Bulletin of Entomological Research (2003) 93, 393–401
DOI: 10.1079/BER2003255
Seasonal variation in the effectiveness of the leaf-feeding beetle Zygogramma bicolorata (Coleoptera: Chrysomelidae) and stem-galling moth Epiblema strenuana (Lepidoptera: Tortricidae) as biocontrol agents on the weed Parthenium hysterophorus (Asteraceae) K. Dhileepan* Tropical Weeds Research Centre, Queensland Department of Natural Resources and Mines, Charters Towers, Queensland 4820, Australia
Abstract Variation in the effectiveness of biocontrol agents on the weed Parthenium hysterophorus L. was evaluated at two properties (Mount Panorama and Plain Creek) in Queensland, Australia for four years (1996–2000) using a pesticide exclusion experiment. At Mount Panorama, higher levels of defoliation by the leaffeeding beetle Zygogramma bicolorata Pallister and galling by the moth Epiblema strenuana Walker in 1996–97 coincided with an above average summer rainfall, but in the following three years with below average summer rainfall the defoliation and galling levels were significantly lower. Biocontrol had significant negative impact on the weed only in 1996–97 with no major impact in the following three years. At Plain Creek, galling by E. strenuana was evident in all the four years, but varied significantly between years due to non-synchrony between P. hysterophorus germination and E. strenuana emergence. At Plain Creek biocontrol had limited impact on the weed in 1996–97 and 1997–98, with no significant impact in the following two years. Over the 4-year period, defoliation and galling resulted in 70% reduction in the soil seed bank at Mount Panorama, but the reduction in the soil seed bank at Plain Creek due to galling was not significant. Effectiveness of Z. bicolorata and E. strenuana was dependent on weather conditions and as a result had only limited impact on the weed in three out of four years.
Introduction Since the beginning of the 19th century approximately 949 exotic agents have been released as weed biocontrol agents worldwide, and the number of weeds targeted for * Present address: Alan Fletcher Research Station, Queensland Department of Natural Resources and Mines, PO Box 36, Sherwood, Qld 4075, Australia Fax: 61 7 33796815 E-mail:
[email protected]
biocontrol is steadily increasing (Julien & Griffiths, 1998). The degree of success achieved by weed biocontrol programmes has been less than 50%, with annual herbs the least successful group of weed (Straw & Sheppard, 1995). The majority of evaluations of the effectiveness of weed biocontrol agents have focused on subjective assessment (Crawley, 1989), on performance of the biocontrol agents or on the effects at plant level (McClay, 1995). Fewer studies have examined the effectiveness of biocontrol at the weed population level and seldom were long-term impacts studied (Huffaker & Kennett, 1959; Moran & Hoffmann,
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1989; McEvoy et al., 1991; Morris, 1997; Hoffmann & Moran, 1998; Blossey & Skinner, 2000; Kok, 2001). Parthenium hysterophorus L. (Asteraceae), commonly known as parthenium, is an annual herb native to the Gulf of Mexico and central South America, and has become widespread in North America, South America, the Caribbean and many parts of Africa, Asia and Australia (Navie et al., 1996). In Australia, parthenium mainly occurs in Queensland affecting 170,000 km2 of prime grazing country and causes severe economic, health and environmental problems (Chippendale & Panetta, 1994; McFadyen, 1995). In a biological control project to control parthenium, nine species of insects and two rust fungi have been introduced since 1980 (Dhileepan & McFadyen, 1997; McFadyen, 2000). Among these, the stem-galling moth Epiblema strenuana Walker (Lepidoptera: Tortricidae), the leaf-feeding beetle Zygogramma bicolorata Pallister (Coleoptera: Chrysomelidae), the stem-boring weevil Listronotus setosipennis Hustache (Coleoptera: Curculionidae), the seed-feeding weevil Smicronyx lutulentus Dietz (Coleoptera: Curculionidae), the leaf-mining moth Bucculatrix parthenica Bradley (Lepidoptera: Bucculatricidae), the stem-galling weevil Conotrachelus albocinereus Fiedler (Coleoptera: Curculionidae), the root-boring moth Carmenta ithacae (Beutenmüller) (Lepidoptera: Sesiidae), winter rust Puccinia abrupta var. partheniicola (Jackson) Parmelee (Basidiomycotina: Uredinales) and summer rust Puccinia melampodii Dietel & Holway (Basidiomycotina: Uredinales) are known to have established in the field (Dhileepan & McFadyen, 1997; McFadyen, 2000; Dhileepan, 2001). The impact of L. setosipennis in the field was limited (Dhileepan, 2003), and only E. strenuana and Z. bicolorata have had any measurable negative impact on the weed (Dhileepan, 2001). In spite of these agents being active in the field for several years, their long-term impact on the weed is not known. Climatic conditions are known to have significant influence
on the effectiveness of some biocontrol agents (Huffaker, 1967; Kok, 2001). Hence, an exclusion trial, initiated in 1996 (Dhileepan, 2001), was continued for four years to assess seasonal variation on Z. bicolorata and E. strenuana and on their impact on parthenium.
