Decomposition of aquatic macrophytes can considerably influence carbon cycling and energy flow in shallow freshwater aquatic ecosystems. The Atchafalaya ...
Hydrobiologia 418: 123–136, 2000. © 2000 Kluwer Academic Publishers. Printed in the Netherlands.
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Decomposition dynamics of aquatic macrophytes in the lower Atchafalaya, a large floodplain river Juliann M. Battle1,2,∗ & Timothy B. Mihuc1,3 LA Cooperative Fish and Wildlife Research Unit, School of Forestry, Wildlife, & Fisheries, Louisiana State University, Baton Rouge, LA 70803, U.S.A. 2 Joseph W. Jones Ecological Research Center, Ichauway, Route 2, Box 2324, Newton, GA 31770, U.S.A. 3 Lake Champlain Research Institute, SUNY-Plattsburgh, 102 Hudson Hall, 101 Broad Street, Plattsburgh, NY 12901, U.S.A. Received 18 February 1999; in revised form 27 August 1999; accepted 7 September 1999
Key words: aquatic macrophytes, decay rates, decomposition, macroinvertebrates, microorganisms, riverfloodplain system Abstract Decomposition of aquatic macrophytes can considerably influence carbon cycling and energy flow in shallow freshwater aquatic ecosystems. The Atchafalaya River Basin (ARB) is a large floodplain river in southern Louisiana that experiences a seasonal floodpulse and is spatially composed of a mosaic of turbid riverine and stagnant backwater areas. During two seasons, winter and fall of 1995, we examined decomposition of four common aquatic macrophytes in the ARB: water hyacinth (Eichhornia crassipes), arrowhead (Sagittaria platyphylla), coontail (Ceratophyllum demersum) and hydrilla (Hydrilla verticillata). To determine decay rates, we used litter bags of two mesh sizes (5 mm and 0.25 mm) and analyzed data with a single exponential decay model. Analysis of decay rates established several trends for aquatic macrophyte decomposition in the ARB. First, macrophytes decayed faster in fall than winter due to the effect of increased temperature. Second, macroinvertebrates were the primary decomposers of macrophytes in riverine sites and microbes were the primary decomposers in backwater areas. These trends may have been related to decomposer-habitat interactions, with well-oxygenated riverine sites more hospitable to invertebrates and backwater areas more favorable to microbes because of high organic inputs and reduced flow. Decay rates for macrophytes, ranked from slowest to fastest, were E. crassipesC. demersum>S. platyphylla>E. crassipes. (Table 1). The initial concentration of highly resistant material (i.e. lignin-cellulose) was higher in E. crassipes, S. platyphylla and H. verticillata than in C. demersum (Table 2). In fresh plant material E. crassipes had the highest ash-free dry mass (AFDM) followed by S. platyphylla, H. verticillata and C. demersum. Based on AFDM, 9–12% of the total weight of the plants was non-organic matter (Table 2). When macroinvertebrates had access to the plant material and fragmentation was permitted (i.e. the coarse-mesh bag treatment) decomposition coefficients ranged from −0.008 d−1 to −0.135 d−1 (Table 1). Plant material in bags that excluded macroinvertebrates and fragmentation (i.e. the finemesh bag treatment) had decay rates that ranged from −0.003 d−1 to −0.042 d−1 . Comparisons of decay
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Figure 2. Decay curves for four plant species in litter bags of two mesh-sizes. Each curve is the average of four replicates. Studies were conducted in the winter and fall in riverine and backwater sites.
