 weeks and I4% and 9%, respectively, remaining after 6 weeks. The exponential decay model used by Petersen & Cummins (1974) and others to describe the decomposition of leaves in aquatic conditions did not adequately describe the weight loss pattern of the slower decomposing species in the present study. For this reason processing coefficients (-k) (Petersen & Cummins, op. cit.) could not be used to compare breakdown rates of different species. The breakdown of E. blakelyi (Fig. ) showed three distinct stages.
Table . Changes with decomposition in the relative ash contents (% dry weight) of the four types of plant material. The values given in brackets are for the fine mesh bags. Weeks after immersion
M. propinquzu
0
27.2
1
39.1
2
48.5
4
55.6
8
-
(74.1)
-
(43.8)
5.3
12.1
(59.3)
S. babylonica
7.2
12.0
10.2
26.0 (7.3)
E. blakelyi
3.3
5.0
4.8
5.6 (4.4)
C. cunninghamiana
5.7
3.5
3.3
3.6
16
(8.7)
5.3
11.2
There was an initial rapid weight loss in the first few days; the result of leaching of soluble compounds. This was followed by a much slower, linear, rate of loss until about 8 weeks. Since there was little fragmentation during this period, it was probably a period of gradual breakdown of epidermal and internal tissue structure. The third stage was one of a more rapid rate of loss resulting from fragmentation by both current and animals. These same three stages were also found by Blackburn & Petr (1979) for leaves of Eucalyptus regnans, Nothofagus sp. and Quercus sp. during winter. There was a marked difference in the appearance of E.
blakelyi leaves from the two mesh sizes after 16 weeks (Fig. 2). In the coarse mesh bags most of the leaf tissue had disappeared leaving only the skeletal framework. In the fine mesh bags, which excluded animals and probably also reduced water currents, the leaves were still intact at 6 weeks and had a similar appearance to leaves in the coarse mesh bags after only 8 weeks. These three distinct stages were not all evident in the breakdown of the other species examined. If present in M. propinquum and S. babylonica, these stages would probably have been masked by the very rapid breakdown of these species. While C. cunninghamianashowed the initial
Fig. 2. Photograph showing the difference in appearance of E. blakelyi leaves after 8 and 6 weeks and between coarse and fine mesh litter bags at 16 weeks. II7
leaching phase, subsequent weight loss was almost linear suggesting that tissue breakdown and fragmentation occurred concurrently. The needle-like leaves of this species did not show any marked change in external appearance, even after 16 weeks, so that erosion of leaf surface tissue was not a factor in its breakdown. Rather, the leaves fragmented into shorter lengths as breakdown occurred. For comparison of breakdown rates of different plant species, initial half-lives (Howard-Williams & Davies, 1979) were estimated from Fig. . In the coarse mesh bags these were 7 days for both M. propinquum and S. babyloca and 45 and 66 days, respectively, for C. cunninghamiana and E. blakelyi. Weight loss from the fine mesh bags was considerably slower than from the coarse mesh bags. The initial half-lives of M. propinquum and S. babylonicain fine mesh bags were 5 and 3.7 times longer (35 and 26 days, respectively) than in the coarse mesh bags (7 days). Even after 16 weeks there was still 26% and 8%, respectively, of these species remaining in the fine mesh bags. ForE. blakelyi there was no difference in weight loss between coarse and fine mesh bags after 4 weeks; but there was a marked difference after I6 weeks, with 40% remaining in the fine mesh bags and only I4% in the coarse mesh bags. The initial half-life of E. blakelyi leaves in fine mesh bags (go days) was only 1.4 times that in coarse mesh bags. Chemical Changes in Plant Material Changes in the relative ash contents of the four plant species are shown in Table I. As decomposition proceeded so the relative ash contents of M. propinquum, S. babylonica and E. blakelyi increased. In C. cunninghamiana,however, there was an initial decrease in ash content during