Materials and methods Study areas An exclusion experiment initiated in July 1996 at Mount Panorama (24°31’S, 148°34’E) in central Queensland and Plain Creek (21°49’S, 146°67’E) in north Queensland (Dhileepan, 2001) was continued until August 2000. Mount Panorama and Plain Creek are in the southern and northern regions of the core parthenium infestation in Queensland respectively and both locations have had severe parthenium infestations since the mid-1970s. Mount Panorama represents an area with regular rainfall pattern where all seven insect species and winter rust are present. Plain Creek represents an area with variable rainfall pattern where only three of the insect species and the newly-introduced summer rust are known to occur. Parthenium germinates in response to rain, usually in spring (September–November) at Mount Panorama and in summer (December–January) at Plain Creek. Flowering begins 6–8 weeks after germination and continues until the plant is killed by frost (March–April) at Mount Panorama or by drought (April–May) at Plain Creek. The Mount Panorama trial site received 642, 718, 981 and 554 mm rainfall per annum (July–June) in 1996–97, 1997–98, 1998–99 and 1999–00 respectively, with 30–66% of the rainfall received in summer (fig. 1). The Plain Creek trial site received 459, 684, 665 and 843 mm rainfall per annum (July–June) in 1996–97, 1997–98, 1998–99 and 1999–00 respectively, with 30–52% of the rainfall received in summer (fig. 1).
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Fig. 1. Monthly rainfall at Mount Panorama () and Plain Creek (▫) over four years (1996–2000).
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At both sites, eight plots, each of 2.25 were maintained free of biocontrol agents using pesticides, and eight plots, each of 2.25 m2, were left exposed to biocontrol agents (Dhileepan, 2001). Both sites were located on beef cattle properties and the cattle were destined for the export market. Therefore the pesticide treatment plots were fenced to prevent cattle grazing to avoid any potential meat pesticide residue problems. Two 40-m2 areas, selected on either side of the biocontrol insect excluded area were also fenced to prevent grazing. Within each 40-m2 area, four 2.25 m2 plots were selected and left exposed to biocontrol insects. To mimic the impact of grazing on grass competition, all plots were mown at the beginning of spring (September–October) before the germination of parthenium, and at the end of autumn (April–May) when all parthenium had died. Sampling at the beginning of the trial revealed no significant differences in the soil seed bank and the number of seedlings emerged, between all plots within each site (t test, P > 0.05). To maintain the plots free of biocontrol agents, monocrotophos (Azodrin®, 400 g l–1 EC), a systemic organophosphate insecticide as a foliar spray (600 g a.i. ha–1) and carbofuran (Furadan®, 100 g kg–1), a broad-spectrum carbamate insecticide as granules to soil (3 kg a.i. ha–1), were applied at monthly intervals, except during periods of peak insect activities (January–March), when they were applied fortnightly. Neither of the insecticides had any phytotoxic effects on parthenium. Insecticide application was suspended during winter when there was no live parthenium in the study sites. All eight plots from which biocontrol agents were excluded were surrounded by a 1-m wide barrier zone sprayed with insecticides. At Mount Panorama, due to lack of both winter and summer rust activity, fungicide was not applied to exclusion plots. At Plain Creek, with the establishment of the summer rust P. melampodii in January 2000, the fungicide Mancozeb® (750 g l-1 DG) mixed with synthetic liquid latex (Bond®) to improve retention and rain-fastness, was applied (2.4 kg a.i. ha–1 in 1600 l) to exclusion plots at fortnightly intervals from February 2000. From 1997 onwards, all plots with biocontrol agents were sprayed with equal amounts of water.
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level, L. setosipennis larval damage intensity and incidence, and intensity of P. melampodii infestation were measured.
Measurement of soil seed bank A single soil sample (16 cm2 area, 2 cm depth) was collected from each of the 16 plots per site at quarterly intervals (winter, spring, summer and autumn) from July 1996 to August 2000 and the soil seed-bank determined. The soil samples were spread uniformly on the top of plastic trays (18 cm × 12 cm × 5 cm) filled with potting mix and maintained in a shade-house for three months with regular watering. The number of germinated seeds was recorded at weekly intervals.