129 Table 1. Decay rates (1±SE) determined for four macrophytes using coarse-mesh and fine-mesh bags. Bags were placed in backwater and riverine locations during the winter and fall of 1995. Correlation coefficient (r 2 ) given for the negative exponential curve. Mean study rate is the average decay rate within each season based on water type and litter bag interaction. k=decay coefficient (d−1 ) Backwater SE
Riverine SE
r2
k
±0.001 ±0.001 ±0.003 ±0.001 ±0.003
0.88 0.92 0.62 0.74
−0.008 −0.013 −0.040 −0.040 −0.025
±0.001 ±0.001 ±0.000 ±0.000 ±0.004
0.52 0.90 0.75 0.60
−0.003 −0.012 −0.011 −0.014 −0.011
±0.000 ±0.001 ±0.001 ±0.001 ±0.001
0.90 0.69 0.84 0.94
−0.004 −0.006 −0.008 −0.006 −0.006
±0.001 ±0.001 ±0.000 ±0.001 ±0.000
0.14 0.12 0.72 0.47
Fall, coarse-mesh bag E. crassipes S. platyphylla C. demersum H. verticillata Mean study rates
−0.022 −0.040 −0.029 −0.061 −0.038
±0.003 ±0.002 ±0.003 ±0.003 ±0.004
0.74 0.86 0.21 0.71
−0.019 −0.034 −0.049 −0.135 −0.059
±0.002 ±0.005 ±0.009 ±0.001 ±0.012
0.79 0.52 0.27 0.77
Fall, fine-mesh bag E. crassipes S. platyphylla C. demersum H. verticillata Mean study rates
−0.020 −0.022 −0.030 −0.042 −0.029
±0.001 ±0.001 ±0.002 ±0.002 ±0.002
0.85 0.49 0.89 0.88
−0.015 −0.026 −0.015 −0.027 −0.021
±0.001 ±0.002 ±0.001 ±0.003 ±0.002
0.82 0.97 0.44 0.51
Plant species
k
Winter, coarse-mesh bag E. crassipes S. platyphylla C. demersum H. verticillata Mean study rates
−0.009 −0.010 −0.025 −0.034 −0.019
Winter, fine-mesh bag E. crassipes S. platyphylla C. demersum H. verticillata Mean study rates
rates for the coarse-mesh bag and the fine-mesh bag treatments showed faster decay of S. platyphylla, C. demersum and H. verticillata in the larger mesh-sized bag for both seasons (p0.05; Figure 2). The fastest decay rates recorded for this study were in the fall riverine site for H. verticillata and C. demersum in the coarse-mesh bag. In the coarse-mesh bag treatment in the fall, H. verticillata and C. demersum decayed faster in the riverine sites than backwater sites (p0.05; Table 1). The slowest decay rates in the coarse-mesh bag occurred in the winter for E. crassipes and S.
r2
Table 2. Initial levels of two internal components for the plant species represented as % oven-dried mass. Ash-free dry mass (AFDM) and hydrolysis resistant organic matter (HROM), a cellulose-lignin assay, given as x±1 SE Plant species
AFDM
HROM
E. crassipes S. platyphylla H. verticillata C. demersum
12.1±3.2 10.5±2.5 9.8±2.5 9.1±0.9
42.8±5.8 39.8±2.5 38.2±3.9 26.7±3.3
platyphylla (Figure 2). For the fine-mesh bag treatment in the fall, H. verticillata and C. demersum decayed faster in the backwater than the riverine loca-
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Figure 3. Density of macroinvertebrates per litter bags shown as bars (x±1 SE). Lines indicate percent of original mass remaining (x±1 SE) as an average of E. crassipes, S. platyphylla, C. demersum and H. verticillata. Plants were in coarse-mesh litter bags placed in riverine and backwater locations during two seasons.
tion. For the fine-mesh bag treatment in the winter, H. verticillata, C. demersum and S. platyphylla decayed faster in the backwater than the riverine site (Figure 2, Table 1). Macroinvertebrates Total density of macroinvertebrates on plant detritus were 2–4 times higher in the riverine sites than the backwater sites in both fall and winter (p 0.05). The winter riverine site exhibited the lowest microbial respiration measured during the study. In the backwater site, microbial respiration was extremely elevated on 2 d compared to the riverine site and the other time points. In the fall, microbial respiration rates did not differ between sites, nor over time (p>0.05) and averaged 0.0470 µmol glucose µg−1 h−1 (Figure 5). In the winter, the bacterial density on plant detritus in the fine-mesh bag did not differ between the plant species, E. crassipes and S. platyphylla, or sites (p>0.05; Figure 6). Plant material that had decomposed for 2 d had a bacterial
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Figure 4. NMS procedure showing macroinvertebrates in habitat space for the first three axes. Points indicate site and season combinations and vectors indicate taxa. Hya=Hyallela azteca; Dip=dipterans; Gam=Gammarus spp.; Lir=Lirceus lineatus; Cae=Caecidotea sp.; Can=Caenis sp.