the first two weeks followed by an increase. The slower rate of decomposition of C. cunninghamianaand E. blakelyi resulted in a slower increase in their relative ash contents. The initial ash content of M. propinquum (27.2% of dry weight) was much higher than that of the three terrestrial species. A similar high ash content (i7%) has also been reported for another macrophyte, Potamogeton pectinatus (HowardWilliams & Davies, 979). The initial ash contents of the three terrestrial species were similar to values reported for terrestrial species by Mathews & Kowalczewski (1969) and Blackburn & Petr (1979). However, the increases in ash content with decomposition found by these workers were much less than those found in the present study. This may be a result of later stages of decomposition being observed in the present study. The cause of the increase in ash content during decom-
position is not clear. Mathews & Kowalczewski (i969) attributed some of the fluctuation in ash content to mineral particles introduced into the material by the current and Howard-Williams & Davies (I979) attributed the large increase in ash content of Potamogeton detritus to a possible accumulation of mollusc shells. Whilst some contamination of plant material by fine mineral particles not removed by washing no doubt occurred in the present study, such increases in ash content would also occur if the more refractory components of the plant tissue have a higher mineral content. Initial phosphorus and nitrogen contents are shown in Table 2 and the loss of these elements with decomposition is shown in Fig. 3. The patterns of loss of these elements from the fine mesh bags were similar to those from the coarse mesh bags with the exception, of course, that loss occurred at a slower rate with the slower decomposition. In the early stages of decomposition of M. propinquum, E. blakelyi and C. cunninghamiana, phosphorus was lost at a rate faster than that of dry weight loss. This indicated that phosphorus was leached at a faster rate than were the other soluble tissue components. This leaching effect was most pronounced in C. cunninghamianawhere 70% of the initial phosphorus, compared with only 30% of the initial dry weight, disappeared in the first week. The exception was S. babylonica where phosphorus was lost at a rate slower than dry weight loss. In M. propinquum, S. babylonicaand E. blakelyi the initial loss of nitrogen occurred at a rate slower than that of the dry weight loss. This rate of loss increased during the later stages of decomposition. Such a situation has been reported in a number of studies (Kaushik & Hynes, I968; Mathews & Kowalczewski, 969; Iversen, I973; Howarth
Table
2.
Initial phosphorus and nitrogen contents (%dry weight)
of the four types of plant material. Plant material
Phosphorus
Nitrogen
M. propinquwum
0.25
1.95
S. babylonica
0.18
3.96
E. blakeZyi
0.09
1.29
C. cunninghamiana
0.09
1.78
AM nrnninnlm
J.~~UUUYf't"t* U
_
80C
40
0) C
0
E C runninhnminnn
.4-
80 C
40
0 0
1
2
4
8
16
0 1
2
4
8
16
Time (weeks) Fig. 3. Loss of nitrogen (A) and phosphorus (0) from decomposing plant material of four species in coarse mesh (open symbols) and fine mesh bags (solid symbols). Broken line represents loss of dry weight.
& Fisher, 1976; Howard-Williams &Davies, 1979; Blackburn & Petr, 1979) and has been attributed to microbial immobilisation of nitrogen released during decomposition and to the complexing of nitrogen with tannic and other phenolic acids (Suberkropp et al., 1976). The more rapid loss of nitrogen in the later stages of decomposition may indicate the dominant role played by microbes as opposed to that of chemical complexing, since microbial activity decreases during the later stages of decomposition (Saunders, 1976). Nitrogen loss from C. cunninghamiana differed from that of the other species in that during the first four weeks it occurred at a rate similar to that of dry weight loss. Some uptake of nitrogen occurred between 4 and 8 weeks. A more rapid loss then occurred during the later stages of decomposition as with the other species.
