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0 Department of Biological Sciences, University of Alabama, Tuscaloosa, Alabama 35487-0206 USA
Received for publication March 11, 1999. Accepted for publication August 24, 1999.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Key Words: allelochemical interactions • allelopathy • autotoxicity • Cyperaceae • Juncaceae • Juncus effusus.
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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). Competitive interactions of both types have been extensively examined (e.g., Thijs, Shann, and Weidenhamer, 1994
; Inderjit, 1998
; Levine, Brewer, and Bertness, 1998
, and numerous additional works reviewed by Gopal and Goel, 1993
and Einhellig, 1995
), and studies exist in which both exploitation and allelopathy were examined simultaneously (e.g., Nilsson, 1994
; Thijs, Shann, and Weidenhamer, 1994
; Inderjit, 1998
). Comprehensive studies such as these are instructive because: (1) allelochemical release may be intimately linked to exploitative competition by influencing soil chemistry (Inderjit, 1998
), and (2) competition and allelopathy may be complementary in their contributions to plant species interactions (Nilsson, 1994
). Because of the coupling between physical and chemical processes in natural systems, elucidation of both types of interaction is necessary to fully appreciate structuring mechanisms in plant communities.
Although recent research into allelochemical interactions has increasingly improved, largely the result of modern technological advances, relatively few recent studies have indicated autotoxicity among plants (Einhellig, 1995
; Elakovitch and Wooten, 1995
; Gopal and Goel, 1993
). This paucity persists despite a suggestion that allelochemical autotoxicity may be a common phenomenon (Edwards et al., 1988
). Terrestrial examples of autotoxicity deal primarily with seed germination in food species (e.g., studies of fig, grape, peach, and sunflower mentioned by McNaughton, 1968
) or weeds, such as pokeweed (Phytolacca americana; Edwards et al., 1988
). Reports of autotoxicity in aquatic systems have been cited for a number of algae (Inderjit and Dakshini, 1994
), ferns (Osmunda spp.; Elakovich and Wooten, 1995
), and higher plant taxa such as Typha (McNaughton, 1968
; Grace, 1983
), Phragmites (Gopal and Goel, 1993
), and Cyperus (Elakovich and Wooten, 1995
). Reports such as the latter are important because many of these higher aquatic plants are clonal in nature and rely heavily upon vegetative growth for maintaining large populations (Grace, 1993
; Eriksson, 1997
).
Juncus effusus (Juncaceae; hereafter, Juncus) is a cosmopolitan, clonal emergent freshwater macrophyte. Juncus frequently occurs in populations of dense tussocks (Godfrey and Wooten, 1981
), all or many of which may be of the same genotype and thereby constitute a single genet. Within a single tussock, individual culms (terete in cross section) of this plant sometimes exceed 1.5 m in height with basal diameters to ~0.3 cm (Godfrey and Wooten, 1981
; G. Ervin and R. Wetzel, unpublished data). Juncus has been shown to produce a net average of ~7 kg ash-free dry mass (AFDM) per square metre per year in aboveground biomass (Wetzel and Howe, 1999
), one of the highest published estimates in any plant community. In the same study, when belowground productivity was included, total productivity estimates were as high as 9.8 kg AFDM·m-2·yr-1. In addition to that evidence of relatively stable biomass that resulted from continuous growth of multiple, overlapping cohorts throughout the annual cycle for Juncus populations, Ervin and Wetzel (1997)
described rapid above- and belowground growth for individual ramets. Although shoot biomass increased by as much as 525%, shoot:root ratios decreased from 3.68 to 0.64 in <100 d. Such a change corresponds to ~3500% increase in belowground biomass, indicative of the extremely high subterranean productivities in this species. The high above- and belowground productivity of Juncus suggests strongly the potential for competitive dominance (sensu Grime, 1979
) in this species.
In addition to possessing the competitive traits cited above, Juncus also contains numerous chemical compounds that may allow this species to employ allelochemical interference. Phenolic compounds such as p-coumaric and vanillic acids (Dong-Zhe et al., 1996
) and cycloartane triterpenes, cycloartane glucosides, and 9,10-dihydrophenanthrene glucosides (Corsaro et al., 1994
; Della Greca et al., 1994, 1995
) have been reported from Juncus. Many such compounds have been shown to possess allelochemical activities (Gopal and Goel, 1993
; Einhellig, 1995
). Most of these chemical analyses have been performed on dried aboveground tissues of Juncus, which are abundant year-round from continuous cohort turnover in ecosystems dominated by this plant (Wetzel and Howe, 1999
). Furthermore, the numerous standing-dead culms of plants in the Juncaceae have been shown to be some of the most slowly decomposing leaf material in freshwater ecosystems (Webster and Benfield, 1986
; Kuehn and Suberkropp, 1998
). The rapid rates in production and senescence of aboveground tissues, coupled with their very slow decomposition, provide extremely high potential for inter- and intraspecific allelochemical interaction with neighboring plants in Juncus-dominated wetland ecosystems.
