Chrysanthemoides monilifera ssp. rotundata invasion alters decomposition rates in coastal areas of south-eastern Australia

Forest Ecology and Management 198 (2004) 387–399

Chrysanthemoides monilifera ssp. rotundata invasion alters decomposition rates in coastal areas of south-eastern Australia Elizabeth A. Lindsay*, Kris French Department of Biological Sciences, University of Wollongong, Northfield Ave, Wollongong, NSW 2522, Australia Received 5 March 2004; received in revised form 12 May 2004; accepted 13 May 2004

Abstract Weed invasion can disrupt ecological processes and the structure of ecosystems. One process potentially affected by weed invasion is leaf litter decomposition, which is important for supplying nutrients and organic matter to the soil. Leaf litter decomposition of the environmental weed Chrysanthemoides monilifera spp. rotundata was compared to that of the native coastal shrubs Acacia longifolia var. longifolia, Banksia integrifolia and Leptospermum laevigatum. This was undertaken in sand dunes heavily infested with C. monilifera and in native un-infested dunes. Coarse and fine mesh litterbags were used to determine the importance of soil microflora and litter invertebrates. C. monilifera decomposition was fitted to a double exponential decay model, whereas the native leaf decomposition was best explained by a single exponential decay model. The succulent C. monilifera leaves decomposed at a significantly higher rate than the sclerophyllous native leaf mix. Time to 99% leaf loss was estimated to be 0.9–1.3 years for C. monilifera and 3.1–4.4 years for the native species. This reflects the physical properties of the leaves and the lower leaf mass area of C. monilifera. C. monilifera leaves decayed faster in the coarse mesh bags compared to the fine, indicating leaf litter invertebrates positively influenced their decomposition. Mesh size had little affect on the native leaf decomposition rate. C. monilifera leaves generally decomposed faster within the weed infestations, partly due to invasion creating a protected environment with an altered microclimate. Replacement of native species with C. monilifera will alter nutrient cycling through changes in litter quality and decomposition rates. This may have implications for ecosystem resilience and stability. # 2004 Elsevier B.V. All rights reserved. Keywords: Bitou bush; Leaf litter decomposition; Leaf quality; Microclimate; Weed invasion

1. Introduction Leaf litter decomposition is a major pathway for supplying energy and nutrients to soils in ecosystems (Staff and Berg, 1981; Spain and Hutson, 1983). Decomposition involves mechanical break down of *

Corresponding author. Present address: Department of Biological Sciences, Macquarie University, Sydney, NSW 2109, Australia. Tel.: þ61-2-9889-7242; fax: þ61-2-4221-4135. E-mail addresses: [email protected], [email protected] (E.A. Lindsay).

litter, leaching of soluble compounds and chemical deterioration of plant tissue (Witkamp, 1971; Lavelle et al., 1996). Litter quality and climate, in particular temperature and moisture, are the main controlling factors of decomposition (Meentemeyer, 1978; Shaw and Harte, 2001). Soil microflora and leaf litter invertebrates also aid leaf litter decay (Vossbrink et al., 1979; Douce and Crossley, 1982) and their abundance and diversity is affected by the physiochemical characteristics of the leaf litter (Blair et al., 1990; Pereira et al., 1998).

0378-1127/$ – see front matter # 2004 Elsevier B.V. All rights reserved. doi:10.1016/j.foreco.2004.05.032

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Weeds can disrupt ecological processes and the structure of ecosystems (Breytenbach, 1986; Usher, 1988) by changing soil nutrient availability (Matson, 1990; Musil and Midgley, 1990; Fogarty and Facelli, 1999) and disrupting nutrient cycling (Vitousek, 1990; Standish et al., 2004). Weeds are likely to produce leaf litter of different quality and quantity to the community it invades. Changes in the leaf litter available to the decomposer community can alter the decomposition rate (Pereira et al., 1998; Ehrenfeld et al., 2001). This disturbance can be further magnified by the low diversity of leaf litter in weed monocultures often supporting fewer invertebrates (Springett, 1976; Slobodchikoff and Doyen, 1977). Invasion by Tradescantia flumensis in New Zealand forests increased the local decomposition rate, with leaves being less sclerophyllous with a lower C:N ratio than the native species. This lead to a reduced leaf litter layer, increased soil nitrate and changes to the litter invertebrate community (Standish et al., 2004). Similarly in South Africa the weed Acacia saligna increased soil nutrients and pH (Musil and Midgley, 1990) through its higher leaf fall and decomposition rates (Witkowski, 1991). In contrast, the grass Bromus tectorum produces litter of lower quality than the native grassland species in Colorado, USA, and has decreased the nitrogen available in the soil (Evans et al., 2001). The evergreen shrub Chrysanthemoides monilifera ssp. rotundata (Family Asteraceae), commonly known as bitou bush, is native to South Africa (Weiss and Noble, 1984). It was introduced to Australia around 1908 and is now a common environmental weed along the south east coast. It was planted to stabilise sand dunes after disturbance (Weiss, 1986; Humphries et al., 1991), but increased wind erosion occurred once native species were displaced and the infestation aged (Thomas, 1997). C. monilifera now covers approximately 80% of the New South Wales coastline, growing on headlands and dunes, where it is the dominant species in 40% of the vegetation (Toth et al., 1996; Holtkamp, 2002). C. monilifera is taller than native grasses and herbs, and shorter than the tree–shrub canopy (Lane, 1981). The dense canopy formed excludes native grasses, herbs and seedlings (Wickham and Stanley, 1984), and in highly infested areas there is a shift towards simpler vegetation, approaching a monoculture (Dodkin and Gilmore, 1985; Thomas, 1997). The leaf litter and soil within C.