Statistical procedures Seasonal variations in defoliation by Z. bicolorata were analysed using one-way ANOVA, followed by a Tukey test. Variations in the incidence of gall damage by E. strenuana in relation to stages of plant growth, locations and years, the impact of biocontrol on individual plant parameters, plant populations, and soil seed bank in relation to locations and years, and the impact of gall damage by E. strenuana on plant height, flower production, and plant biomass in relation to locations were analysed using General Linear Model (GLM) Repeated Measures ANOVA and the main effects compared. Regression analysis was employed to study the following interactions: prevalence of gall damage at rosette stage and the proportion of plants producing flowers; levels of defoliation and flower production and the proportion of plants producing flowers and plant biomass.
Results Variation in damage intensity of biocontrol agents At Mount Panorama, the level of defoliation by Z. bicolorata varied significantly between years (fig. 2). In 1996–97, defoliation was evident in 100% of plants resulting in 96% leaf area loss. In 1997–98 and 1998–99, defoliation was only evident in 46% and 35% of plants resulting in 15% and 27% leaf area loss respectively. In 1999–2000, feeding a 100
The densities of parthenium seedlings, rosettes, preflowering and flowering plants were recorded along with plant height and flower production, at both sites at monthly intervals. In plots exposed to biocontrol, the proportion of plants with E. strenuana gall damage, number of E. strenuana galls per plant, the proportions of plants with defoliation by Z. bicolorata and of leaf area defoliated by Z. bicolorata (0–100% using visual scores), oviposition in flowers by L. setosipennis and incidence of other biocontrol agents were recorded at monthly intervals (Dhileepan, 2001). At Plain Creek the proportion of plants, leaves and leaf area with summer rust infestation were recorded at monthly intervals from January to June 2000. Plots from which biocontrol agents were excluded were also sampled at monthly intervals to confirm the absence of biocontrol agents. At the end of each season, all parthenium plants were removed and the plant height, plant biomass, number of flowers, number of leaves, E. strenuana gall incidence, Z. bicolorata defoliation
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Fig. 2. Mean % of leaves defoliated by Zygogramma bicolorata at Mount Panorama over four years (1996–2000). Bars indicate SE of mean. One way ANOVA, F3,31 = 53.37, P < 0.001. Tukey test: means with the same letter are not significantly different (P > 0.05).
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damage was noticed in only 2.3% of the plants resulting in the loss of less than 1% leaf area. Zygogramma bicolorata was not recorded at Plain Creek. Gall damage by E. strenuana was noticed at both sites in all the four years (fig. 3). At Mount Panorama, the proportion of plants with gall damage was higher in 1996–97 than in later years. At Plain Creek, the proportion of plants with gall damage (67–92%) did not differ significantly between years. At both sites, 11–24% of plants had gall damage initiated at the rosette stage, the damage being similar from 1996 to 1999. However, in 1999–2000, 3% of plants at Mount Panorama and none at Plain Creek respectively were galled at the rosette stage. At Mount Panorama, the level of defoliation by Z. bicolorata (R2 = 0.003, P = 0.94) and galling by E. strenuana (R2 = 0.004, P = 0.89) was not dependent on the total annual rainfall. The higher levels of defoliation by Z. bicolorata and galling by E. strenuana at Mount Panorama in 1996–97 coincided with an above average summer rainfall, but in the following three years with below average summer rainfall the defoliation and gall incidence levels were lower (fig. 4). At Plain Creek there was a negative relationship between E. strenuana gall damage levels and total annual rainfall (R2 = 0.85, P = 0.08), but the relationship between E. strenuana gall damage levels and total summer rainfall was not significant (fig. 4). At both sites other biocontrol insects (L. setosipennis, S. lutulentus and B. parthenica) were recorded only occasionally and the winter rust P. a. partheniicola was not recorded. The summer rust P. melampodii became established at Plain Creek in the summer of 2000.
Variation in the effectiveness on individual plants Biocontrol had a significant negative impact on plant height and flower production, but the significance of the impact varied with the year and location (fig. 5). Biocontrol reduced plant height by 40% at Mount Panorama in 1996–97
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Fig. 4. Relationship between total summer rainfall and % leaf area defoliated by Zygogramma bicolorata at Mount Panorama ( ) and % of plants galled by Epiblema strenuana at Mount Panorama (□) and Plain Creek (●). Bars indicate SE of mean. Linear regression between total summer rainfall and % leaf area defoliated at Mount Panorama (y = 175.9 + 0.76x, R2 = 0.77, P = 0.13), and % of plants galled at Mount Panorama (y = 137.6 + 0.68x, R2 = 0.78, P = 0.12) and Plain Creek (y = 85.1 – 0.06x, R2 = 0.27, P = 0.48). and by 39% and 46% in 1996–97 and 1997–98 respectively at Plain Creek. Significant impact on flower production due to biocontrol was achieved only in 1996–97, with 82% reduction at Mount Panorama and 49% reduction at Plain Creek. No significant impacts of biocontrol on plant biomass (fig. 5) and number of branches (F1,28 = 0.61, P = 0.44) were recorded. At Plain Creek, in 1999–2000, galling and summer rust P. melampodii infection had no impact on plant height, flower production and plant biomass (fig. 5). All surviving defoliated plants produced flowers irrespective of the level of defoliation. There was no relationship between level of defoliation and the proportion of plants producing flowers (R2 = 0.003, P = 0.82). The negative impact of galling on plant height, flower production and plant biomass was more severe when galling was initiated at rosette and pre-flowering stages than after flowering (fig. 6). Galling in the rosette stage reduced the proportion of plants producing flowers at Plain Creek (fig. 7). In contrast, the impact of galling at the rosette stage at Mount Panorama (R2 = 0.04, P = 0.26), and at the preflowering stage at Plain Creek (R2 = 0.14, P = 0.08) and Mount Panorama (R2 = 0.13, P = 0.08), on the proportion of plants producing flowers was not significant.