The objective of the present research was to determine the contribution of chemical interactions toward dominance of Juncus over species from the Cyperaceae found growing sympatric with, but subordinate to, Juncus. Research presented here is part of a broader program initiated to explore whether physical or chemical characteristics of Juncus are more influential in allowing this species to dominate southeastern wetland ecosystems.
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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). After a 14-d leaching period, leachate was passed through a 0.25-mm mesh Nitex sieve to remove large particulate materials and then through GF/F filters (precombusted, 500°C; 0.7-µm pore size), atop which was placed precombusted (500°C) glass wool to aid in removal of remaining large particles of detritus. Filtered leachate was then lyophilized (Virtis Unitop 600L, Virtis Co., Gardiner, New York, USA) and stored under vacuum desiccation until use. Organic carbon content of the lyophilized material was 0.38 ± 0.08 mg C/mg leachate (mean ± 1 SD). These values were obtained via total organic carbon (TOC) analyses with a Shimadzu TOC-5000 TOC analyzer (Shimadzu Scientific Instruments, Inc., Kyoto, Japan) as follows. Lyophilized extracts were dissolved in ultrafiltered, deionized water and acidified with 100 µL 2 mol/L HCl per 5.0 mL extract solution. This solution was sparged with nitrogen gas to remove dissolved inorganic carbon. Subsamples (21 µL) were withdrawn automatically and combusted at 680°C to convert all nonpurgeable organic carbon to CO2. Carbon dioxide was detected by a nondispersive infrared gas analyzer and concentration was calculated by integration from the detection signal.
Bioassay species
Juncus seeds were collected during late spring of the previous year from the TWE by removing entire inflorescences from culms that had begun to senesce. Inflorescences were collected only from culms on which senescence had progressed to 
1 cm below the point of attachment of the inflorescence. Seeds were stored in dark at 4°C until used in the experiments.
Scirpus cyperinus (Cyperaceae; hereafter, Scirpus) is perennial sedge found in wetlands throughout eastern Canada and the United States and is tussock-forming, characterized by tall (1–2 m) scapes bearing inflorescences of 200–500 individual spikelets. Achenes of Scirpus are three-angled and pale in color, with six relatively long perianth bristles that protrude from the spikelet (Godfrey and Wooten, 1981
). Achenes were harvested in spring of the previous year by removing intact inflorescences from plants in both the TWE and a small wetland near Lake Grace in eastern Tuscaloosa County (Alabama, USA) and were stored immediately in dark at 4°C.
Eleocharis obtusa (Cyperaceae; hereafter Eleocharis) is an annual species of sedge that occurs in shallow waters and along edges of emergent wetlands in both the eastern and western thirds of the United States and Canada. Eleocharis grows to ~0.5 m in height in dense tussocks of hundreds of individual culms. Spikes are simple and borne individually at the apices of the culms. Achenes are biconvex and typically 1–1.5 mm long (Godfrey and Wooten, 1981
). Achenes were collected during summer of the previous year in the TWE only from spikes atop culms that had begun to senesce. Achenes were then stored in dark at 4°C.
Seed sterilization
Prior to incubation, seeds (achenes) were surface sterilized according to the method of Wetzel and McGregor (1968)
. After 15 rinses in ultrafiltered, deionized water (pyrogen-free, >18 MOhm/cm), seeds were desiccated in 70% ethanol for 3–5 min on a rotary shaker at low speed (<100 rpm). Ethanol was then decanted, 5.25% sodium hypochlorite (bleach, undiluted) was added, and seeds were washed in this solution for 40 min on a wrist-action shaker at full speed. Following the hypochlorite treatment, seeds were rinsed an additional three times with autoclaved, ultrafiltered deionized water. All handling of seeds during and after sterilization was performed within a sterile laminar flow hood using axenic techniques.
Growth conditions
After surface sterilization, several seeds were transferred aseptically to each well of sterile 24-well cell culture plates that contained 1.0 mL of either 100% Hoagland's solution (controls; Hoagland and Arnon, 1938
) or 100% Hoagland's solution amended with lyophilized leachate from Juncus (treatment, see below). Because of variability in seed sizes, numbers of seeds varied by species from a maximum of approximately ten Juncus to a minimum of 4–6 Eleocharis/well.