Figure 5. Mean microbial respiration rates (±1 SE) determined with a 14 C tracer method on decomposing E. crassipes and S. platyphylla. Fine-mesh litter bags were located in riverine and backwater sites.
density averaging 1.4×106 cm−2 and the numbers decreased to 2.0×105 cm−2 by the end of the experiment (Figure 6).
Discussion Differences in decay rates between plant species have been related to the structural attributes of the plant tissue (Kulshreshtha & Gopal, 1982; Webster & Benfield, 1986). The highly dissected and fragile plants, H. verticillata and C. demersum, were more prone to fragmentation than the solid blade species, E. crassipes and S. platyphylla. Breakdown rates are dependent on a number of factors including the nutritional value that the plant material provides to microbial and invertebrate detritivores (Petersen & Cummins, 1974). E. crassipes had the slowest decay of the four plant types, probably due to high levels of lignocellulose
Figure 6. Bars indicate the average density (±1 SE) of bacteria on two plant species, E. crassipes and S. platyphylla. Plants were in fine-mesh bags located in riverine and backwater sites during the winter experiment. For each date, three samples of both plant species were measured.
132 Table 3. Reported decay rates (k) for hydrilla (Hydrilla verticillata), coontail (Ceratophyllum spp.), and water hyacinth (Eichhornia crassipes) Species
Temp. or season
H. verticillata H. verticillata
18–22 ◦ C 12 ◦ C 28 ◦ C
C. demersum C. demersum C. echinatum C. demersum
10 ◦ C 18 ◦ C 16–18 ◦ C 18–22 ◦ C 12 ◦ C 28 ◦ C
E. crassipes E. crassipes E. crassipes
28 ◦ C July–Nov. 20 ◦ C
E. crassipes
28 ◦ C
E. crassipes E. crassipes
25–34 ◦ C 12 ◦ C 28 ◦ C
k (d−1 )
Experimental conditions
Source
−0.020 −0.010† −0.037† −0.035† −0.098† −0.033 −0.042 −0.021 −0.066 −0.009† −0.032† −0.023† −0.039† −0.022 −0.006 −0.028 −0.039 −0.009 −0.013 −0.030 −0.003† −0.008† −0.018† −0.020†
Laboratory microbial Swamp microbial Swamp Swamp microbial Swamp Laboratory microbial Laboratory microbial Laboratory microbial Laboratory microbial Swamp microbial Swamp Swamp microbial Swamp Laboratory microbial Experimental ponds River microbial River Laboratory microbial Lake Lake Swamp microbial Swamp Swamp microbial Swamp
Kulshreshtha & Gopal, 1982 This study
Best et al. 1990 Bastardo, 1979 Kulshreshtha & Gopal, 1982 This study
Singal et al. 1993 Reddy & DeBusk, 1991 Bartodziej, 1992 Gaur et al. 1992 Howard-Williams & Junk, 1976 This study
†Value based on average of riverine and backwater sites.
and a waxy-cutin outer layer (Table 2). Initial level of nitrogen is also an indication of the value of the plant as a food source (Webster & Benfield, 1986). A review of the literature indicated that nitrogen concentrations from lowest to highest were E. crassipes (1.7%), H. verticillata (2.3%), C. demersum (2.8%) and S. platyphylla (3.2%) (Karim, 1948; Langeland, 1982; Sutton & Portier, 1983; Sutton & Portier, 1991; Newman, 1991; Zimba et al., 1993). E. crassipes decay rates did not differ in the presence or absence of invertebrates, which suggests that leaching and microorganisms were responsible for the majority of E. crassipes decay. This conclusion is supported by Gaur et al. (1992) who found that in the presence of microbes the decay rate of E. crassipes was double that of a non-microbial treatment. Still, microbial breakdown of E. crassipes was very slow compared to the other plant types, suggesting that detritus unpalatable to invertebrates is also resistant to microbial colonization (Bärlocher & Kendrick, 1981).
Our practice of pre-drying the plants may have altered the natural decay process (Gessner, 1991). Bärlocher & Biddiscombe (1996) measured fungal biomass up to five times higher on aerial leaf parts than those submersed and suggested early decomposition of emergent plants occurs while the plant is still located above the water and bacterial processes become dominant when emergent plants enter the water. Therefore our methods of pre-drying may have underestimated the contribution of fungi in decay, especially for emergent plants (Newell et al., 1995; Bärlocher & Biddiscombe, 1996), and accelerated leaching for all plant species (Gessner, 1991). Nonetheless, decay rates from this study were comparable to studies in other regions that examined different aquatic macrophyte species (Hill & Webster, 1982; Kulshreshtha & Gopal, 1982; Chergui & Pattee, 1990; Bianchi & Findlay, 1991). Comparison of similar plant species also showed that our decay rates corresponded to what others have reported (Table 3).
