leaf decomposition and stream macroinvertebrate colonisation … · 2017. 2. 7. · 1department of...

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JEFFREY H. BRAATNE**, 1, S. MAZEIKA P. SULLIVAN*, 1 and ERIN CHAMBERLAIN2

1Department of Fish and Wildlife Resources, University of Idaho, P.O. Box 441136, Moscow, Idaho,USA 83844–1136; email: [email protected]

2Environmental Science, University of Idaho, P.O. Box 443306, Moscow, ID, USA

Leaf Decomposition and Stream Macroinvertebrate Colonisationof Japanese Knotweed, an Invasive Plant Species

key words: allochthonous inputs, Japanese Knotweed

Abstract

Japanese knotweed (Fallopia japonica HOUTT. RONSE DECRANE) is a highly invasive exotic plant thatforms monocultures in riparian areas, effectively reducing plant diversity. This change in riparian plantcomposition alters the allocthonous input of leaf litter into adjacent streams. A field experiment wascompleted to understand how leaf decomposition and macroinvertebrate colonisation associated with theincorporation of exotic leaf litter. Leaf packs of Japanese knotweed, native alder (Alnus incana L.),native cottonwood (Populus trichocarpa TORR. and GRAY), and two additional mixed pack types (alderand cottonwood; alder, cottonwood, and Japanese knotweed) were placed into a 50 m stream reach inClear Creek, Idaho, and removed over a three-month period. Leaf decomposition and macroinvertebrateassemblages were similar between leaf types, despite differences in nitrogen and phosphorus content.The diversity of leaf types within a given leaf pack also had no effect on leaf decomposition or macroin-vertebrate dynamics. These findings suggest that allochthonous inputs of Japanese knotweed fulfill adetrital function similar to that of native leaf litter.

1. Introduction

Riparian habitats are highly susceptible to invasion by exotic plant species (NationalResearch Council, 2002; SHER et al., 2002). The invasion of riparian areas is related to thedynamic nature of riverine systems where higher flows disturb riverbanks and create openspace for plant recruitment (PLANTY-TABACCHI et al., 1996). Streams also facilitate thedownstream dispersal of seeds and rhizomes (PYSEK and PRACH, 1994). Natural dispersaland recruitment, along with anthropogenic changes in riverine systems provide ideal envi-ronments for invasive plants (BEERLING, 1991; PYSEK and PRACH, 1993; BEERLING et al.,1994; PLANTY-TABACCHI et al., 1996). Since detrital inputs by plants influence multipletrophic levels within streams ecosystems (VANNOTE et al., 1980; WALLACE et al., 1997), ithas been hypothesized that changes in the species composition of litterfall may affect streamfood webs (CUMMINS et al., 1989).

Several studies have investigated the potential effects of riparian exotic plants on leaf lit-ter processing and macroinvertebrate assemblages; effects have varied depending on theexotic leaf type. Studies of Eucalyptus plantations in Spain and Portugal have shownchanges in macroinvertebrate growth and survival (CANHOTO and GRAÇA, 1995), macroin-vertebrate composition (ABELHO and GRAÇA, 1996), macroinvertebrate colonisation of leaf

Internat. Rev. Hydrobiol. 92 2007 6 656–665

DOI: 10.1002/iroh.200611009

* Corresponding author** Deseased, October 2006

Decomposition and Colonisation of Knotweed 657

© 2007 WILEY-VCH Verlag GmbH & Co. KGaA, Weinheim www.revhydro.com

litter (BASAGUREN and POZO, 1994; POZO et al., 1998), and leaf decomposition rates (CAN-HOTO and GRAÇA, 1996; SCHULZE and WALKER, 1997; POZO et al., 1998). Other studies havefound that shredder preferences were not influenced by the geographical origin of the leaflitter (PARKYN and WINTERBOURN, 1997; GRAÇA et al., 2001; ROYER et al., 1999).

Japanese knotweed (Fallopia japonica HOUTT., Polygonaceae), a native of Asia, was firstintroduced into the United Kingdom as an ornamental and subsequently to North Americawhere it has become increasingly abundant in riparian zones (SEIGER, 1997). As an intro-duced species, Japanese knotweed displaces native riparian vegetation through several keyadaptations. First, it competitively excludes sunlight by emerging in early spring and byquickly growing to a height of 2–3 meters. With an extensive rhizome system, Japaneseknotweed also dominates water and nutrient resources (CHILD and WADE, 2000). Establish-ment occurs primarily through fragmentation and downstream dispersal of rhizomes (SEIGER,1997). These invasive properties commonly lead to monospecific stands of Japaneseknotweed along riparian corridors (CONOLLY, 1977; SEIGER, 1997).