Plates were maintained in growth cabinets (pH Environmental, North Billerica, Massachusetts, USA and Percival, Boone, Iowa, USA) for the duration of the experiment. Cabinets were maintained at 29°C with light supplied by 20-W fluorescent bulbs, supplemented by 20-W Gro-Lux bulbs (Osram Sylvania, Danvers, Massachusetts, USA) at 80 µmol·m-2·sec-1 photosynthetically active radition (PAR; 14 h light/10 h dark) at the level of the plates. Seeds were grown for ~3 wk prior to subsamples being harvested for mass and pigment analyses. At 4–7 d intervals, the media in the plates was either augmented with 0.5-mL ultrafiltered, deionized water (days 6 and 17) or completely drained and replaced with media of the original composition (100% Hoagland's or Hoagland's plus leachate; day 10) to compensate for evaporation.
In the first set of growth experiments (sensitivity assays), treatment solutions for bioassay of species sensitivity to leachate material were mixed at a concentration of ~31 mg lyophilized material per 1.0 L of 100% Hoagland's solution, to yield a TOC concentration of 11.8 ± 2.5 mg C/L (mean ± 1 SD). These values were well within limits measured in the surface and interstitial waters surrounding tussocks of Juncus in the TWE (Mann and Wetzel, 1995
).
To examine Juncus autotoxicity indicated by the sensitivity assays, a second set of experiments (dose response assays) examined the effects of leachate preparation and concentration on Juncus seedlings only. Bioassay treatment solutions were prepared from lyophilized Juncus leachates previously used for sensitivity analyses (lyophilized leachate, LL), and by sterile filtration only of Juncus extracts (0.22-µm pore size membrane filters; nonlyophilized leachate, NL). An additional source of leachate was 100% Hoagland's medium in which Juncus seeds had been germinated and allowed to grow for 14 d (seedling leachate, SL). This final leachate preparation method was used because of microbial responses observed in earlier, nonaxenic seed germination experiments in which Juncus seedlings appeared to inhibit algal growth. Leachate materials were added to growth media at the concentrations shown in Table 1. Solution for SL treatments were at dilutions of 25, 50, and 75% in full-strength Hoagland's solution and at 100% SL solution.
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Chlorophyll a, as opposed to chl b or a combination of chl a and b, was selected as the assay pigment for a number of reasons: (1) chl a is a biosynthetic precursor of chl b (Falkowski and Raven, 1997
), (2) chl a molecules outnumber chl b from 1.4 to 4.4 in the photosystem complexes of higher plant chloroplasts (Dey and Harborne, 1997
), and (3) chl a serves in both light-harvesting and photochemical reactions, whereas chl b functions solely in light harvesting (Dey and Harborne, 1997
).
Chlorophyll a content (micrograms chl a per milligram plant mass) for each sample was determined by modifications to the phytoplankton method of Wetzel and Likens (1991)
, as follows. Seedlings in each sample were counted and weighed as above, and then stored in polypropylene centrifuge tubes wrapped in foil at -20°C for 6 d. Once the tubes were removed from storage, 2.0 mL of 90% alkaline acetone (4°C) were added to each tube. All preparations for extraction were conducted in a semidarkened room in a fume hood. Seedlings were then sonicated (Kontes ultrasonic cell disrupter, Kontes Scientific Instruments, Vineland, New Jersey, USA) at 0°C on a setting of 30 by sonicating 10 s, pausing 10 s, then sonicating an additional 10 s. The tubes were then placed on a rotary shaker in a darkened cold room (6°C) for 18–24 h. After the extraction period, samples were returned to the semidarkened laboratory and analyzed as per Wetzel and Likens (1991)
on a Beckman DU 650 Spectrophotometer (Beckman Instruments, Inc., Fullerton, California, USA).
Statistical analyses
Seedling mass and chlorophyll a concentration were analyzed with one-way ANOVA for differences among treatments, and Bonferroni pairwise comparisons were used to determine significantly different levels of treatments (Data Desk® 6.0, Data Description, Inc., Ithaca, New York, USA). Seed germination and shoot development were analyzed with repeated-measures MANOVA, with Bonferroni comparisons used to determine significantly different levels within treatments. Software used for these tests automatically compensated for unbalanced ANOVA designs. Percentage differences between controls and leachate treatments are reported as mean difference ± 1 SE (two-sided t test; SigmaStat® version 1.0 for Windows, Jandel Corporation, Erkrath, Germany).