133 Macroinvertebrate assemblages showed distinct patterns between seasons and habitats during this study. In winter, amphipods and isopods were the predominant taxa in both habitats. High densities of isopods only occurred in winter (J. Battle, personal observation) implying that these detritus feeders have adapted their life history to the annual input of organic material. Amphipods, Hyallela azteca and Gammarus spp., are omnivore-detritivores (Merritt & Cummins, 1996) and inhabit vegetation and debris throughout the ARB. Bartodziej (1992) found that H. azteca and Gammarus trigrinus substantially increased decay of E. crassipes. Similarly, Kaushik & Hynes (1971) observed that Gammarus spp. significantly contributed to decay of allochthonous detritus. The mayfly Caenis, a prevalent insect in the backwater during fall and winter, is documented to prefer sediments in littoral regions of lentic habitats (Merritt & Cummins, 1996) and is capable of inhabiting oxygen-stressed habitats because it has a large gill surface area (Berner & Pescador, 1988). By living in a stressful environment, Caenis is able to avoid competition and predation by other macroinvertebrates, but is supplied with an abundant food source that may be lacking in riverine areas because river flow can rapidly remove organic material. H. azteca and dipterans, composed mainly of chironomids, were major contributors to decay in the fall riverine site. Dipterans are recognized as a group of ecologically important aquatic insects that feed on a variety of detrital materials (Pinder, 1986). In general, patterns in macroinvertebrate assemblages between habitat and season during these experiments reflected differences in physical and chemical characteristics between backwater and riverine habitats in the ARB and seasonal life history traits of macroinvertebrates in the ARB. To some extent, macroinvertebrate density and composition differences likely had an effect on observed differences in plant mass loss. For example, the riverine site had a higher macroinvertebrate density, primarily detritivorous amphipods and higher decomposition rates than the backwater sites. This suggests that the higher density of macroinvertebrates in riverine sites is increasing plant mass loss by consumption and fragmentation. Processing of macrophytes by microorganisms was slower in winter than fall most likely due to substantially lower temperatures. It has been well documented that reduced temperatures can decrease microbial metabolism (Bärlocher & Kendrick, 1974; Moran & Hodson, 1989). Yet, both the fall and winter backwater sites had similar microbial respiration on macrophyte
species. The high microbial respiration recorded in the winter backwater site may be explained by the fact that the water level was rising at this time (Figure 1). Edwards & Meyer (1986) found that in a large floodplain river in Georgia, bacterial numbers increased as water levels rose and were greatest during the first flood of the season. In winter, the backwater area had more elevated microbial respiration associated with the detrital samples than the riverine site and this accounted for the faster decay rates by microorganisms in the backwater location (Table 1). Microorganisms most likely flourished in stagnant backwater areas because there is an abundant energy source provided by decaying autochthonous matter (i.e. macrophytes, phytoplankton, periphyton), allochthonous material from the floodplain and dissolved organic matter derived from leaching. In the fall experiment, no positive relationship was detected between microbial respiration and decay rates. We found that plants had faster decay by microbes in backwater than riverine sites, but microbial respiration rates on macrophytes did not differ between habitat types. A possible explanation for the lack of correlation is that the hypoxic conditions in the backwater site caused the establishment of an anaerobic microbial community and their respiration could not be detected by our assay. Most likely, microbes in the backwater were facultative anaerobic bacteria that adapted their metabolism to grow either in the presence or absence of oxygen using fermentation or anaerobic respiration. The initial high microbial respiration rates measured in this study suggests that microorganisms were quickly colonizing the detritus and removing the labile products, but then rates slowed as the substrate became more refractory. Hargrave (1972) reported that oxygen consumption of microorganisms colonizing Phragmites detritus increased up to the second or third day and fell to a stable level by 7 d; we measured similar patterns of microbial respiration. Respiration rates may have also decreased in later stages of decay because of overcrowding of microorganisms (Hargrave, 1972; Naiman, 1983). During initial decomposition of leaves it has been found that fungi tend to be dominant and bacteria are important in later stages (Suberkropp & Klug, 1976). In our study bacteria colonized rapidly (1.4×106 cm−2 by 2 d) and then declined to 2.0×105 cm−2 after 28 d. Average bacteria density we reported was also lower then those reported for allochthonous inputs (Bengtsson, 1992; Sridhar & Bärlocher, 1993; Baldy et al.,
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Figure 7. Simple diagram indicating the distribution of mass loss for aquatic macrophytes in the ARB during winter and fall. The four plant species were averaged to determine a mean mass loss caused by microbes and other agents (animals and fragmentation) for the last day of each experiment. Leaching was the average mass loss of the four plant species that occurred the first day they were in the water during the fall experiment. Unprocessed indicates amount of material remaining at the end of the experiment. To calculate percentages: ‘microbes’=[initial mass (100%) – leaching (28%)] – % mass remaining in fine-mesh bag, and ‘other agents’=‘microbes’ – % mass loss for coarse-mesh bag.