By displacing native riparian vegetation, Japanese knotweed alters the makeup of alloch-thonous inputs. However, knowledge of their potential effects on leaf litter processing andmacroinvertebrate communities is limited (DANGLES et al., 2003). Objectives of this studywere to: 1) Quantify and compare the leaf decomposition rates of Japanese knotweed rela-tive to a native cottonwood (Populus trichocarpa TORR. and GRAY, Salicaceae) and nativealder (Alnus incana L., Betulaceae); 2) Assess the associations between leaf litter composi-tion, and leaf decomposition and macroinvertebrate colonisation; 3) Quantify shredder abun-dance and richness on both exotic and native leaf packs, and 4) Assess the potential role ofleaf nutrient content on decomposition rates. Since Japanese knotweed changes riparian veg-etation composition, we predicted that this could alter leaf decomposition rates and thatmacroinvertebrate assemblages would differ from those of native vegetation. Because Japan-ese knotweed is new to the ecosystem, we also hypothesized that macroinvertebrates wouldmore readily colonize native leaves and that both the number of macroinvertebrates and thediversity of shredders would be higher on native leaves.

2. Methods

2.1. Study Site

This study was conducted along Clear Creek, a fourth order stream in the Clearwater River Basin ofnorthern Idaho, USA (46°75´N, 115°56´W, elev. 390 m). The mean annual temperature of this regionis 17.9 °C, with a mean annual precipitation of 61.6 cm (NOAA – Northwest Regional Climate Center,Seattle, WA). A 50-m riffle reach near the mouth of Clear Creek and its confluence with the MiddleFork of the Clearwater River was selected for leaf decomposition and macroinvertebrate studies. Japan-ese knotweed had recently (2002) invaded this reach, so was significantly less abundant than the othernative riparian species (i.e., alder and cottonwood), in fact, at the time of the study, there were only twosmall patches (<1–2 m surface area) of Japanese Knotweed along the length of the reach.

2.2. Water Quality

Stream temperature was recorded continuously with 2 data loggers (Hobo®). Discharge was measuredusing a Marsh-McBirney flowmate (Model 2000). Conductivity, pH, and dissolved oxygen were meas-ured using a multi-probe (YSI 556 MPS). Water samples were also collected and analyzed for alkalin-ity, total nitrates, and soluble reactive phosphorus (Anatech Labs, Moscow, ID). These physical andchemical characteristics are reported in Table 1.

658 J. H. BRAATNE et al.


2.3. Leaf Decomposition

The leaves of the three study species (Japanese knotweed, alder, and cottonwood) were collected justprior to leaf fall. Fresh leaves were aggregated into 8.0 ± 0.1 g batches (N = 30/species) and placed into15 × 22 cm mesh bags with openings of 5 mm. This size mesh was chosen to contain leaves while allow-ing macroinvertebrates access (BENFIELD, 1996). Mixed leaf packs (N = 30) were also prepared using acombination of alder and cottonwood (i.e., native) as well as a combination of alder, cottonwood, andJapanese knotweed (i.e., mixed). Leaf packs were stored overnight and placed into the stream within24 hours in early October 2003. These leaf packs were attached with cable ties to bricks and placedalong the streambed where leaves would naturally accumulate. Five ‘extra’ leaf packs per leaf pack typewere brought back to the lab and processed to quantify initial Dry Mass (DM) and Ash Free Dry Mass(AFDM).

Leaf packs were randomly selected and removed from the stream reach after 1, 2, 4, 6, 10 and14 weeks (N = 25/collection date). Prior to week 14, a large flow event displaced several bricks mak-ing these leaf packs unusable for data analysis. Leaf packs were placed into plastic bags and stored onice in a cooler following removal from the stream. Within 24 h, all leaf packs were processed in thelaboratory. Sediment and macroinvertebrates were rinsed from the leaves over a 250 µm sieve. This leafmaterial was then used to determine both DM and AFDM.

Leaves from all leaf packs were dried at 50 °C for 24 hrs and weighed to determine DM. Dried leaveswere ground into a fine powder and a 250 mg sub-sample was ashed at 550 °C to determine AFDM.The mean AFDM of the initial leaf packs was used to estimate the initial AFDM of all leaf packs. Threesub-samples of ground leaf tissue were also selected to assess the nitrogen and phosphorus content ofeach leaf type on each collection date. Total nitrogen and phosphorus of these samples were determinedby modified micro-Kjeldahl and nitric acid/hydrogen peroxide digestion (PARKINSON and ALLEN, 1975)by MDS Harris Laboratories (Lincoln, NE).