monilifera infestations have been shown to impede the growth of native seedlings (Vranjic et al., 2000). Weeds that form a dense canopy can change the light regime and microclimate (Breytenbach, 1986). This can lead to changes in the decomposition process and nutrient cycling (Belyea, 1996; Heneghan et al., 1999; Shaw and Harte, 2001). The aim of this study was to compare decomposition rates of litter from C. monilifera and three native species. This was undertaken within native vegetation and C. monilifera infestations to determine if invasion altered the decomposition process. Litterbags were used to assess the importance of invertebrates in the decomposition of each leaf type and within each habitat. Several microclimatic and physiochemical leaf parameters that could influence the decomposition process were also examined.

2. Methods 2.1. Study areas Four sites were chosen along the New South Wales coastline, located at Anna Bay (328460 S, 1528050 E), Seven Mile Beach (348480 S, 1528320 E), Comerong Island (348520 S, 1508440 E) and Warrain Beach (348580 S, 1508470 E). Within each site, two 30 m 30 m areas were chosen at least 100 m apart. One area was heavily infested with C. monilifera, with a minimum 70% cover, and the other area was uninfested. No chemical or mechanical weed control work had been undertaken on the C. monilifera for at least 10 years. The infestations were at least 12 years old, although usually between 22 and 33 years old. The dominant vegetation within the un-infested native areas consisted of the shrubs Banksia integrifolia, Leptospermum laevigatum and Acacia longifolia var. longifolia or Acacia longifolia var. sophorae. Westringia fruticosa was also dominant at Anna Bay. Sites were located on foredunes, except for the C. monilifera area at Anna Bay. The C. monilifera area at Anna Bay is located on bedrock of rhyolitic ignimbrite, forming part of the Carboniferous Nerong Volcanics (Whitehouse, 1997). Most soils were loose loamy quartz sands with low fertility and high permeability (Hazelton, 1992, 1993; Murphy, 1995). The exceptions were the C. monilifera areas at Warrain

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Beach and Anna Bay, which are sandy clay loams. All soils were slightly to strongly acidic, with varying amounts of organic matter. During the study, Nelson Bay near the most northern site of Anna Bay had a mean maximum day temperature of 23.6 8C and a minimum of 13.7 8C. Sites further south on the coastline were cooler and received slightly less rainfall, with Culburra near Warrain Beach having a mean maximum day temperature of 22.3 8C and a minimum of 12.7 8C. The average annual rainfall was 1340 mm at Nelson Bay and 1250 mm at Culburra (Australian Bureau of Meteorology). 2.2. Decomposition rates B. integrifolia, L. laevigatum and C. monilifera leaves and A. longifolia phyllodes were collected from plants on the foredunes and hind-dunes of the NSW South Coast during September and October 2000. New growth was avoided. Freshly fallen leaves were not used, as there were insufficient quantities of C. monilifera. Litterbags were used to monitor decomposition (Crossley and Hoglund, 1962). Two types of bags were used; a fine (0:50 mm  0:25 mm) mesh polyester netting sewn into bags of 200 mm  200 mm, and a coarse (4:0 mm  4:0 mm) mesh nylon tube of 200 mm  250 mm. The coarse mesh was used to allow mesofauna (Collembola, Acarina) and most macrofauna (Diplopoda, Isopoda, earthworms) inside. The fine mesh excluded most of these soil animals, and was used to monitor the effects of microbial activity and leaching. Leaves were air dried to constant weight at approximately 25 8C for 3 weeks. Six samples of each leaf species were oven dried at 60 8C for 24 h to obtain a dry weight conversion factor. These leaves were also analysed for total carbon and total nitrogen using a LECO CN 2000 TM analyser. The leaves in the litterbags were not artificially dried as this could affect microbial activity, and consequently the decomposition rate (Tanner, 1981). The bags were filled with either C. monilifera leaves (18:09  0:17 g, dry weight) or a native leaf mix (18:50  0:13 g, dry weight). The native leaf mix contained equal amounts of B. integrifolia, A. longifolia and L. laevigatum, to mimic the natural litter layer (Blair et al., 1990). The

