The effect of water pollution on biological control of water hyacinth

South Africa has one of the world’s biggest gold mining regions with an associated problem of acid mine drainage (AMD), which increases the bioavailability of heavy metal contaminants in water. The prevalence of water hyacinth (Eichhornia crassipes) in South African water systems, despite the release of seven biocontrol agents since 1974, is often attributed to high levels of eutrophication. Metal concentration in plant shoots is known to affect insect herbivory. Nevertheless, little is known about the effect of heavy metals or AMD on Neochetina eichhorniae and Neochetina bruchi, which are the most widely established biocontrol agents on E. crassipes in South Africa. Herein, the effect of eight different heavy metals common in AMD (arsenic (As), gold (Au), copper (Cu), iron (Fe), mercury (Hg), manganese (Mn), uranium (U) and zinc (Zn)), as well as three different simulated AMD concentration treatments (low, medium and high), on the performance of Neochetina weevils were investigated by releasing adults on plants growing in tubs and pools, three weeks after the addition of individual metal or AMD treatments. After six weeks, the number of weevil larvae per plant, the number of adult survivors per plant, the number of adult feeding scars on leaves, and the number of larval mines per plant were recorded. Two females of N. eichhorniae and N. bruchi from each tub were dissected and the number of ovariole follicles was counted. Adult feeding in Neochetina was significantly reduced on plants exposed to both Cu and As while larval feeding was significantly reduced on plants exposed to Hg, Zn, As and Cu, with Cu causing the greatest effect. Similarly, weevil feeding and reproduction were reduced in the medium and high concentration AMD treatments. Larval development was significantly impaired by both metal and AMD treatments. These negative effects disagree with published data which showed no effect of metals on Neochetina weevils. The disparity is explained by long exposure of the weevils on whole plants, rather than short exposure to excised leaves, as recorded in the literature. Finally these findings provide evidence that some heavy metals and AMD might be constraining biocontrol agents of water hyacinth in South Africa.     

Weevil borne microbes contribute as much to the reduction of photosynthesis in water hyacinth as does herbivory

Arthropods released for weed biocontrol can have effects other than simply removing biomass and frequently decrease photosynthetic rate more than can be attributed to the mere loss of photosynthetic surface area. Some of this effect may result because biological control agents facilitate the transfer and ingress of deleterious microbes into plant tissues on which they feed. We evaluated this facilitation effect using water hyacinth (Eichhornia crassipes) and a weevil (Neochetina eichhorniae) and compared the reductions in photosynthetic rates between leaves subject to herbivory by adult weevils sterilized with 3.5% chlorine bleach, to those that were unsterilized. The results showed that weevils carried both fungi and bacteria, transferred these to leaves on which they fed, and that microbes and biomass removal contributed almost equally to the 37% decrease in photosynthetic productivity. Hence, maximising the effectiveness of using arthropods that damage leaf surfaces for biocontrol requires the presence of microorganisms that are deleterious to plants.     

Effect on waterhyacinth ofNeochetina eichhorniae [Col.: Curculionidae] combined withOrthogalumna terebrantis [Acari: Galumnidae]

Seven hundred mottled waterhyacinth weevils,Neochetina eichhorniae Warner, were released in a Fort Lauderdale, Florida, canal on a mat of waterhyacinth,Eichhornia crassipes (Mart.) Solms-Laubach. At the time of weevil release, the mat contained ca. 100 adult waterhyacinth mites,Orthogalumna terebrantis Wall-work/plant, and ca. 15 immature waterhyacinth mites/cm². Waterhyacinth weevil populations increased to ca. 4 adults and 5 larvae/plant after 50 weeks, and were unaffected by weather. Waterhyacinth mite populations reached a peak of ca. 840/plant after 16 weeks, at which time they were reduced in number by low temperatures. Decrease in size and density of waterhyacinth closely followed buildup of weevil populations, with petiole length decreasing by 35% and plant density reduced by 45% over a 50 week period. The phytopathogenic fungusAcremonium zonatum (Saw.) Gams., which causes zonate leaf spot disease of waterhyacinth, developed in waterhyacinth mite tunnels after the adult mite created an emergence hole, but was not observed in weevil feeding spots.     

Biological control of water hyacinth in California’s Sacramento–San Joaquin River Delta: observations on establishment and spread

Water hyacinth (Eichhornia crassipes (Martius) Solms-Laubach) is a serious invasive weed in the Sacramento–San Joaquin River Delta of California. Three insects: Neochetina eichhorniae Warner and Neochetina bruchi Hustache (Coleoptera: Curculionidae) and Niphograpta (=Sameodes) albiguttalis (Warren) (Lepidoptera: Crambidae) were released during 1982–1987 at four locations for the biological control of water hyacinth. Observations in 1985 suggested that all three species had established. By 2002, water hyacinth populations in the Delta still required an aggressive chemical control campaign and the status of the biological control agents was in question. In late 2002, a field survey to determine the distribution and abundance of the released insects was performed. Water hyacinth plants were collected by boat in the main water channels and from land at smaller sloughs and examined for insects. In total, 27 sites with water hyacinth distributed across the Delta were examined of which 21 had weevils. Weevil abundance ranged from 0 to 10.9 weevils per plant, with an average of 0.93 (±0.47 SEM) adult weevils per plant. All weevils (n?=?518) were identified as N. bruchi. No N. eichhorniae were recovered and no larvae or evidence of larval feeding by N. albiguttalis were observed. A total of 322 weevils were examined for microsporidia and none was found infected, indicating an infection rate of less than 1%. These results suggest that N. bruchi may be the only established biological control agent of water hyacinth in the Delta and that infection by microsporidia does not appear to be limiting its population abundance.     