Colonisation of Litter Bags The fine mesh litter bags excluded virtually all macroinvertebrates from the plant material. Only two small chironomid larvae were found in the 30 bags examined. In contrast to this, the coarse mesh bags were colonised by large numbers of animals. The percentage composition of the fauna in the substrate and coarse mesh litter bags is shown in Table 3. Colonisation of the bags was rapid, with most taxa being present after I week. All taxa present in the substrate, except for gomphid dragonfly larvae, were found at some stage in the litter bags. Despite the common presence of the taxa there were differences between the bags and substrate in relative abundances. The Ephemeroptera and Tanypodinae consistently comprised a higher proportion of the fauna in the bags than in the substrate. For the 119
Table 3. Percentage composition of the invertebrate fauna in the stream bed and in the coarse mesh litter bags in Commissioners Waters on each of five sampling occasions. Data for bags containing plant material of four species and PVC strips are combined. All insects are larvae or nymphs unless specified. S -stream bed, LB - litter bags. * - denotes species present but comprising less than o.I% of total fauna. WEEKS IN STREAM
2 LB
LB
4
S
16
LB
S
LB
S
LB
0
0
TURBELLARIA
0
0.2
0.1
3.7
OLIGOCHAETA
18.3
16.3
34.3
17.1
43.7
20.4
49.1
2.6
0
0.1
1.1
0.1
2.2
2.3
11.4
1.2
0.3
0.1
0.7
0
0.4
0
*
0
0.1
1.1
0.2
1.2
1.3
0.5
0.2
0.8
0.5
0.5
*
0.7
0.4
1.4
0.1
15.3
19.7
38.6
9.8
14.0
2.4
1.8
27.3
37.2
0
PELECYPODA Corbiculina sp.
GASTROPODA Bulinus sp.
OSTRACODA Ilyodromus sp. COPEPODA Microcyclops
sp.
EPHEMEROPTERA Tasmanocoenis
scotti
Jappa kutera Atalophlebia
spp.
12.3
31.9
18.1
2.6
1.8
2.9
10.2
1.1
40.0
0.7
27.6
5.5
42.1
1.9
27.0
Atalophlebioides sp.
3.0
4.5
0.4
11.8
0.2
2.1
0
1.7
Baetis sp.
3.3
2.5
0.1
1.7
0.6
1.8
0
0.1
(51.3)
(65.7)
(47.2)
(69.7)
(37.5)
(50.9)
(i5.8)
(87.5)
0
0
0.1
0
0.2
0
0.2
0
Psychomyiidae
3.8
3.2
1.8
2.5
2.6
5.8
7.8
4.4
Philorheithridae
0.1
*
0.1
0
0.6
*
2.6
0
Leptoceridae
0
*
0
0
0
0.4
0
0.1
Odontoceridae
*
*
0.1
*
0.1
0.2
0.2
0.3
Hydroptilidae
0
0
0
0
0
2.2
0.3
0.1
(Total Ephemeroptera) ODONATA Gomphidae TRICHOPTERA
DIPTERA Chironominae
10.3
5.9
11.2
4.6
7.1
7.5
4.3
1.2
Tanypodinae
11.5
6.3
0.7
3.9
1.0
2.4
0.6
11.8
Ceratopogonidae
0.6
*
0
0.3
0
*
0
*
Tipulidae
0.9
*
0.7
0
0.9
0
1.6
0
Tabanidae
0.3
0.1
0
0
0
0
0.5
0
Gyrinidae
0.4
0.7
0
0.5
0.1
0.9
0.1
0
Dytiscidae
0.5
*
0.2
0.2
0.3
0.6
0.1
0.1
Helminthidae
0.4
*
0.5
0.1
1.2
0.1
2.8
*
Helminthidae - adults
0.3
*
0.4
0
0
0
0.5
0.1
Hydrophyllidae
0
0
0
0.5
0.6
0.1
*
COLEOPTERA
Table 4. The proportions (%) of invertebrates retained on I.o mm and 0.25 mm mesh sieves in fauna extracted from litter bags and the stream bed from Commissioners Waters. The results are given for chi-square tests carried out on the actual numbers present at each time.
Sample time (weeks after immersion)
4
Sieve mesh
size (mm)
0.25 mm
16
***
Litter
bed
bags
91.6
56.2
mm
8.4
43.8
0.25 mm
78.6
70.2
1.0
21.4
29.8
0.25 mm
78.0
87.7
1.0
22.0
12.3
1.0
8
Stream
mm
mm
x2
504.8 ***
30.5 ***
57.1 ***
Significant at P < 0.001.