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Fig. 3. Incidence of galling by Epiblema strenuana at rosette ( ), preflowering ( ) and flowering (□ ) stages of parthenium at Mount Panorama and Plain Creek over four years (1996–2000). Bars indicate SE of mean. GLM repeated measures ANOVA: year, F3,126 = 6.3, P = 0.001; year × plant stage, F6,126 = 9.0, P < 0.001, year × location, F3,126 = 7.2, P < 0.001, year × plant stage × location, F6,126 = 7.2, P < 0.001.
Variation in the effectiveness on weed population Biocontrol had a negative impact on seedling emergence, seedling establishment and plant density, the impact varying with year and location (fig. 8). At Mount Panorama, biocontrol reduced seedling emergence by 92% and 53% in 1997–98 and 1998–99 respectively. At Mount Panorama, in 1996–97, biocontrol reduced seedling establishment rate by 40% and plant density by 90%, but the impact in the following three years was not significant (fig. 8). At Plain Creek, there was no reduction over time in the number of
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Fig. 5. Impact of biocontrol on plant height, number of flowers per plant and biomass per plant at Mount Panorama and Plain Creek over four years (1996–2000). Solid bars () = plants without biocontrol and open bars (□) = plants with biocontrol. Bars indicate SE of mean. GLM repeated measures ANOVA: plant height, year, F3,84 = 31.9, P < 0.001; year × biocontrol, F3,84 = 7.7, P < 0.001, year × location, F3,84 = 28.9, P < 0.001, year × biocontrol × location, F3,84 = 12.1, P < 0.001; number of flowers, year, F3,84 = 22.3, P < 0.001; year × biocontrol, F3,84 = 2.1, P = 0.14, year × location, F3,84 = 12.1, P < 0.001, year × biocontrol × location, F3,84 = 0.63, P = 0.61; plant biomass, year, F3,84 = 19.2, P < 0.001; year × biocontrol, F3,84 = 1.7, P = 0.17, year × location, F3,84 = 6.7, P < 0.001, year × biocontrol × location, F3,84 = 3.6, P = 0.02. Tukey Test: for each plant parameter, means with the same letter are not significantly different (P > 0.05).
seedlings emerged in plots with biocontrol. However, the rate of increase of seedling numbers over time was significantly less in plots with biocontrol. At Plain Creek, biocontrol had no negative impact on seedling establishment rate and plant density in all four years (fig. 8). Biocontrol had a significant negative impact on the proportion of plants producing flowers (F1,28 = 24.714, P < 0.001), and the impact varied with the location (F1,28 = 47.8, P < 0.001). At Plain Creek in 1996–97 and 1997–98, the proportion of plants producing flowers in plots with biocontrol was 28% and 18% lower, respectively, than in plots without biocontrol. However, in other years, and at Mount Panorama in all four years, the impact was not significant. The impact of biocontrol on number of flowers per m2 (F1,28 = 7.9, P < 0.01) and biomass per m2 (F1,28 = 32.1, P < 0.001) was dependent on the location. At Mount Panorama biocontrol reduced the number of flowers per m2 in 1996–97 and 1997–98 by 63% and 24% respectively, and weed biomass per m2 by 76% in 1996–97. At Plain Creek, the number of flowers per m2 was reduced by 73% in 1997–98, but the impact in other years, and on weed biomass in all four years was not significant.
Variation in the effectiveness on soil seed bank At both sites, at the beginning of the trial, there was no significant difference in the soil seed bank between plots
with and without biocontrol (t test, P > 0.05). The soil seed bank was 45% higher at Mount Panorama (4167 ± 362) than at Plain Creek (2300 ± 256) (F1,112 = 63.5, P < 0.001). Soil seed bank numbers were 32–45% lower in spring, summer and winter than in autumn (F3,112 = 6.9, P < 0.001). Biocontrol reduced the soil seed bank by 70% at Mount Panorama over the 4-year period, but the reduction at Plain Creek was not significant (fig. 9).