The effect of two biological control agents, the weevil Neochetina eichhorniae and the mirid Eccritotarsus catarinensis on water hyacinth, Eichhornia crassipes , grown in culture with water lettuce, Pistia stratiotes

We assessed the effect of two biological control agents, the mirid Eccritotarsus catarinensis (Carvalho) and the weevil Neochetina eichhorniae (Warner), singly or in combination, on the competitive ability of their host plant, water hyacinth, Eichhornia crassipes (Mart.) Solms-Laub., grown in a screen house, in competition with another aquatic plant (Pistia stratiotes L.). Water hyacinth plant growth characteristics measured included fresh weight, leaf and petiole lengths, number of inflorescences produced, and new shoots. Without herbivory, water hyacinth was 18 times more competitive than water lettuce (across all experimental combinations of initial plant densities), as estimated from fresh weights. Both insect species, singly or in combination, reduced water hyacinth plant growth characteristics. E. catarinensis alone was less damaging than the weevil and under normal conditions, i.e., floating water hyacinth, is not expected to increase control of water hyacinth beyond that of the weevil. When combined with the weevil, half the inoculum of weevils and half the inoculum of mirids produced the same growth reduction as the full inoculum of the weevil. Under conditions where the weevils are not effective because water hyacinths are seasonally rooted in mud, the mirid, which lives entirely on leaves, should become a useful additional biological control agent. Handling Editor: John Scott.     

Effect oforthogalumna terebrantis [Acari: Galumnidae] on neochetina eichhorniae [col. curculionidae] eggs and oviposition

Adult waterhyacinth mites,Orthogalumna terebrantis Wallwork, did not consume eggs of the mottled waterhyacinth weevil,Neochetina eichhorniae Warner, under 4 temperature regimes (viz. 5°–25°, 10°–30°, 15°–35° and 20°–40° C). Microscopic examination showed that mites did not feed or attempt to feed on weevil eggs and they starved when weevil eggs were the only source of food. At the same temperature regimes, 0, 50, 100, 150 and 200 mites were added to aluminium pans containing 3 pairs of adult weevils and a fresh waterhyacinth pseudolamina. Weevils laid more eggs/female (P≤0.05) in the presence of mites.     

Leaf scarring by the weevils Neochetina eichhorniae and N. bruchi enhances infection by the fungus Cercospora piaropi on waterhyacinth, Eichhornia crassipes

Additive or synergistic effects among introduced and native insect and plant pathogen agents are necessary to achieve biological control of waterhyacinth (Eichhornia crassipes), a globally damaging aquatic weed. In field plots, plants were infested with waterhyacinth weevils (Neoechetina bruchi and N. eichhorniae) and leaves were scarred by weevil feeding. Subsequent infection by the fungal pathogen Cercospora piaropi caused necrotic lesions to form on leaves. Necrosis development was 7.5- and 10.5-fold greater in plots augmented with both weevils and C. piaropi and weevils alone, respectively, than in plots receiving only C. piaropi. Twenty-four days after weevil infestation, the percentage of laminar area covered by lesions on third-youngest and oldest live leaves was elevated 2.3–2.5-fold in plots augmented with weevils. Scar density and necrosis coverage on young leaf laminae were positively correlated, even though antipathogenic soluble peroxidases were elevated 3-fold in plots augmented with weevils alone or weevils and C. piaropi. Combined weevil and fungal augmentation decreased shoot densities and leaves per plant. In a no-choice bioassay, weevil feeding on oldest but not young leaves was reduced 44 two weeks after C. piaropi inoculation. Protein content and peroxidase activities were elevated 2–6-fold in oldest leaves three weeks after inoculation. Augmentation with both waterhyacinth weevils and C. piaropi led to the development of an additive biological control impact, mediated by one or more direct interactions between these agents, and not plant quality effects.     