Macroinvertebrates were preserved in 70% ethanol and later counted and identified to the lowest pos-sible taxonomic level using a 40X-dissecting microscope. Identification was completed to genus formost taxa using MERRITT and CUMMINS (1996). Taxa were also assigned to functional feeding groups.

2.4. Numerical and Statistical Analyses

Leaf decomposition rates were determined using the exponential decay model:

Wt = W0 e–kt. (1)

Where W0 is the initial AFDM (g), Wt is the final AFDM (g) at time t, and k is the decay coefficient(PETERSON and CUMMINS, 1974). The decomposition rate (k) was determined by regressing the naturallog of % AFDM remaining by time.

Table 1. Physical and chemical characteristics of Clear Creek, Idaho between October 2003and January 2004 (SRP = Soluble Reactive Phosphorus; DO = Dissolved Oxygen)

Parameter N Mean Range

Stream Width (m) 6 15.3 14.5–16.3Water Depth (m) 70 0.1 0.1–22.0Conductivity (µS/cm) 35 35.8 28.0–45.0DO (mg/l) 35 12.7 10.8–14.3pH 35 7.0 6.5–7.6Alkalinity (µg/l) 4 24.5 21.0–28.0Discharge (m3/S) 7 0.8 0.5–1.5SRP (µg/l) 3 24.3 13.0–35.0Total Nitrates (µg/l) 4 39.6 10.0–85.0



Data were analyzed using both univariate (ANOVA) and multivariate (MANOVA) tests. When nec-essary, data were ln (x + 1) transformed to meet assumptions of both univariate and multivariate analy-ses. A MANOVA was performed to look at potential differences in macroinvertebrate response vari-ables (i.e., total macroinvertebrate abundance, total shredder abundance and generic richness, and totalabundance of the most common shredder genera) across leaf pack types and collection dates. A two-factor ANOVA (leaf pack type and collection date) was used to examine differences in shredder com-position among leaf packs. A second MANOVA was performed to assess potential differences in leaftissue nitrogen and phosphorus among leaf pack types and collection dates. All statistical analyses wereperformed using SAS version 8.2 (2001) of the SAS Institute, Inc., Cary, NC.

3. Results

3.1. Nutrient dynamics

The nitrogen and phosphorus content of leaf tissues differed among leaf pack type(MANOVA; F = 190.63, P < 0.001, df = 4) and collection date (MANOVA; F = 12.84,P < 0.001, df = 5). However, there was no significant interaction between leaf pack type andcollection date (MANOVA; F = 1.79, P = 0.098, df = 10). Overall, the nitrogen and phos-phorus content of Japanese knotweed and cottonwood leaves were less then half that foundin alder.

3.2. Leaf Decomposition

Within four weeks, the leaf mass in all leaf packs had declined by more than 40%. Bythat time, stream temperatures had dropped close to 0 °C, with fluctuations between 0 °Cand 4 °C (Fig. 1). By the end of the study, 51% to 58% of the initial leaf mass remainedundecomposed. Decomposition rates ranged from 0.006 (Japanese knotweed) to 0.008(mixed leaf pack, Table 2), but showed no significant differences among leaf pack types(ANOVA; F = 1.24, P = 0.295, df = 4). All leaf pack types fell within the medium process-ing range (PETERSON and CUMMINS, 1974).

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Figure 1. Continuous temperature recordings in Clear Creek, Idaho, from 5 Oct. 2003 – 13 Dec. 2003.



3.3. Macroinvertebrate Colonisation

Macroinvertebrate variables analyzed included: 1) total macroinvertebrate abundance, 2)total shredder abundance and generic richness, and 3) total abundance of the most commonshredder genera: the caddisfly Lepidostoma and the stonefly Taenionema. The macroinver-tebrate community of the study reach was found to be diverse, with all functional feedinggroups (e.g., collectors, predators, scrapers, grazers, etc.), and all major taxa (e.g., Ephe-meroptera, Plecoptera, Trichoptera, Diptera, etc.) represented in our field collections. How-ever, there was no significant difference in the abundance of macroinvertebrates among leafpack types (Fig. 2: MANOVA; F = 1.37, P = 0.157, df = 4). Despite a significant differencebetween collection dates (MANOVA; F = 15.03, P < 0.0001, df = 5) that represented anincrease of macroinvertebrates over time, there was no significant interaction effect betweenleaf pack type and collection date (MANOVA; F = 0.78, P = 0.885, df = 10).