Discussion Variation in damage intensity of biocontrol agents Biocontrol had a significant negative impact on parthenium, but the impact varied between years. Biocontrol was more effective at Mount Panorama than at Plain Creek, primarily due to defoliation by Z. bicolorata. Rainfall appears to be the major factor influencing the effectiveness of both Z. bicolorata and E. strenuana. At Mount Panorama the effect was due to total amount of summer rainfall while at Plain Creek the timing of onset of rainfall is believed to be the determinant. Rainfall pattern is a crucial element in the success of the biocontrol in St John’s wort Hypericum perforatum L. (Clusiaceae) also (Huffaker, 1967). It appears that the higher summer rainfall at Mount Panorama in 1996–97 favoured the build-up of the Z. bicolorata population, resulting in continued defoliation pressure throughout the life of the weed. In the following three years,
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Fig. 7. Impact of galling by Epiblema strenuana at rosette stage on parthenium plants attaining flowering stage in 1996–97 ( ), 1997–98 ( ), 1998–99 () and 1999–2000 (). Linear regression between gall incidence at rosette stage (x) and % of flowering plants (y) in 1996–97 (y = 92.1 – 1.2x, R2 = 0.86, P < 0.001) and 1998–99 (y = 93.7 – 0.8x, R2 = 0.99, P < 0.001). The regression was not significant in 1997–98 and 1999–2000.
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due to below-average summer rainfall only low levels of defoliation were achieved. Summer rainfall also affected the incidence of E. strenuana gall damage at Mount Panorama and, as a result, the proportion of plants with the galls was higher in 1996–97 than in the following three years. In contrast, the effectiveness of biocontrol insects on ragwort was independent of variation in environmental conditions (McEvoy et al., 1991). At Plain Creek, the level of gall damage by E. strenuana was not dependent on the amount of summer rainfall, and did not vary significantly between years. But the proportion of plants with gall damage initiated at the rosette stage was significantly greater in 1996–97 and 1998–99 than in other years. The reason for the variation in gall damage levels at the rosette stage is not known. In 1996–97, due to synchronization between onset of rainfall in spring (October 1996) resulting in parthenium germination and an increase in temperature and photoperiod resulting in the emergence of E. strenuana from diapause, 61% of plants had gall damage before they attained flowering stage. This prevented 32% of the plants from producing any flowers (Dhileepan, 2001). It is suspected that low (October 1997) or no rainfall (October 1999) in late spring (fig. 1) could have affected the level of gall incidence in rosette stage plants in 1997–98 and 1999–2000. The incidence of other biocontrol agents did not appear to have any measurable impact on the weed.
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Fig. 6. Impact of gall damage by Epiblema strenuana at rosette ( ), pre-flowering (□ ) and flowering ( ) stages of parthenium on plant height, plant biomass and flower production at Mount Panorama and Plain Creek over three years (1996–1999). Bars indicate SE of mean. Bonferroni test: at each location, means with the same letter are not significantly different (P > 0.05).
The reduction in plant height and flower production at Mount Panorama in 1996–97 was due to the combined effect of defoliation by Z. bicolorata and galling by E. strenuana. Feeding by Z. bicolorata on parthenium damaged the apical meristems and reduced the plant height (Dhileepan et al., 2000a). The reductions in plant height at Mount Panorama in 1998–99 and Plain Creek in 1996–97 and 1997–98 were due to galling by E. strenuana which, when initiated at early stages of plant growth, damages the meristems and reduces plant height (Navie et al., 1998a; Dhileepan & McFadyen, 2001). Parthenium can readily regenerate and compensate if the
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Fig. 8. Impact of biocontrol on seedling emergence, seedling establishment rate and plant density at Mount Panorama and Plain Creek over four years (1996–2000). Solid bars ( ) = plots without biocontrol and open bars (▫ ) = plots with biocontrol. Bars indicate SE of mean. GLM repeated measures ANOVA: seedling emergence, year, F3,84 = 10.2, P < 0.001; year × biocontrol, F3,84 = 17.7, P < 0.001, year × location, F3,84 = 36.6, P < 0.001, year × biocontrol × location, F3,84 = 25.1, P < 0.001; seedling establishment rate, year, F3,84 = 25.6, P < 0.001; year × biocontrol, F3,84 = 6.6, P < 0.001, year × location, F3,84 = 9.1, P < 0.001, year × biocontrol × location, F3,84 = 6.5, P = 0.001; plant density, year, F3,84 = 160.5, P < 0.001; year × biocontrol, F3,84 = 65.9, P < 0.001, year × location, F3,84 = 175.9, P < 0.001, year × biocontrol × location, F3,84 = 95.7, P < 0.001. Tukey test: for each plant parameter, means with the same letter are not significantly different (P > 0.05). defoliation is maintained for a short duration (Dhileepan et al., 2000a) and if galling is initiated after flowering (McFadyen, 1985). The absence of a reduction in plant height, flower production and plant biomass in three out of four years at Mount Panorama was due to low defoliation and galling pressure. At Plain Creek the reduction in flower production in 1996–97 was due to galling by E. strenuana initiated during the early stages of plant growth. No significant reductions in flower production in the following three years were due to low levels of gall damage during the early stages of plant growth. This appears to have been due to lack of synchrony between parthenium germination and E. strenuana emergence.