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four types of bags are referred to as fine native, coarse native, fine bitou and coarse bitou. The bags were placed in the field during November and December 2000. They were placed in 24 groups of four, with one of each bag type in each group. Each group of bags was at least 2 m apart. Most sites were either well protected or densely vegetated, prevented bag displacement. In highly exposed areas one end of the bag was secured with a metal stake. Four groups (four litterbags of each type) were randomly retrieved after 78, 165, 220, 292 and 609 days. These were placed in labelled airtight plastic bags and stored in the freezer. They were oven dried at 60 8C for 24 h, cleaned and re-weighed to determine mass loss. Sand was the main contaminant and was easy to separate from the decaying leaves. During the last collection generally less than four bags were retrieved at each site. Most losses were due to bags being torn open by animals and a heavy storm that resulted in sand dunes collapsing into the ocean. These results were not included in the analysis. 2.3. Statistical analysis The decomposition data (mass loss) was fitted to two different models. The first model assumed single negative exponential decay (Olson, 1963). The decomposition constant (k) was calculated from the following expression: Mt =Mi ¼ ekt , where Mt is the litter mass at time t, Mi the initial litter mass and time is expressed in years. The time (t) for 99% of the initial mass to decay was determined from the equation: t ð99% decayÞ ¼ ln 0:01=k. The C. monilifera data fitted poorly to this model, so the data was also fitted to a double exponential decay model (Lousier and Parkinson, 1976; Hunt, 1977; Wieder and Lang, 1982). This model separates leaf material into two components, one that is soluble or easy to decompose and another that is recalcitrant or insoluble. This was performed using the nonlinear (least squares, Gauss Newton) function of SYSTAT version 10 (SYSTAT, 2000), with the expression: Mt =Mi ¼ A ek1 t þ ð1  AÞ ek2 t , where A is a constant that indicates the easily decomposable fraction of the leaf, and (1  A) the recalcitrant fraction. The value of A is related to the carbon to nitrogen ratio of the leaf material and was determined using the equation developed by Hunt (1977):

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A ¼ 0:07 þ 1:11(N/C)1/3, where N is the nitrogen concentration and C the carbon concentration. To determine the time for 99% decay the equation was solved for t and a substitution of U ¼ et was used. The Newton iterative technique was then used to solve for U (Anton, 1992). A three-factor analysis of variance was performed for each site, using SYSTAT (2000). This was to determine differences in the decomposition rate between C. monilifera infested and un-infested areas, leaf types and bag types. The proportion of material remaining was arcsine square root transformed before analysis (Zar, 1999) to improve normality and homogeneity (Cochrans Test). Multiple comparisons of means were performed using a Student–Newman– Keuls test (SNK) at the 0.05 level. Each site was analysed separately, as an appropriate model could not be found with site as a random factor; as there were no appropriate mean squares for the denominator for several factors of interest (Underwood, 1997). 2.4. Leaf structure Several parameters were measured to determine the degree of sclerophylly of the four leaves used. The initial moisture content of each leaf type was determined by oven drying at 60 8C, for 72 h on the day of collection. Samples were then re-weighed and the mass difference determined. The sclerophylly of a leaf is related to its density and leaf mass per unit area (LMA) (Witkowski and Lamont, 1991; Groom and Mamont, 1999). Leaf area was determined on 10 leaves by scanning them and analysing using AutoCAD LT 2000i (AutoCAD, 2000). Leaf thickness was measured with vernier callipers at the widest part of the leaf. LMA was determined by dividing air dried mass by area. Leaf density was determined by dividing LMA by thickness. The area of C. monilifera leaves was determined before drying, as the leaves curled and changed shape.