All data were examined for satisfaction of equal variance and normality test assumptions. Normal probability plots and the Kolmogorov-Smirnov test were used to examine data for normality. Equal variance was examined with studentized residuals vs. predicted value plots and Levene's median test. For all significant differences reported, data passed these tests for normality and equal variance with an alpha value of 0.05 or better.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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0.013, Fig. 1B), leachates caused no significant reduction in Scirpus seedling chlorophyll a concentration (P 0.48; Fig. 1B). Neither Eleocharis nor Scirpus showed a significant reduction in mean seedling mass in the leachate treatment (P 0.26 for Eleocharis, and P 0.065 for Scirpus with a reduction of 39 ± 18% in Scirpus seedling mass; Fig. 1A).
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0.01; Fig. 1A) in the leachate treatment, as compared to controls. Chlorophyll a concentration in the Juncus seedlings was reduced by 42 ± 4% (P 0.0007, Fig. 1B) with the addition of leachate. As mentioned above, there was no significant difference in germination between the control and leachate-treated Juncus seeds (Fig. 2A). On day 8 of the experiment, only one out of 330 seedlings in the leachate treatment had formed a second leaf, whereas 37% of control seedlings had formed at least two leaves (Fig. 2B). This difference remained statistically significant through day 17 of the experiment (P 0.032).
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0.0007) in LL-exposed seedlings and 63 ± 10% (P 0.0011) in NL-exposed seedlings, compared to controls (Fig. 3A). No significant differences were found for mean seedling mass between the NL and LL treatments.
Seedling chl a content exhibited a 43 ± 1% (P 0.0001) decrease from controls in the LL treatment. In NL seedlings, chl a concentration decreased 31 ± 3%, compared to controls (P 0.0001; Fig. 3B). Additionally, LL seedling chl a concentration was 17 ± 4% lower than in the NL treatment (P 0.037).
As in the sensitivity analysis, no significant differences in seed germination were found among treatments or concentrations (Table 4, Figs. 4A, 5A). There were, however, significant delays in formation of the second leaf in both the NL and LL treatments (repeated-measures MANOVA P 0.0001 for each; Figs. 4A, 5A). These differences agreed with those in the chl a analyses in that LL seedlings experienced a longer significant reduction in shoot development than NL seedlings (Table 5; Figs. 4B, 5B). In LL seedlings, the percentage of seedlings with two leaves was significantly lower than in controls through day 14 (P 0.0001). In NL seedlings, however, the significant difference between leachate-treated and control plants persisted only through day 10 (P 0.003).
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Calculations based on data from Wetzel and Howe (1999)
, Grime, Hodgson, and Hunt (1990)
, and unpublished field data (G. Ervin and R. Wetzel) provide estimates of <1% to <7% allocation of annual net productivity to seed production in this species. However, in our field studies of this species conducted during March through August 1998, no Juncus seedlings were observed within 40 cm of isolated, established ramets, despite the above-estimated production of more than 4 x 106 seeds ·m-2·yr-1. During the same study period, seedling emergence was recorded for >20 other species within 40 cm of observed ramets. Germination in Juncus effusus is sensitive to shading by neighboring plants and to desiccation (Richards and Clapham, 1941
; Lazenby, 1955
), two conditions to which seedlings would have been exposed during the 1998 study. Experimental removal of shading from sediments surrounding Juncus ramets in March through June 1999 permitted Juncus seed germination, but seedlings displayed inhibition of second-leaf formation that could not be explained by shading alone.
Results of the present study are reminiscent of those encountered by McNaughton (1968)
and Grace (1983)
in studies of autotoxicity in the competitive wetland macrophyte Typha latifolia. In those earlier experiments, it was noted that growth of Typha seedlings was diminished when incubated with aqueous extracts from aboveground Typha tissues. It was further proposed by McNaughton (1968)
that autotoxicity was responsible for the absence of Typha seedlings within mature stands. However, other researchers have since suggested competition, particularly competition for light, to be at least as important as autotoxicity in preventing establishment of Typha seedlings within these stands (see Gopal and Goel, 1993
). Photosynthetically active radiation reaching the sediments was shown to be as low as 15% of above-canopy PAR in dense stands of Typha (Grimshaw et al., 1997
).
Proposed reasons for a given species to exhibit autotoxicity vary. Autotoxicity was suggested by McNaughton (1968)
to be important in the "unidirectional modification" of plant communities. However, such strategy could be accomplished through general allelopathic interference while still allowing for intraspecific seedling establishment. A more logical reason for the presence of autotoxicity, especially in highly competitive plant species, is its potential role in spatial or temporal dispersal of seed germination and seedling establishment (Edwards et al., 1988
). For species whose germination is inhibited by autotoxins, this strategy would avoid intraspecific competition between adults and seedlings. However, in species whose seeds are allowed to germinate in the presence of autotoxins, such as Juncus effusus, this is an unlikely mechanism for dispersal.