Variation in the effectiveness on weed population The impact of biocontrol on parthenium populations was dependent on rainfall. At Mount Panorama, the aboveaverage rainfall in 1996–97 resulted in higher parthenium density but also favoured Z. bicolorata and E. strenuana, resulting in a 90% reduction in weed density. This reduction was due to lower seedling establishment and higher mortality among flowering-stage plants. Zygogramma bicolorata caused 96% reduction in weed density at Bangalore in India (Jayanth & Bali, 1994; Jayanth & Visalakshy, 1996). Similar reductions have been achieved in populations of St
John‘s wort H. perforatum (Huffaker & Kennett, 1959), mission prickly pear Opuntia ficus-indica Mill (Cactaceae) (Zimmerman & Moran, 1982), tansy ragwort Senecio jacobaea L. (Asteraceae) (McEvoy et al., 1991), orange wattle Acacia saligna Wendland (Mimosaceae) (Morris, 1997), rattlebox Sesbania punicea Benth. (Fabaceae) (Hoffmann & Moran, 1998), yellow starthistle Centaurea solstitialis L. (Asteraceae) (Woods et al., 2000), nodding thistle Carduus thoermeri Weismann (Asteraceae) and plumeless thistle C. acanthoides L. (Asteraceae) (Kok, 2001) with other biocontrol agents. The reduction in parthenium biomass per m2 was due to reduction in plant density, there being no effect on individual plants. In contrast, the reduction in numbers of flowers per m2 was due to the combined reduction of plant density and numbers of flowers per plant. Below-average rainfall in three years of the 4-year study period affected both parthenium and its biocontrol agents, as evident from reduced plant density and lower biocontrol agent abundance. All established parthenium plants survived till the end of the season and produced flowers in these years with no evidence of major pressure from biocontrol agents. The reductions in plant density and flower production in 1996–97 due to biocontrol resulted in lower seedling emergence in the following two years. However, biocontrol did not have any negative impact on seedling survival and establishment in those two years due to lack of defoliation and galling pressure at Mount Panorama, and delayed
400
K. Dhileepan
Germinable seed per m2 (×1000)
15 a
Mount Panorama
12 9 b
6
bd
cd
c
3
Variation in the effectiveness on soil seed bank
b
b
c 0 96/97
Germinable seeds per m2 (×1000)
98/99
99/00
Plain Creek
5 4
97/98
a a ab
a
ab 3
ab
ab
2
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98/99
thereby reducing the flower density on an area basis. At Plain Creek, the higher plant density in 1996–97 resulted in a reduced proportion of galled plants producing flowers. The effect of intraspecific competition is known to enhance the negative effects of herbivory (McEvoy et al., 1993).