placed inside large mesh bags to prevent them moving. Four buttons were randomly placed at each site. The temperature was recorded every hour for 7 days. Data was divided into night (6 pm–5 am) and day (6 am– 5 pm) for analysis. A three-factor ANOVA was performed to determine if the maximum temperature varied at each site (random), within the weed infested and un-infested areas (fixed) and at day and night time (fixed). A SNK post hoc test was performed at the 0.05 level. Soil moisture and canopy light penetration were recorded once during the spring 2002. Eighteen soil samples were taken per site along two 20 m transects. A 7 cm diameter core was taken to the A1 horizon. Samples were stored in airtight plastic bags and transported in insulated containers. Sieved (2 mm) soil was weighed ( 60 g) in aluminium trays and dried for 3 days at 105 8C, before being re-weighed. The percent moisture dry weight was determined by the difference between wet and dry weights. A twofactor analysis of variance was performed on arcsinetransformed data, to determine if moisture varied between weed infested and un-infested areas (fixed) for all sites (random). A quantum light sensor (LI-990SA, LI-COR) was used to measure the relative light intensity in light moles/m2 at ground level. Readings above the vegetation and 5 cm above ground level were taken every 1 m along two 20 m transects. If a reading could not be taken above the vegetation, a reading was taken in the open. This was done between 10 am and 2 pm in spring when there was little cloud cover. The percent mean transmittance was calculated. A two-factor analysis of variance was performed on 4th root arcsinetransformed data to determine if light transmittance was lower in weed infested areas than in un-infested areas (fixed), for all sites (random).

3. Results

2.5. Environmental differences

3.1. Decomposition study

The soil surface temperature was measured at Warrain Beach and Seven Mile Beach in spring 2002 using digital thermometer ibuttons (DS1921, Maxim/Dallas Semiconductor). The top organic leaf litter layer was removed to expose the soil surface and the dataloggers

The C. monilifera leaves decomposed much faster than the native leaf mix (F1:94 ¼ 324729, P ¼ 0:001) (Table 1). This occurred in both habitats and bag types (Fig. 1). Leaf material remained in all native litterbags on the last collection (day 609),

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Table 1 Summary of a four-factor ANOVA for each field site for the mean mass lost of C. monilifera and native leaves with time Source

d.f.

Weed Leaf type Bag type Time Weed  leaf Weed  bag Weed  time Leaf  bag Leaf  time Bag  time Weed  leaf  bag Weed  leaf  time Weed  bag  time Leaf  bag  time Weed  leaf  bag  time

1 1 1 3 1 1 3 1 3 3 1 3 3 3 3

Error

Anna Bay

Seven Mile Beach

Comerong Island

Warrain Beach

F

P

F

P

F

P

F

P

0.157 729 4.59 24.4 2.41 4.99 1.85 1.59 0.56 4.12 13.5 1.23 0.530 0.610 0.820

0.690 0.001 0.035 0.001 0.120 0.028 0.140 0.210 0.640 0.009 0.001 0.300 0.670 0.610 0.490

3.90 560 47.3 47.7 9.71 2.48 2.94 15.4 0.450 2.66 0.031 0.440 1.23 1.64 1.00

0.051 0.001 0.001 0.001 0.002 0.119 0.037 0.001 0.001 0.720 0.053 0.860 0.720 0.300 0.190

23.0 444 2.14 26.7 4.86 1.77 0.612 4.61 0.438 0.295 0.729 0.417 0.053 0.731 1.77

0.001 0.001 0.150 0.001 0.030 0.190 0.610 0.034 0.730 0.830 0.400 0.740 0.980 0.540 0.120

8.81 324 0.197 13.9 0.028 0.960 0.720 0.001 0.440 0.250 2.33 0.450 0.160 0.520 0.390

0.004 0.001 0.660 0.001 0.870 0.330 0.540 0.980 0.730 0.860 0.130 0.720 0.920 0.670 0.760

96

The leaves were either in coarse or fine litterbags (Bag type) in a C. monilifera infested area or a native un-infested area (Weed). P < 0:05 significance level.

100 Native fine in bitou Native fine in native Native coarse in bitou Native coarse in native Bitou fine in native Bitou fine in bitou Bitou coarse in native Bitou coarse in bitou

90 80

Percent mass remaining

70 60 50 40 30 20 10 0 0

5

10

15

20

Months

Fig. 1. The mean percentage of the original weight remaining in small and large litterbags in C. monilifera (bitou) and native un-infested areas, through time pooled across all sites. Error bars are one standard error.