The total abundance of shredders among leaf packs increased minimally over time throughweek 6, with a slight increase from weeks 6–10 (Fig. 3a). Shredder richness per leaf pack

Table 2. Decomposition coefficients (k) of 5 different leaf pack types in Clear Creek,Idaho. (Mixed = alder, cottonwood, and Japanese knotweed, native = alder and cottonwood).

Leaftype k ± 1 SE R2

Alder 0.00779 ± 0.0010 0.6844Cottonwood 0.00800 ± 0.0009 0.7356Japanese knotweed 0.00665 ± 0.0016 0.3792Mixed 0.00811 ± 0.0012 0.6386Native 0.00795 ± 0.0010 0.6906

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Figure 2. Total macroinvertebrate abundance on leaf packs collected over ten weeks from Clear Creek,Idaho. Native and mixed leaf types are combination of leaf types (native = alder and cottonwood;mixed = alder, cottonwood, and Japanese knotweed). Symbols represent means of five replicates of eachleaf type at each collection date. Leaf pack types were not significantly different from each other

(MANOVA; P > 0.05).



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(Fig. 3b) also increased over time, but there was no significant difference among leaf types(ANOVA; F = 1.4, P = 0.240, df = 4). At the beginning of the study, total Taenionema perleaf pack were found in very low numbers (Fig. 3c), but increased five-fold from week 6 toweek 10 (ANOVA; F = 70.56, P < 0.0001, df = 5). In contrast, numbers of Lepidostoma(Fig. 3d) showed no differences between collection dates (ANOVA; F = 2.07, P = 0.090,df = 5). By the end of the study, Japanese knotweed and cottonwood had lower numbers thannative, mixed, and alder leaf packs.

4. Discussion

Differences in decomposition are often correlated with the nutrient content of the differ-ent leaf types (WEBSTER and BENFIELD, 1986; IRONS III et al., 1988), yet leaf decompositionrates in this study were similar despite differences in nutrient content. Alder contained twicethe amount of nitrogen than cottonwood or Japanese knotweed, but showed no significantdifference in decomposition rate.

Temperature influences decomposition rates by affecting microbial and macroinvertebrateactivity, with lower temperatures retarding decomposition (IRONS III et al., 1994; ROBIN-SON et al., 1998). In the present study, there was a dramatic decrease in temperature byweek 4 that coincided with declines in leaf decomposition for all leaf types (Fig. 1). Theselower temperatures may have masked potential differences in decomposition due to nitrogencontent. In some streams, habitat characteristics as well as macroinvertebrate and microbialcomposition have been more important than nutrient content in controlling leaf decomposi-tion (IRONS III et al., 1994; ROBINSON et al., 1998; DANGLES et al., 2003). ROBINSON et al.(1998) studied Alnus virdis (CHAIX) DC. in glacial streams (0.8–2.3 °C) and found break-down rates to range from k = 0.0029–0.0305. This wide range in k was due to differing habi-tat characteristics, as well as varied macroinvertebrate and fungal composition among studysites rather than nutrient content. In the present study, composition of macroinvertebrate and

Figure 3. Total shredder abundance (a), shredder taxa (b), Taenionema abundance (c), and Lepidos-toma abundance (d) on leaf packs collected over ten weeks from Clear Creek, Idaho. Native and mixedleaf types were a combination of leaf types (native = alder and cottonwood; mixed = alder, cottonwood,and Japanese knotweed). Symbols represent means of five replicates of each leaf type at each collec-

tion date. Leaf pack types were not significantly different from each other (MANOVA; P > 0.05)

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microbial communities and/or temperature regime appears to have been more important indriving decomposition rates than leaf nutrient quality.

Leaf decomposition rates of Japanese knotweed were not significantly different fromnative or mixed native-invasive leaf packs. This implies that neither leaf litter diversity norspecies composition of leaf packs were important in influencing decomposition patterns.Because decomposition rates remained consistent in leaf packs with multiple species, it islikely that Japanese knotweed leaf litter fulfills a similar detrital function as native leaf lit-ter. These findings contrast with those of SWAN and PALMER (2004), who found that decom-position rates of mixed leaf packs were slower than predicted by the decomposition rates ofindividual species. In their study, leaves that decomposed more slowly provided protectionfor those that decomposed more rapidly, inducing an overall slower rate of decomposition.This may have important ecological implications by increasing the amount of time leaf mate-rial is available for microbial and macroinvertebrate colonisation. However, they observedthis pattern only during the warmer summer months, and similar to our findings, was notapparent during the cooler fall season (SWAN and PALMER, 2004).