Oligochaeta (mostly Tubificidae and Naididae), the opposite was the case. No consistent trends were evident for the other taxa, possibly because of their relatively small numbers. The bags apparently provided a more suitable habitat for active animals such as the Ephemeroptera than for the more sedentary oligochaetes. Among the Ephemeroptera there were marked differences between the relative abundances of different species in the substrate and the bags (Table 3). Atalophlebia spp., Atalophlebioides sp., Baetis sp. constituted a much higher proportion of the Ephemeroptera in the bags than in the substrate. This tended to indicate a preference by these species for large particle detritus as a food source and, perhaps, a refuge. T. scotti was found to be more abundant in the substrate than in the bags at all times except at the last sampling occasion. A similar trend was shown by Jappa kutera Harker, a burrowing mayfly, which initially formed a relatively small proportion of the bag fauna but increased in abundance in the later stages of the study. Both these species feed on very fine study possible reflects an increase in the accumulation of fine particle organic matter in the bags. As well as specific differences in the relative abundances of the animals in the litter bags and substrate there also existed size differences. Measures of these were given by the number of animals retained on the two sieves used in
fauna extraction (Table 4). In spring (September-November) the bags contained a higher proportion of large animals than did the substrate, while in summer (January) there were more large animals in the substrate than in the bags. These proportional differences were all found, using a chi-square test, to be significantly different (P < o.oo ). The seasonal difference that existed in these proportions suggests that in spring some large animals may have used the bags as a pre-emergence refuge as well as a food source. The total number of animals per bag in those containing plant material increased as the material presumably became more palatable through decomposition and microbial activity and then decreased as the available plant material disappeared through fragmentation (Fig. 4 (a)). This process took place over a very short period in the rapidly decomposing M. propinquum and S. babylonica. Peak numbers occurred after 2 weeks, declining rapidly by 4 weeks to a level which remained virtually constant for subsequent samples of apparently empty bags. In contrast, the numbers in the bags of E. blakelyi and C. cunninghamiana increased for 8 weeks and then slowly declined. Numbers in the PVC control bags increased more slowly than in the plant material bags. After 2 weeks the rate of increase in numbers was almost linear. This indicated that the PVC became increasingly a more suitable habitat with increased exposure. Since the PVC did not decompose this I21
Table 5. Analysis of variance comparisons of the number of animals per litter bag type for coarse mesh bags on five sampling occasions. For comparison of means, bag types are ranked in ascending order and designated as M (M. propinquum), S (S. babylonica), E (E. blakelyi), C (C. cunninghamiana), P (black PVC strip) and MS (empty bags). Those underscored by the same line do not differ significantly at the level of P < 0.05 as determined by the Newman-Keuls test (Zar, 1974). Weeks after imersion
F
Ranked litter bag types
1
7.86 ***
P
S
E
C
M
2
3.69 *
P
M
E
C
S
4
17.97 ***
M
P
S
E
C
8
7.96 **
MS
P
E
C
16
13.28 ***
MS
C
E
P
those bags containing plant material were consistently higher than in those containing PVC. From this it would appear that the animals were preferentially colonising the plant material which represented a primary food source and not a refuge and a site for the accumulation of fine detritus and the growth of periphyton. As a measure of the numbers of animals colonising plant material for food rather than refuge, the mean number of animals in the PVC bags was subtracted from the mean number in bags containing plant material for the first four weeks. After
300
co 200
-0 100 co
100
aQ
Significant at P < 0.05 **
Significant at P < 0.01
***
Significant at P < 0.001
must be attributed to an increase in the accumulation of fine particle detritus and the growth of periphyton on the PVC itself. Total numbers of animals per bag were compared for each sampling occasion in order to detect differences in the rates of colonisation of the different materials. A oneway analysis of variance was carried out on the log (N + I) transformed data and a comparison of the mean total numbers of animals per bag was made using a NewmanKeuls test (Zar, I974). The results of these analyses are shown in Table 5. During the first two weeks total numbers in the PVC bags were lower than in bags containing plant material. After 4 weeks numbers in the E. blakelyi and C. cunninghamiana bags were significantly greater than those in the PVC bags and the bags containing the