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E.A. Lindsay, K. French / Forest Ecology and Management 198 (2004) 387–399 100

Percent original mass remainaing

90

C. monilifera coarse in weed C. monilifera coarse in native C. monilifera fine in weed C. monilifera fine in native Native coarse in weed Native coarse in native Native fine in weed Native fine in native

80 70 60 50 40 30 20 10 0 0

0.2

0.4

0.6

0.8

1

1.2

1.4

1.6

1.8

Time (years) Fig. 2. The fitted curves from the single exponential decay model for the native leaf mix litterbags and the double exponential decay model for C. monilifera (bitou) litterbags.

whereas most C. monilifera leaves had completely decomposed. At Warrain Beach decomposition was faster in the C. monilifera areas compared to the native areas (F1:91 ¼ 8:81, P ¼ 0:004). At Seven Mile Beach and Comerong Island only the C. monilifera leaves decomposed faster within the C. monilifera areas compared to the native areas (F1:94 ¼ 9:71, P ¼ 0:002 and F1:96 ¼ 4:86, P ¼ 0:03). Native leaf decomposition was generally unaffected by the habitat type. At Anna Bay only the native coarse bag treatment decomposed faster in the C. monilifera area (F1:95 ¼ 13:5, P ¼ 0:001) and at Warrain Beach all treatments were faster in the C. monilifera area (F1:91 ¼ 8:81, P ¼ 0:004). The C. monilifera leaves decomposed faster within the coarse litterbags at Seven Mile Beach (F1:94 ¼ 15:4, P ¼ 0:001) and Comerong Island (F1:96 ¼ 4:61, P ¼ 0:034). This trend was also evident at Warrain Beach. At these sites the native leaf mix tended not to decompose significantly faster in the coarse bags within a habitat type. Decomposition of the native litter mix fitted the single exponential decay model better than the double exponential decay model based on the regression

coefficients (Fig. 2, Table 2). For the double exponential decay model, A (the easily decomposable fraction) was calculated as 0.42 from the nutrient values (Table 3). The results were highly variable as shown by the large standard errors in Fig. 1. As a result, the ANOVA analyses were unclear on the effect of weed infestation on native leaf decomposition; however the decay constants indicate that native leaves do decay faster in the C. monilifera areas (Table 2). The decomposition results reinforced the ANOVA results for the effect of mesh size on decay rates, with the coarse bag treatment being faster than the fine treatment in C. monilifera areas, where as there was little difference within the native areas (Table 2). The double exponential decay model explained C. monilifera decay better than the single exponential model based on the regression coefficients (Fig. 2, Table 2). The constant A was calculated as 0.47 (Table 3). The k2 values were more influenced by the treatment type than k1, with all having a rapid initial decay. The trends in the ANOVA results were again reinforced by the decomposition constants. When comparing k2 values, the coarse mesh treatment was faster than the fine in both habitats and both mesh

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Table 2 The decomposition constants (k) for the single and double exponential decay models Litter bag

Habitat

Single exponential model 1

NC

Weed Native Weed Native Weed Native Weed Native

NF CC CF

Double exponential model 1

2

Decay time 99% (years) 1

2

k (year )

R

k1 (year )

k2 (year )

R

1.48 0.970 1.12 1.04 7.20 6.30 6.60 6.33

0.88 0.93 0.73 0.80 0.89 0.77 0.76 0.71

4.19 3.68 4.46 4.08 19.7 19.9 19.8 18.9

0.532 0.255 0.232 0.193 4.30 3.70 3.41 3.14

0.79 0.70 0.65 0.69 0.96 0.95 0.91 0.91

3.11 4.75 4.11 4.43 0.923 1.07 1.16 1.26

The regression coefficients (R2) for the double exponential decay model were calculated from observed vs. predicted values. NC: native coarse, NF: native fine, CF: C. monilifera fine, CC: C. monilifera coarse. Table 3 The mean initial leaf percent carbon and nitrogen concentrations of each species, and the native leaf mixture Species

C%

S.E.a

N%

S.E.

C:N ratio

C. monilfera L. laevigatum A. longifolia B. integrifolia Native mix

39.4 51.5 49.8 50.2 50.5

1.7 0.5 0.2 0.7 0.5

1.9 1.4 2.6 1.2 1.7

0.2 0.2 0.4 0.02 0.2

20.7 36.8 19.2 41.8 29.7

a

The C. monilifera leaves were moister than the native leaves (Table 4), while native leaves were denser and had higher LMA values. A. longifolia and L. laevigatum leaves were thicker than C. monilifera leaves. The L. laevigatum leaves had the highest density, whereas the A. longifolia phyllodes were the thickest and had the highest LMA (Table 4). 3.3. Environmental differences

Standard error.

sizes decayed faster within the C. monilifera infestations (Table 2). 3.2. Leaf quality The native leaves all had a higher percentage of carbon than the C. monilifera leaves (Table 3). However, A. longifolia leaves had the lowest C:N ratio, followed closely by the C. monilifera leaves, indicating a high nitrogen concentration in the A. longifolia leaves.