Macroinvertebrate colonisation of Japanese knotweed did not differ from native leafpacks. Similarly, macroinvertebrate abundance was similar in both single and multiplespecies leaf packs. There was some divergence in macroinvertebrate abundance towards theend of the study period; alder, mixed, and native leaf pack types had more macroinverte-brates and shredders than cottonwood and Japanese knotweed. Although these results werenot significant, they may provide evidence of an emerging trend had the study period beenextended. All three leaf pack types with higher mean abundance included alder, which has been shown to be preferred as a food source due to its higher nitrogen and lower tan-nin content (IRONS III et al., 1988).

While the traditional view of leaf decomposition suggests that leaching, microbial condi-tioning, and macroinvertebrate consumption are sequential steps, GESSNER et al. (1999) pro-posed that fungi and macroinvertebrate shredders likely compete for shared resources. Nev-ertheless, in our study, microbiotic activity may have sufficiently conditioned leaves so thatthere were divergent trends in overall macroinvertebrate and shredder abundance.

In previous studies, shredders have shown a preference among leaf types (e.g., NOLEN andPEARSON, 1993), but these preferences were not necessarily dependent on the geographicalorigin of the leaves (PARKYN and WINTERBOURN, 1997). Shredders were attracted to lea-ves’ intrinsic properties, instead of showing a local adaptation to specific plant species(GRAÇA et al., 2001; PARKYN and WINTERBOURN, 1997; YEATES and BARMUTA, 1999). Ifexotic vegetation has intrinsic leaf properties that are not preferred by shredders, there maythen be an effect on shredder populations, as documented in studies of introduced eucalyp-tus along rivers in southern Europe (BASAGUREN and POZO, 1994; CANHOTO and GRAÇA,1995; ABELHO and GRAÇA, 1996; POZO et al., 1998). Eucalyptus has a waxy cuticle, phe-nols, low nitrogen content, and essential oils that negatively influence fungal and shreddercolonisation (BASAGUREN and POZO, 1994; CANHOTO and GRAÇA, 1995; ABELHO and GRAÇA,1996; POZO et al., 1998). Similarly, invasive European willows were preferred over nativeeucalyptus by shredders along Australian rivers (YEATES and BARMUTa, 1999; PARKYN andWINTERBOURN, 1997; SCHULZE and WALKER, 1997).

Another possible explanation for the similar shredder numbers, on both native and Japan-ese knotweed leaf packs, may be the availability of alternate food sources and habitat with-in leaf packs. Though shredders primarily feed on detritus, they also consume other foodsources, such as algae and Fine Particulate Organic Matter (FPOM) trapped within leafpacks (FRIBERG and JACOBSEN, 1994; DANGLES et al., 2001). FPOM trapped within leaf bagsalso provides habitat that may attract macroinvertebrate colonisation (DANGLES et al., 2001).These alternate food sources and available habitat within leaf packs in conjunction with thegeneralist detrital tendencies of some shredder taxa may help explain our observations ofmacroinvertebrate assemblages on exotic leaf packs.





Japanese knotweed exhibited no differences from native leaf litter in either decompositionrate or macroinvertebrate colonisation dynamics. Reduction in plant diversity within leafpacks showed no differences as well, with multiple-species leaf packs showing similar pat-terns as did single-species leaf packs. These results may be due to a number of factorsincluding minimal differences between leaf quality of Japanese knotweed and native plants,and alternate food sources within leaf packs for shredders. External factors, such as tem-perature, may have also influenced leaf decomposition rates and macroinvertebrate colo-nisation, thus, results may differ in a warmer year or season.

5. Acknowledgements

We would like to thank James B. JOHNSON, TIMOTHY LINK, and STEVEN HOLLENHORST for their assis-tance with this research. Thank you also to JULIE LORION for her help with field and lab work.

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YEATES, L. V. and L. A. BARMUTA, 1999: The effects of willow and eucalypt leaves on feeding prefer-ence and growth of some Australian aquatic macro invertebrates. – Austral. J. Ecol. 24: 593–598.

Manuscript received May 16th, 2006; revised June 26th, 2007; accepted July 2nd, 2007

Editor-in-Chief: Mufit Bahadir, Germany

Editors:

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2007. Vol. 35. 6 Issues.Print ISSN: 1863-0650Online ISSN: 1863-0669

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