E z
(b) 60
g)
a)
40
E z 20
0 01
2
4
remaining M. propinquum and S. babylonica. A similar
situation existed after 8 weeks, while after 6 weeks the increase in numbers in the PVC bags and decrease in the E. blakelyi and C. cunninghamiana bags resulted in there be-
ing a significant difference between these three as a group and the empty bags. During the first four weeks the numbers of animals in 122
8
16
Time ( weeks ) Fig. 4. Colonisation by invertebrates of four species of decomposing plant material in coarse mesh litter bags. (a) Mean number of animals per bag. (b) Mean number of animals minus control number per g dry weight of plant material. O C. cunninghamiana * E. blakelyi --PVC strips
A S. babylonica A M. propinquum
this time the numbers in the empty bags were taken as a control. This was done because the accumulated fine detritus and the periphyton in the PVC bags had begun, by 8 weeks, to represent a sufficient food source to attract an increasing number of animals. The total number of animals minus control per gram of plant material is shown in Fig. 4 (b), where the effect of the decomposition rate of plant material on colonisation is shown more clearly. The rapidly decomposing M. propinquum and S. babylonica were colonised at a much faster rate than the more slowly decomposing E. blakelyi and C. cunninghamiana.Also, the number per gram in E. blakelyi and C. cunninghamiana continued to increase throughout the study indicating an increased attractiveness of these materials to the fauna with continued decomposition. However, with continued decomposition and fragmentation a stage is reached where only refractory components of the plant material remain. At this stage the material is no longer attractive to animals. In the present study this stage was reached very quickly in the rapidly decomposing species although this may be an artifact of the very small amount of material remaining. With the two more slowly decomposing species this refractory stage has apparently not been reached by 16 weeks.
Discussion The seasonal timing of the present study contrasted with most northern hemisphere studies which have been carried out during autumn and winter on autumn-shed leaves and with the only other Australian study, that of Blackburn & Petr (1979). This makes comparison with the results of such studies difficult because of the effect on breakdown rates of large differences in temperature between autumnwinter and spring-summer experiments. Some allowance for such temperature effects must therefore be made when comparing results of different studies. Spring was chosen as the starting point for the present study to coincide with the peak litter fall in Australia and to allow for any lifecycle adaptations of the benthic fauna to take advantage of this, such as has been suggested by Hynes (1970) and Cummins (1974) for some northern hemisphere species. This, however, meant that the leaves of S. babylonicawere experimentally introduced at a time of minimal natural input of this species into the stream. There have been few studies comparing breakdown rates in winter and summer. The summer decomposition rate of Carya glabra leaves was found to exceed the
autumn-winter rate by 3.3 times (Petersen & Cummins, 1974) and 4.8 times (Suberkropp et al., 1975), while for Quercus alba leaves an increase of 5.4 times was found by Suberkropp et al. (975). Anderson & Sedell (1979) reported at least a fourfold increase in breakdown of alder leaves between temperatures of60 C and 5°C. At the site of the present study average water temperatures for autumnwinter and spring-summer are 2°C and 22 0C, respectively, (Pidgeon, 1978) giving a temperature difference comparable with theirs. Thus, for comparison of the summer breakdown rates of the present study with winter rates of other studies, a fourfold difference will be assumed possible. On this basis the comparable winter processing rates for C. cunninghamianaand E. blakelyi (half-lives of 4 x 45 = 18o days and 4 x 66 = 264 days, respectively) would place these species in the slow breakdown category of Petersen & Cummins (1974). Winter processing rates for S. babylonica and M. propinquum (half-life 4 x 7 = 28 days) would place these species in the fast breakdown category. These breakdown rates indicate that even the slowest species (E. blakelyi) would be broken down in less than one year. In terrestrial habitats Eucalyptus leaves generally decompose more slowly than leaves of many European broad leaved trees. However, weight losses of up to 97% in one year, similar to those suggested for the present study, have been recorded in moist coastal habitats (Wood, 1974). Blackburn & Petr (I979) found a half-life of approximately 85 days for E. regnans in a Victorian mountain stream during winter(maximum water temperature 8. 