The C. monilifera areas at Anna Bay, Comerong Island and Warrain Beach were all significantly moister than the native areas (F3:135 ¼ 46:4, P ¼ 0:001) (Fig. 3). The same trend was evident at Seven Mile Beach but it was not significant. The rainfall was higher than average during the study. Normally there is less then 200 mm difference in annual precipitation across all sites (Australian Bureau of Meteorology), however, Anna Bay received more than double the rainfall of Seven Mile Beach during the study (Fig. 3). The two sites with the highest rainfall also had the highest soil moisture.

Table 4 The percent moisture and physical leaf parameters for each species

C. monilifera L. laevigatum A. longifolia B. integrifolia a b

Standard error. Leaf mass area.

Moisture (%)

S.E.a

Thickness (mm)

S.E.

LMAb (mg mm2)

S.E.

Density (mg mm3)

S.E.

90.0 58.8 73.6 46.4

0.08 0.64 1.6 4.9

0.57 0.79 0.87 0.48

0.02 0.01 0.07 0.02

90.8 152.5 278.7 268.0

7.6 5.9 23.7 9.4

160.1 817.0 324.3 557.1

16.4 24.2 17.1 16.1

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3500

Native C. monilifera

Percent soil moisture

3000 2500

15

2000 1500

10

Total precipitation (mm)

Precipitation

20

1000 5 500 0

0 Anna Bay

Seven Mile Beach Comerong Island Warrain Beach

Fig. 3. The mean percent soil moisture (dry weight) within the C. monilifera invaded (bitou) and un-infested (native) areas of each field site and the total precipitation of each field site during the study (November 2000 to June 2002). Error bars are one standard error.

Daytime soil surface temperatures were warmer within the native areas then the C. monilifera areas of Seven Mile Beach and Warrain Beach (F1:2472 ¼ 26:6, P ¼ 0:001) (Native 21:7  0:23, weed 17:2 0:20). There was no difference in nighttime temperatures (Native 15:1  0:16, weed 15:2 0:10).

The percent light transmittance was much lower in all C. monilifera areas than the native areas (F1:3 ¼ 46:1, P ¼ 0:007) (Fig. 4). The maximum value in the native area was 98% but only 15.2% for the C. monilifera areas. The large standard errors in Fig. 4 show how variable the results were for the native areas, reflecting the diversity in the vegetation.

30 Native C. monilifera

Percent light transmittance

25

20

15

10

5

0 Anna Bay

Seven Mile Beach

Comerong Island

Warrain Beach

Fig. 4. The mean percent light transmittance at four sites, within the C. monilifera infested or native un-infested areas. Error bars are one standard error.

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4. Discussions 4.1. Environmental parameters C. monilifera invasion appears to change several environmental parameters and consequently alter the microclimate. This combined with the high quality C. monilifera leaf litter results in rapid leaf litter decomposition. The decomposition constants (k2) were faster for the C. monilifera leaves within the C. monilifera infestations with this clearly reflected in the faster times for 99% decay (Table 3). There was a similar pattern for the native leaves, especially the coarse bag treatments, which decomposed faster within the C. monilifera areas. The C. monilifera sites had a much lower light transmittance with little light detected at ground level. The dense infestations were almost monocultures with a closed canopy and few gaps. This gave protection to the ground and leaf litter beneath. The uninvaded foredunes were a mixture of herbs, grasses, ferns and shrubs of various heights and canopy cover. This produced a variable light transmittance across the sites. More of the ground litter within the native areas is exposed and could be desiccated by the sun and wind, especially as it takes considerably longer to decompose. The changed light regime within C. monilifera infestations could contribute to an altered vegetation structure. For example, native seedling growth could be impaired in the low light environment. In temperate climates adequate soil moisture is required for rapid decomposition (Meentemeyer, 1978; Heneghan et al., 1999). Sand dunes are dry areas, and changes in moisture within dry areas can have large impacts on decomposition rates (Murphy et al., 1998). In general, the sand dunes invaded by C. monilifera were moister than the native areas. The C. monilifera leaves also had a higher moister content than the native leaves (Table 4), so the leaf litter layer under C. monilifera is probably also moister, which would further enhance decomposition. Temperature and moisture interact in a complicated manner in controlling leaf litter decomposition (Couteaux et al., 1995; Guo and Sims, 2001). The areas invaded by C. monilifera had become moister and cooler than the uninvaded native areas. The magnitude of difference between areas was greater for moisture