Seeds of Juncus sink in water and thus are quickly buried within sediments in low-gradient wetland ecosystems, where they establish persistent seed banks (Grime, Hodgson, and Hunt, 1990
). Following disturbance, these seed banks can regenerate former Juncus populations. Evidence of this phenomenon was encountered in the TWE in 1997, after an extreme spate caused the destruction of a beaver dam. Resulting drainage of a previously long-lived impoundment was followed by colonization of much of the exposed wetland sediments by Juncus seedlings. This series of events supports hypotheses offered by Edwards et al. (1988)
and Grace (1983)
, wherein autotoxicity functions in temporal dispersal of seedling establishment and population regeneration after disturbance. In Juncus, dispersal through time likely is accomplished by the combination of rapid seed burial and prevention of seedling establishment by both shading and autotoxicity.
Interspecific effects
The only interspecific growth suppression detected in these studies was the slight reduction in chl a concentration in Eleocharis seedlings. However, these experiments examined interactions of Juncus with only two other species, and only aqueous extracts from aboveground tissues were used as the source of potential allelochemicals. Eleocharis obtusa and Scirpus cyperinus were chosen for these assays because these two species displayed the closest negative correlation with Juncus abundance in 1997 vegetation surveys of the TWE. Although the present study did not indicate allelochemical interactions between Juncus and either of these species, allelochemistry cannot be ruled out as a potential structuring mechanism in these communities because these studies used only aqueous extracts from aboveground tissues.
Aqueous extracts were used in this research for two primary reasons. First, all natural leaching of potential allelochemicals from the large quantities of aboveground tissues of Juncus (~4 kg AFDM/m2 at any one point in time; Wetzel and Howe, 1999
) is induced by water. Leaching from aerial plant tissues is caused by precipitation, and extraction continues within surface waters after collapse and submersion of dead material (Mann and Wetzel, 1996
; Kuehn and Suberkropp, 1998
; Kuehn et al., in press
). Second, much previous research has successfully isolated and identified allelochemical agents from aqueous extracts of plant tissues. Recent examples are studies on root interaction among desert shrubs (Mahall and Callaway, 1992
), attractional compounds released from roots of crop plants (Vierheilig et al., 1998
), and the numerous species of aquatic plants surveyed by Elakovich and Wooten (1995)
.
Although many water-soluble compounds have been shown to possess allelochemical activity, many other compounds that are either insoluble or only somewhat soluble in water recently have been demonstrated to induce allelochemical responses. Low-solubility sesquiterpene lactones were implicated as germination stimulants in witchweed (Striga asiatica; Fischer et al., 1990
). Terpenoid compounds were again shown to be allelopathically active by Inderjit, Muramatsu, and Nishimura (1997)
in both agar and soil bioassays. Finally, a submersed aquatic plant, Ceratophyllum demersum, was shown by Bankova et al. (1995)
to contain allelopathic phenolic, volatile, and sesquiterpene compounds.
Many studies have shown that roots are influential in plant–plant and other types of interspecific chemical interactions. Studies on chemical signaling among desert shrubs (Mahall and Callaway, 1992
) indicated a strong influence of belowground chemical interactions in structuring desert plant communities. Furthermore, these interactions were often mediated by water-insoluble signals. Root exudates of several weed species were shown to affect growth of soybean (Pope, Thompson, and Cole, 1985
), and belowground interactions among grasses were implicated in observed changes in clonal morphology (Huber-Sanwald, Pyke, and Caldwell, 1997
).
Based on results of the present study, autotoxicity appears to be the primary function of allelochemicals contained within aqueous extracts of aboveground Juncus tissues. It is not known, however, whether allelochemicals from other tissues of this plant or with different water solubility influence the productivity of sympatric wetland species. Because of the high belowground productivity in Juncus, it is plausible that root exudates could interact with neighboring plants. Furthermore, present knowledge that aboveground tissues of Juncus contain water-insoluble cycloartane triterpenes (Della Greca et al., 1994
) indicates that water-insoluble, biologically active compounds merit further investigation in this plant. In order to fully understand the mechanisms responsible for structuring Juncus-dominated wetland ecosystems, further multifaceted studies will be required, such as those suggested by Nilsson (1994)
, Thijs, Shann, and Weidenhamer (1994)
, and Inderjit (1998)
.
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FOOTNOTES |
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2 Author for correspondence, current address: Department of Entomology, University of Arkansas, Fayetteville, Arkansas 72701 USA.
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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