5 °C). This was only slightly slower than the summer rates found in the present study for E. blakelyi and indicates a much smaller difference between winter and summer breakdown rates than the fourfold difference suggested above. Differences in physico-chemical properties of the two streams, particularly the greater current velocities in the Victorian study, may be partly responsible for this. The rapid decomposition of M. propinquum is probably typical of submerged macrophytes in streams. Fisher & Carpenter (1976) found very similar weight losses for three species of macrophytes. However, the rapid decomposition of S. babylonica in the coarse mesh bags in the present study (half-life 7 days) is in marked contrast to rates reported by other workers for autumn shed leaves of Salix spp. Petersen & Cummins (1974) reported half-lives of 89 and I12 days for two species of Salix and Mathews & Kowalczewski (969) found a half-life of approximately go days for mixed Salix spp. in the Thames. It is unlikely that the differences from our study can be attributed solely to temperature effects since this would require a Qio of ap123
proxi mately 13. But if a fourfold difference between summer a.nd winter rates is assumed reasonable then the winter decoi position of S. babylonicain our fine mesh bags (halflife 4 x 26 = 104 days) is comparable with that found in the other studies. However, the winter decomposition in our coars e mesh bags (half-life 4 x 7 = 28 days) would still be much faster than that found in other studies and this suggests that the contribution of invertebrates to decomposion here was much greater than in other studies. This couldIbe a result of differences in the taxonomic composition cof the fauna and also the higher density of colonisation ffound in the present study. The maximum colonisation Ilevel for S. babylonica in the present study was 64 animaals g-' at 2 weeks whereas the maximum level found by M.athews & Kowalczewski (1969) was 43 animals g-' at six months (estimated from their data without allowing for ccolonisation of bags per se). In contrast to the present study Mathews &Kowalczewski (I 969) found no significant difference in weight loss betweeen coarse and fine mesh bags and concluded that invertel)rates did not play a significant role in decomposition. To some extent the difference in weight loss between the coarsee and fine mesh bags in the present study must have result ed from the greater retention of small particles by the fine nnesh. Some loss of small whole leaves of M. propinquum and S. babylonica may also have occurred. How-
8( O -
6C
0) E-
E
40 I
-
20
I
]I
20
IlA
40
l
60
IZ l_
80
J
100
Fig. 5. Relationships between colonisation of plant material by invert ebrates (number of animals minus control per g) and stage of dec, omposition (% initial dry weight lost). Values marked *are not inccluded in the regression analysis. A s. babylonica O C. cunninghamiana A M. propinquum *E. bllakelyi I24
ever, the much greater erosion of leaf tissue of E. blakelyi in the coarse mesh bags (Fig. 2) suggests invertebrates and current were important factors responsible for the differences, at least in the fragmentation phase. Reice (1977) found that water velocity was not a significant factor influencing the weight loss during early stages of decomposition. This may also be true for the present study. However, the current must have played some role in the later fragmentation stage of decomposition, at least in so far as to remove small particles fragmented by invertebrates. Petersen &Cummins (1974)have questioned the validity of drawing such conclusions from litter bag experiments suggesting that, as well as excluding the large 'shredder' species, litter bags might inhibit microbial decomposition because of reduced water exchange and possible anaerobic conditions. Whilst these conditions might have applied to the very fine mesh (o.I5 mm) bags used in the present study, such effects have not been demonstrated. In fact, Mathews & Kowalczewski (969) found no significant difference in breakdown rates between bags with 3.0 mm and 0.26 mm mesh and there would probably have been a considerable difference in water exchange between these two types of bags. The two rapidly decomposing species in the present study also had higher initial phosphorus and nitrogen contents than the two slow species. This trend has also been found by other workers (Witkamp, 1966; Blackburn & Petr, 1979) and reflects the higher cellulose and lignin content of more resistant leaves. . ,. · .'