395

than temperature. The higher temperatures within the native areas had minimal effects on mass loss, most likely due to the lack of moisture (Murphy et al., 1998). The soil surface temperature appears related to the soil moisture and percent light transmittance. The native areas of Seven Mile Beach and Warrain Beach were several degrees warmer than the C. monilifera areas during the day. These areas had low soil moisture and high light transmittance (Guo and Sims, 2001). The decomposition rates varied between sites, due to local climate and geography. The C. monilifera area at Anna Bay had the highest soil moisture and the slowest decomposition rate of all the C. monilifera areas. This soil contains 11% clay, and has lower permeability than the other sites (Murphy, 1995). Combining this with the heavy rainfall (Fig. 3), the soil could have become saturated. Anaerobic conditions may have resulted, and decomposition impaired (Couteaux et al., 1995). 4.2. Decomposition rates The single exponential decay model explained more of the variation in the native leaf decomposition than the double exponential decay model. However, there was a large bias in the decay constant, with the model trying to fit to the initial rapid loss of labile components (Spain and Le Feuvre, 1987). This is evident for all treatments, with the model over estimating mass loss as time increased. With complete decomposition data the double exponential model may have explained more variance in the data, and made more accurate long-term predictions. The decomposition rates for the native leaf mix are comparable to that found by Maggs and Pearson (1977). They determined that the mean turnover time for the litter layer in coastal scrub in Sydney NSW was 3.8 years. In this study the time for 99% of the native leaf mix to decay in the native areas was calculated to be between 4 and 5 years (Table 2). It could take longer than this, as the decomposition constants were determined using fresh leaves. These are likely to have a higher nutrient content than senescent leaves and will consequently decompose faster. For the C. monilifera leaves the double exponential decay model explained more of the variation than the single exponential decay model (Table 2). This model

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is considered to be more realistic as it separates decomposition into two stages (O’Connell, 1987). The initial stage is faster, represented by k1, and involves soluble components leaching out, and easily degraded compounds (sugars, starches, proteins) being utilised by decomposers, usually microorganisms (Crossley and Hoglund, 1962; Songwe et al., 1995). The initial mass loss was fastest in the first 8 months for all treatments (Fig. 1). It was extremely rapid for C. monilifera, indicating these leaves contain more soluble compounds or simple sugars and soft leaf tissue than the native leaves. k2 represents the second stage of decomposition, and involves the breakdown of resistant components, including cellulose, waxes, tannins and lignin (Lousier and Parkinson, 1976). With time the relative amount of recalcitrant material increases and the rate decreases (Wieder and Lang, 1982). k2 was considerably lower than k1 for all C. monilifera leaf treatments. The treatment type (i.e. bag type, leaf type and habitat) also had more impact on the k2 values. The rapid breakdown of C. monilifera could alter nutrient cycling within these disturbed sites. This combined with the altered light transmittance and soil moisture could further enhance the establishment of C. monilifera monocultures. 4.3. Leaf quality The initial C:N ratio and nitrogen concentration of leaves have been used to predict decomposition rates (Meentemeyer, 1978; Mellio et al., 1982) as it is thought that nitrogen is essential but often limiting to the growth of the decomposer community (Palm and Rowland, 1997). However in this study the C:N ratio did not predict the decomposition of all species. The A. longifolia and C. monilifera leaves had similar C:N ratios, which were considerably lower than the C:N ratios for the B. integrifolia and L. laevigatum leaves (Table 3). Low C:N ratios are often associated with fast decomposing nutritious leaves, where as leaves with high C:N ratios, like that obtained for B. integrifolia and L. laevigatum, are generally tough and resistant to the early stages of decomposition (Witkamp, 1966; Blair, 1988; Taylor et al., 1989). The C. monilifera leaves decayed the fastest, yet the A. longifolia leaves were still observed in the mixed litterbags on the final collection. The high nitrogen concentration of the A. longifolia leaves is probably