99/00
Fig. 9. Impact of biocontrol on germinable soil seed bank of parthenium at Mount Panorama and Plain Creek over four years (1996–2000). The values are the average of all four seasons within each year. Solid bars ( ) = plots without biocontrol and open bars (□) = plots with biocontrol. Vertical bars represent standard error. GLM repeated measures ANOVA, tests of between subject effects: biocontrol, F1,112 = 63.5, P < 0.001; location, F1,112 = 26.7, P < 0.001, biocontrol × location, F1,112 = 18.9, P < 0.001. Tukey test: for each location, means with the same letter are not significantly different (P > 0.05). galling pressure at Plain Creek. In 1999–2000, even though a higher seedling survival was recorded than in the previous two years, very low seedling emergence resulted in reduced plant density. Increased seedling emergence in plots excluded from biocontrol compared with plots with biocontrol, was due to a higher proportion of plants producing flowers and to a higher mean number of flowers per plant. At Plain Creek galling by E. strenuana did not reduce seedling establishment and plant density. Galling seldom kills the plant, even when initiated at early stages of plant growth. This is due to the ability of E. strenuana to avoid poor quality hosts and choose more vigorous plants (Dhileepan & McFadyen, 2001). However, galling at early stages of plant growth reduced both the proportion of plants producing flowers and the number of flowers per plant,
Biocontrol reduced the seed bank of parthenium in the soil, due to reduced plant density at Mount Panorama and to fewer flowering plants at Plain Creek. This supports the findings of Dhileepan et al. (2000b) who reported 13–94% reduction in the seed bank. Up to 70% reduction in the seed bank of the weed S. jacobaea was achieved due to biocontrol (McEvoy et al., 1991). Very large parthenium seed banks in plots excluded from biocontrol suggest that, without biocontrol, the seed banks would be much higher than the existing levels. In areas with continued outbreaks of Z. bicolorata it was expected that the existing seed bank would be reduced even further, resulting in reduced weed density in 6–7 years (Dhileepan et al., 2000b). However, with complete defoliation in only three seasons (1992–93, 1995–96 and 1996–97) in the last decade, it is unlikely that the predicted reductions in seed bank or weed density will be achieved within 6–7 years. Temporal variations in parthenium seed banks are due to timing of input via the seed rain and loss of viability over time (Navie et al., 1997). As a result, seeds accumulated during the flowering period (summer to autumn) increased the seedbank in autumn, but numbers declined subsequently in the following seasons, due to very short longevity of surface-lying seeds (Navie et al., 1998b). However, buried seed persists for a long time, with around 50% remaining viable for up to six years (Navie et al., 1998b). Higher rainfall and, consequently, more severe parthenium infestations are responsible for the larger seed bank at Mount Panorama than at Plain Creek.
Acknowledgements The author thanks Paula Ludwig, Scott Dearden, Stephen Setter, Mathew Madigan, Caroline Lowe, Clinton McPherson, Leon Hill, Tracy Splatt and Florentine Singarayar for their support in the field studies, David Green for the statistical advice, and Rachel McFadyen, Dane Panetta and Joe Scanlan for useful comments on the manuscript. Facilities provided by Haward Smith, Gail Smith (Mount Panorama), Reid Russell and Robyn Russell (Plain Creek) to conduct the trial on their properties are gratefully acknowledged. The Queensland Government under the Strategic Weed Eradication and Education Program funded this study.
References Blossey, B. & Skinner, L. (2000) Design and importance of postrelease monitoring. pp. 693–706 in Spencer, N.R. (Ed.) Proceedings of the Tenth International Symposium on Biological Control of Weeds, Montana State University, Bozeman, USA. Chippendale, J.F. & Panetta, F.D. (1994) The cost of parthenium weed to the Queensland cattle industry. Plant Protection Quarterly 9, 73–76. Crawley, M.J. (1989) The success and failures of weed biocontrol using insects. Biocontrol News and Information 10, 213–223.
Variation in the effectiveness of biocontrol in parthenium weed Dhileepan, K. (2001) Effectiveness of introduced biocontrol insects on the weed Parthenium hysterophorus (Asteraceae) in Australia. Bulletin of Entomological Research 91, 167–176. Dhileepan, K. (2003) Current status of the stem-boring weevil Listronotus setosipennis (Coleoptera: Curculionidae) introduced against the weed Parthenium hysterophorus (Asteraceae) in Australia. Biocontrol Science and Technology 13, 3–12. Dhileepan, K. & McFadyen, R.E. (1997) Biological control of parthenium in Australia – progress and prospects. pp. 40–44 in Mahadeveppa, M. & Patil V.C. (Eds) Proceedings of the First International Conference on Parthenium Management, University of Agricultural Sciences, Dharwad, India. Dhileepan, K. & McFadyen R.E. (2001) Effects of gall damage by the introduced biocontrol agent Epiblema strenuana (Lepidoptera: Tortricidae) on the weed Parthenium hysterophorus (Asteraceae). Journal