...'.1-L....1 T In many studies large particle teecling 'shredder' species of invertebrates have been shown to play an important role in the breakdown of leaves (Anderson &Sedell, 1979). However, in the pool zone of Commissioners Waters such 'shredder' species were relatively unimportant. Plecoptera were restricted to the riffle zones while tipulids formed a very small proportion of the fauna and only occurred in the bags during the early stages of decomposition. Most of the pool fauna were fine particle feeders and hence their contribution to the breakdown of the plant material would be through the activity of 'scraner' species on softened tissue and by mechanical fragmentation through ambulatory activity of 'collector' species. The most important 'scraper' species in the present study were the mayflies A talophlebiaspp. and A talophlebioidessp. which showed a distinct preference for the litter bags compared to the 'collector' species. In common with other studies of colonization the number of animals per g of plant material increased with decomposition until only small amounts of refractory mate-
rial remained. However, there was little evidence of an initial 'conditioning' period (as described in other studies: Peterson & Cummins, 1974; Sedell et al., 1975; Benfield et al., 1977) during which colonisation is low until microbial activity makes the material palatable for macroconsumers. Perhaps such microbial conditioning occurred very rapidly at the higher temperatures encountered in the present study. The more rapid colonisation of the fast processing species M. propinquum and S. babylonica agrees with the findings of Kaushik &Hynes (1971) and Petersen &Cummins (1974), who found a preference by stream invertebrates for detritus undergoing faster rates of decomposition. Such preferences suggest that colonisation of detritus may be a function of the stage of decomposition, regardless of plant species. The likelihood of this was examined by plotting an index of colonisation (N) against an index of decomposition (WL). Excluding the values for M. propinquum and S. babylonica at 4 weeks (when < I g of plant material remained) it was found that a highly significant linear relationship existed between these two indices (Fig. 5). The equation for this relationship, derived by the method of least-square regression analysis (Zar, 1974), was: N = -20.33 + 0.98 WL (r2 = 0.80, P < O.OOI) where, N is number of animals minus control per g, WL is percentage initial dry weight of plant material lost and r 2 is the coefficient of determination. This relationship must be considered as giving substantial support to the above idea. Pidgeon (1978) suggested that the apparently minor contribution made by willow detritus to benthic fauna production may have been the result of willow being unpalatable to the indigenous fauna of Commissioners Waters. The findings of the present study show that this is clearly incorrect. Blackburn & Petr (1979) have also shown that leaves of exotic Quercus sp. were colonised by indigenous benthic fauna of Cement Creek, Victoria. An alternative explanation for the minor role played by willow detritus is that the combination of rapid decomposition and relatively short period of input of willow leaves into the system results in these being available to the benthic fauna for only a short period and this is insufficient to support a significant increase in invertebrate production. Low diversity of the terrestrial detritus input may also be a factor limiting invertebrate production. Petersen & Cummins (1974) suggested that the different decomposition rates of the various leaf species entering woodland streams would be advantageous to the fauna since it would
extend the availability of terrestrial detritus through a step-wise addition of new food sources. Reduction of the diversity of available detrital material would then reduce the temporal availability of detritus to invertebrates. This was suggested by Benfield et al. (1977) as a reason for the absence of 'shredder' species from a pastureland stream. However, such effects are likely to be most important when leaf fall is confined to a relatively short period as with northern hemisphere deciduous trees. With the continuous leaf fall of the evergreen Australian vegetation, under natural conditions diversity of leaf input is likely to be of little significance to invertebrates compared to the magnitude of input and the effects of fluvial transport on detritus availability. The latter may also be affected by the planting of dense stands of willows along small streams since these inhibit the growth of macrophytes which, in turn, reduces the capacity of the stream to retain detritus.