due to this plant being an active nitrogen fixer (Lawrie, 1981). In a study by Prescott (1995) Pinus contorta var. latifolia trees were fertilised and the resulting litter had a five-fold increase in nitrogen content. This litter decomposed at the same rate as litter from control trees, indicating endogenous nitrogen availability is not the only factor controlling decay as suggested by this study. Litter quality and physical leaf characteristics have been suggested as better predictors of decomposition rates (Gallardo and Merino, 1993; Akanil and Middleton, 1997; Hobbie, 2000). They also reflect the chemical properties of the leaf (Palm and Rowland, 1997) and the palatability to soil fauna (Witkamp, 1966). The more sclerophyllous and tough a leaf, the poorer the carbon quality and the slower the decay (Gallardo and Merino, 1993; Akanil and Middleton, 1997; Hobbie, 2000). Sclerophyllous leaves have extra structural tissue, generally from increased cell lignification or cutinisation (Dickson, 2000). Density and LMA are good indicators of sclerophylly, with values increasing as leaves become more sclerophyllous (Witkowski and Lamont, 1991; Groom and Mamont, 1999). The native leaves were low in moisture and had high density and LMA values (Table 4). The A. longifolia leaves had the highest lamina thickness and LMA values. This is related to their stem morphology (phyllodes), which incorporates many fibres and a thick cuticle (New, 1984). In contrast, the C. monilifera leaves were very moist, and had low LMA and density values. Therefore, the extra cellulose, hemicellulose and/or lignin in the native leaves slowed their decomposition (Hobbie, 2000). The thick cell walls and thick cuticles could also retard decomposition by preventing toxic compounds from leaching out and/or reduce fungal penetration (Pereira et al., 1998). 4.4. Leaf litter invertebrates Many studies have shown that invertebrates and microbes will invade litter bags and form simple microhabitats (Crossley and Hoglund, 1962; Anderson, 1975; Vossbrink et al., 1979). The effect invertebrates have on decomposition appears to be highly variable, but positive (Santos and Whitford, 1981; Douce and Crossley, 1982; Heneghan et al., 1999). For the native leaf mix at most sites, the coarse bag

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treatment did not decay significantly faster than the fine bag treatment, indicating the leaf litter invertebrates did not greatly enhance decay. The leaf species and quality can affect the arthropod and microbial diversity and density (Wiegert, 1974; Blair et al., 1990; Heneghan et al., 1999). Tough leaves with higher C:N ratios are a low quality food source, with lower palatability and digestibility to mesofauna (Witkamp, 1966). If the native leaves were left until they were fully decomposed and the C:N ratio lowered, the leaves could have become more appealing to the invertebrates and more of an impact might have been evident. The C. monilifera leaves in the coarse treatment decomposed slightly faster than the fine bag treatment, especially within the C. monilifera areas. This is clearly indicated in the k2 values (Table 2), with the litter in the coarse bags decaying up to 20% faster. Therefore, leaf litter invertebrates had a positive impact on C. monilifera decay. Spillage affects could also result in the coarse litterbags appearing to have a faster decay rate then the fine mesh litterbags. Particles could be lost from the bags if they were disturbed by animals, and when the bags were retrieved from the field. However, as most native litterbag treatments within native areas had a similar decay rate regardless of mesh size, spillage affects seam negligible. Invertebrates enhance decomposition by directly feeding on leaf material, and indirectly by inoculating litter with microflora and stimulating microbes (Douce and Crossley, 1982; Seastedt, 1984). The C. monilifera leaves are high in moisture, which would aid microbial and fungal colonisation (Couteaux et al., 1995). Therefore, as well as providing a different food source, the moist rapidly decomposing leaf litter layer within C. monilifera infestations would also provide a different habitat for the leaf litter invertebrates. The total abundance of invertebrates was similar in the native and C. monilifera areas, with the weed infestations supporting a different invertebrate assemblage of lower diversity (E.A. Lindsay, unpublished data). However, several groups of invertebrate detritivores, including the amphipods and isopods, were found in significantly higher abundance and detected more frequently within the C. monilifera, which could contribute to the increased decay rate.

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5. Conclusion This study has established that weed infestations can alter ecosystem processes in coastal sand dunes. C. monilifera leaves decompose faster than those of the common coastal shrubs B. integrifolia, L. laevigatum and A. longifolia. Dense infestations of C. monilifera alter the decomposition process by increasing the quality of the leaf litter layer and modifying the microclimate. This is likely to have implications for other elements in the ecosystem, such as the soil microflora and may result in the system being less resilient to perturbations, or other climatic impacts that adversely affect this weed compared with the native species. The rapid decomposition within C. monilifera infestations is likely to increase the speed of nutrient cycling on the sand dunes, leading to alterations in soil nutrient availability. Ultimately, the nutrient cycling regime could shift to one that favours C. monilifera at the expense of native vegetation. Increasing the rates of nutrient cycling may influence the rate of loss of nutrients from the ecosystem, especially as sand has a low retention capacity. Such impacts have rarely been measured in coastal systems, and yet the consequences of weed invasion could be extensive.

Acknowledgements We thank C.J.W Lindsay for generous help on all parts of the project, especially the statistical analysis. The authors thank everyone who assisted with fieldwork, and to R. Keenan for making valuable comments on the manuscript. A Linnean Society of Australia Travel Grant funded part of this work and E.A.L. was on an Australian Postgraduate Award scholarship.

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