of Applied Entomology 125, 1–8. Dhileepan, K., Setter, S. & McFadyen, R.E. (2000a) Response of the weed Parthenium hysterophorus (Asteraceae) to defoliation by the introduced biocontrol agent Zygogramma bicolorata (Coleoptera: Chrysomelidae). Biological Control 19, 9–16. Dhileepan, K., Setter, S. & McFadyen, R.E. (2000b) Impact of defoliation by the introduced biocontrol agent Zygogramma bicolorata (Coleoptera: Chrysomelidae) on parthenium weed in Australia. BioControl 45, 501–518. Hoffmann, J.H. & Moran, V.C. (1998) The population dynamics of an introduced tree, Sesbania puniceae, in South Africa, in response to long-term damage caused by different combinations of three species of biological control agents. Oecologia 114, 343–348. Huffaker, C.B. (1967) A comparison of the status of biological control of St John‘s wort in California and Australia. Mushi 39, 51–73. Huffaker, C.B. & Kennett, C.E. (1959) A ten-year study of vegetational changes associated with biological control of Klamath weed. Journal of Rangeland Management 12, 69–82. Jayanth, K.P. & Bali, G. (1994) Biological control of parthenium by the beetle Zygogramma bicolorata in India. FAO Plant Protection Bulletin 42, 207–213. Jayanth, K.P. & Visalakshy, P.N.G. (1996) Succession of vegetation after suppression of parthenium weed by Zygogramma bicolorata in Bangalore, India. Biological Agriculture and Horticulture 12, 303–309. Julien, M.H. & Griffiths, M.W. (1998) Biological control of weeds: a world catalogue of agents and their target weeds. 4th edn. 223 pp. Wallingford, Oxon, CAB International. Kok, L.T. (2001) Classical biological control of nodding and plumeless thistles. Biological Control 21, 206–213. McClay, A.S. (1995) Beyond ‘before-and-after’ experimental design and evaluation in classical weed biocontrol. pp. 213–219 in Delfosse, E.S. & Scott, R.R (Eds) Proceedings of the Eighth International Symposium on Biological Control of Weeds, Lincoln University, Canterbury, New Zealand. McEvoy, P.B., Cox, C. & Coombs, E. (1991) Successful biological control of ragwort Senecio jacobaea, by the introduced insects in Oregon. Ecological Applications 1, 430–442. McEvoy, P.B., Rudd, N.T., Cox, C.S. & Huso, M. (1993) Disturbance, competition, and herbivory effects on ragwort
401
Senecio jacobaea populations. Ecological Monographs 63, 55–75. McFadyen, R.E. (1985) The biological control programme against Parthenium hysterophorus in Queensland. pp. 789–796 in Delfosse, E.S (Ed.) Proceedings of the Sixth International symposium on the Biological Control of Weeds, Agriculture Canada, Ottawa, Canada. McFadyen, R.E. (1995) Parthenium weed and human health in Queensland. Australian Family Physician 24, 1455–1459. McFadyen, R.E. (2000) Biology and host specificity of the stem galling weevil Conotrachelus albocinereus Fielder (Col: Curculionidae), a potential biocontrol agent for parthenium weed Parthenium hysterophorus L. (Asteraceae) in Queensland, Australia. Biocontrol Science and Technology 10, 195–200. Moran, V.C. & Hoffmann, J.H. (1989) The effects of herbivory by a weevil species, acting alone and unrestrained by natural enemies, on growth and phenology of the weed Sesbania punicea. Journal of Applied Ecology 26, 967–977. Morris, M.J. (1997) Impact of the gall-forming fungus Uromycladium tepperianum on the invasive tree Acacia saligna in South Africa. Biological Control 10, 75–82. Navie, S.C., McFadyen, R.E., Panetta, F.D. & Adkins, S.W . (1996) The biology of Australian weeds 27. Parthenium hysterophorus L. Plant Protection Quarterly 11, 76–88. Navie, S.C., McFadyen, R.E., Panetta, F.D. & Adkins, S.W . (1997) A study of the soil seed bank of parthenium weed in central Queensland. pp. 74–78 in Rajan, A. (Ed.) Proceedings of the Sixteenth Asia-Pacific Weed Science Society Conference, Malaysian Plant Protection Society, Kuala Lumpur, Malaysia. Navie, S.C., Priest, T.E., McFadyen, R.E. & Adkins, S.W . (1998a) Efficacy of the stem-galling moth Epiblema strenuana Walk. (Lepidoptera: Tortricidae) as a biological control agent for the ragweed parthenium (Parthenium hysterophorus L.). Biological Control 13, 1–8. Navie, S.C., Priest, T.E., McFadyen, R.E. & Adkins, S.W . (1998b) Behaviour of buried and surface-lying seeds of parthenium weed (Parthenium hysterophorus L.). Weed Research 38, 338–341. Straw, N.A. & Sheppard, A.W . (1995) The role of plant dispersion pattern in the success and failure of biological control. pp. 161–168 in Delfosse, E.S. and Scott, R.R. (Eds) Proceedings of the Eighth International Symposium of Biological Control of Weeds, Lincoln University, Canterbury, New Zealand. Woods, D.M., Pitcairn, M.J. & Joley, D.B. (2000) Sequential impact of endemic pathogens, exotic molluscs and insects on Yellow Starthistle (Centaurea solstitialis L.) in California. pp. 17–23 in Spencer, N.R. (Ed.) Proceedings of the Tenth International Symposium on Biological Control of Weeds, Montana State University, Bozeman, USA. Zimmerman, H.G. & Moran, V.C. (1982) Ecology and management of cactus weeds in South Africa. South African Journal of Science 78, 314–320.
(Accepted 2 June 2003) © CAB International, 2003
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