Summary Stream ecosystems are currently regarded as being dependent upon allochthonous organic matter and the contribution made by riparian trees is considered very important. In Australia the native riparian trees are almost exclusively evergreen, providing what could be considered as a continuous energy input and shading effect. However, in agricultural areas of south-eastern Australia the native riparian trees have been replaced with exotics such as willows (Salix spp.). Such changes to the composition of the riparian vegetation have been thought to alter the energy flow patterns in affected streams. Willow leaves have been suggested to be in some way unavailable to the indigenous benthic fauna. To test this the decomposition and colonisation by invertebrates of willow leaves along with leaves of the native riparian tree species E. blakelyi and C. cunninghamiana and the aquatic macrophyte M. propinquum was examined in Commissioners Waters, a small stream on the New England Tableland. Coarse mesh ( o mm) litter bags were filled with each of the four types of plant material and strips of black plastic (PVC) sheeting and placed in the stream. Bags of each type were sampled after I, 2, 4, 8 and 6 weeks. From these bags all animals were removed and sorted and the remaining plant material dried and weighed. Decomposition of S. babylonica, E. blakelyi and M. propinquum in the absence of macroinvertebrates was measured using fine mesh (0. 15 mm) litter bags. Five bags for each species were removed 4 and 6 weeks after immersion. The fauna inhabiting the 125
substrate was sampled at 4, 8 and 6 weeks after the immersion of the litter bags. Qualitative changes in the plant material were assessed through the measurement of relative ash, organic nitrogen and phosphorus contents of each species collected at each sample time. Weight loss from the course mesh litter bags was far greater for M. propinquum and S. babylonica than for E. blakelyi and C. cunninghamiana. Initial half-lives were 7 days for M. propinquum and S. babylonicaand 45 and 66 days, respectively, for C. cunninghamianaand E. blakelyi. Weight loss from the fine mesh bags was considerably slower than from the course mesh bags. This was taken as evidence of the importance of benthic fauna in decomposition processes. E. blakelyi showed three distinct stages of breakdown: an initial period of rapid leaching, a period of gradual breakdown of epidermal and internal tissue structure and a period of rapid loss resulting from fragmentation. These three stages may have occurred in the other species but were masked by either the speed of breakdown or, in the case of C. cunninghamiana, leaf structure. The relative ash contents increased as decomposition proceeded. In general, phosphorus was lost at a rate faster than weight loss, while nitrogen was lost initially at a rate slower than weight loss. All taxa present in the substrate, except for gomphid dragonfly larvae, were found at some stage in the course mesh litter bags. Colonisation was rapid, with the litter bags providing a more suitable habitat for the more active animals such as the Ephemeroptera than for the more sedentary oligochaetes. The total number of animals per bag increased as plant material presumably became more palatable and then declined as it began to disappear with fragmentation. Animals appeared to colonise the plant material primarily as a food source and not just as a refuge. The rapidly decomposing M. propinquum and S. babylonica were colonised at rates much faster than the slower decomposing E. blakelyi and C. cunninghamiana. Of the four types of plant material, M. propinquum and S. babylonica were considered to belong to Petersen & Cummins' (974) fast breakdown group (half-lives < 46 days) while E. blakelyi and C. cunninghamianawere considered to belong to the slow breakdown group (half-lives > 138 days). This was based on the assumption of a fourfold difference between summer and winter processing. The more rapid breakdown of S. babylonicain comparison with other studies, further suggested the importance of invertebrates in litter decomposition. The rapid colonisation by invertebrates of fast processing species of plant material (M. propinquum and S. babylonica) is consistent with I26
the findings of other workers. It was suggested that the colonisation of detritus may be a function of the stage of decomposition, regardless of plant species. Willow leaf detritus, rather than being unpalatable to benthic fauna, plays a minor role in invertebrate production because of its rapid decomposition and relatively short period of input into the system and not because of any unpalatability. It is available for a period too short to support a significant increase in invertebrate production.
Acknowledgements We would like to thank the members of the second year ecology class who assisted in the initial preparations for the study and in the analysis of early samples. Thanks also to Mr. J. Bowles of the CSIRO Division of Animals Production for assistance with chemical analyses of plant material and to Dr. D. J. Woodland of the Zoology De-
partment, University of New England, for helpful criticism of the manuscript.
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