1995) and for C. demersum (Underwood, 1991). The fast colonization rate and rapid decline in density may be due to deleterious effects of the small mesh-size of the litter bags. Bags of such fine-mesh material may have resulted in reduced flow over plant material and provided a surface for microbes to colonize and thereby altered the microhabitat (Petersen & Cummins, 1974). The role of bacteria, as well as fungi, in the decay of macrophytes in the ARB is an area for future research. To examine decay of macrophytes in the ARB incorporating temporal and spatial features we designed a simple diagram (Figure 7). The diagram distributes mass loss into different compartments: leaching, microbes, other agents (animals and fragmentation), and unprocessed material. Macrophytes exposed to other agents in riverine habitats had equal or greater mass loss than plants processed by microbes exclusively. Greater mass loss of plant material by other agents in riverine sites compared to backwater sites is most likely attributed to the higher macroinvertebrate density (Merritt & Lawson, 1979). This suggests that the role of macroinvertebrates in plant breakdown differs among habitats and emphasizes the importance of invertebrates in decomposition processes in
riverine habitats. High macroinvertebrate numbers in riverine areas may be a product of the constant flow that provides well-oxygenated waters and allows continual colonization by invertebrates. In addition, the high macroinvertebrate density and strong current in riverine habitats may be a source of significant biotic and abiotic fragmentation. In contrast, backwater areas seasonally have low D.O. levels and minimal flow that might prevent establishment of some invertebrates. Furthermore, we found that other agents caused greater mass loss in the winter than the fall, probably because winter temperatures did not inhibit the ability of invertebrates to process material. Microorganisms contributed to a larger portion of plant loss in backwater areas than in riverine sites (Figure 7). Riverine sites have high turbidity (Davidson, 1996) and microbes may have contributed less to the decay of plants due to the effects of sedimentation, which can limit the activity of microorganisms and compact the litter (Vargo et al., 1998). Apart from the decomposition of plant material, bacteria can seriously influence large river systems (Edwards & Meyer, 1986). Bacteria can deplete oxygen levels in low-flow backwater areas, thereby altering species composition and establishment of aerobic organisms.
135 Decomposer microbes may also modify the system by recycling carbon (Rich & Wetzel, 1978) and nutrients (Weibe, 1979) that can be vital to macrophytes and other organisms living on the periphery of backwaters. The mosaic of anaerobic and aerobic conditions in backwater and riverine habitats may help explain the high productivity of southern river-floodplain systems (Lambou, 1990).
Acknowledgements We extend thanks to Frank Spiess, Becky Jesse and James Mancuso for their help in the field and laboratory. S. Golladay and several anonymous reviewers provided useful comments. We are grateful to K. Carman and S. Pomeranko for their advice and use of their laboratory in completing the microbial part of this study. Funding for this project was provided by Federal Emergency Management Agency through the U.S. Fish and Wildlife Service and the Louisiana Department of Wildlife and Fisheries. Additional assistance was provided by the Louisiana Cooperative Fisheries and Wildlife Research Unit and Louisiana State University School of Forestry, Wildlife, and Fisheries. Support in preparing this manuscript was provided by the Joseph W. Jones Ecological Research Center.
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