Assessing the true status of the fish species Labeo cylindricus (Peters 1868) (Teleostei: Cyprinidae) in Lake Baringo,Kenya

Eutrophication contributes to the proliferation of alien invasive weed species such as water hyacinth Eichhornia crassipes. Although the South American moth Niphograpta albiguttalis was released in South Africa in 1990 as a biological control agent against water hyacinth, no post-release evaluations have yet been conducted here. The impact of N. albiguttalis on water hyacinth growth was quantified under low-, medium- and high-nutrient concentrations in a greenhouse experiment. Niphograpta albiguttalis was damaging to water hyacinth in all three nutrient treatments, but significant damage in most plant parameters was found only under high-nutrient treatments. However, E. crassipes plants grown in high-nutrient water were healthier, and presumably had higher fitness, than plants not exposed to herbivory at lower-nutrient levels. Niphograpta albiguttalis is likely to be most damaging to water hyacinth in eutrophic water systems, but the damage will not result in acceptable levels of control because of the plant's high productivity under these conditions. Niphograpta albiguttalis is a suitable agent for controlling water hyacinth infestations in eutrophic water systems, but should be used in combination with other biological control agents and included in an integrated management plan also involving herbicidal control and water quality management.     

Observations on the effect of the weevils Neochetina eichhorniae Warner and Neochetina bruchi Hustache on the growth of water hyacinth

Water hyacinth Eichhornia crassipes (Mart.) Solms. is an aquatic weed that infests most of the White Nile system in the Sudan. Serious economical and ecological problems are caused by this weed. The two weevils Neochetina eichhorniae and Neochetina bruchi were imported and released in an attempted biological control against the weed. The adults of these weevils attack the plant and feed by removing tissues from the leaf pseudolamina and petioles. The larvae tunnel inside the petioles and the crown. The optimum temperature for feeding and development of both species is 25° C. Results obtained from stocking hyacinth plants with adults and larvae of both species separately revealed that N. bruchi is more efficient in checking the growth of the plant. The progeny of a pair of N. bruchi and N. eichhorniae reared separately on 41 hyacinth plants for a period of 61 days (one generation period) reduced their population growth by 25.4% and 12.7% respectively. The progeny of both species in a mixed culture reduced the growth of the plants by 22.5% in the same period, while in the control the population of the plants increased 136.6%.     

The effects of insect–insect interactions on the performance of three biological control agents released against water hyacinth

Insect–insect interactions can have implications for biological control programmes when multiple agent species are released. In many cases there is an increase in the efficacy when more than one species is used; however, there is a possibility that releasing an additional species into a programme could have a negative effect. The interactions between three arthropod agents of water hyacinth Eichhornia crassipes (Martius) Solms-Laubach, Eccritotarsus catarinensis (Carvalho), Neochetina bruchi Hustache and Neochetina eichhorniae Warner were investigated in an experiment to measure the impact that pairwise combinations of the insects may have on their performance. There was a significant interaction between the mirid E. catarinensis and the weevil N. eichhorniae, with significantly fewer weevil feeding scars when in combination with the mirid (approximately 0.2 scars per cm²) than when alone (approximately 0.4 scars per cm²). There were also slightly fewer petioles mined by N. eichhorniae when in combination with the mirid. Interestingly there was a negative interaction between the two weevil species when in combination, with the number of feeding scars being significantly lower per individual when the two species were in combination. None of the insects performed significantly better when in combination with another insect, however, the mirid was never negatively affected by the presence of either weevil species. The interactions observed between the insects tested were identifiable but subtle and are unlikely to have implications on establishment or performance of the insects in the introduced range, South Africa.     

Pre-release evaluation of the efficacy of the leaf-sucking bug Carvalhotingis visenda (Heteroptera: Tingidae) as a biological control agent for cat's claw creeper Macfadyena unguis-cati (Bignoniaceae)

In classical weed biological control, assessing weed response to simulated herbivory is one option to assist in the prioritization of available agents and prediction of their potential efficacy. Previously reported simulated herbivory studies suggested that a specialist herbivore in the leaf-feeding guild is desirable as an effective biological control agent for cat's claw creeper Macfadyena unguis-cati (Bignoniaceae), an environmental weed that is currently a target for biological control. In this study, we tested (i) whether the results from glasshouse-based simulated herbivory can be used to prioritise potential biological control agents by evaluating the impact of a leaf-sucking tingid bug Carvalhotingis visenda (Drake & Hambleton) (Hemiptera: Tingidae) in quarantine; and (ii) the likely effectiveness of low- and high-densities of the leaf-sucking tingid after its release in the field. The results suggest that a single generation of C. visenda has the potential to reduce leaf chlorophyll content significantly, resulting in reduced plant height and leaf biomass. However, the impact of one generation of tingid herbivory on below-ground plant components, including the roots and tuber size and biomass, were not significant. These findings are consistent with results obtained from a simulated herbivory trial, highlighting the potential role of simulated herbivory studies in agent prioritisation.     

Effect of simulated herbivory on growth of the invasive weed Hygrophila polysperma: Experimental and predictive approaches

Herbivory simulation studies, through mechanical removal of leaf tissue, provide valuable insight about plant compensation and tolerance to defoliation. A mesocosm experiment was conducted to examine the effects of defoliation on growth and biomass accumulation of Hygrophila polysperma and thereby determine the critical level of herbivory necessary to achieve significant reduction in growth of this invasive plant. The data collected during the experiment were used to develop an empirical plant growth model to examine the usefulness of a model-based approach for a priori understanding of plant response to defoliation. The results of the mesocosm experiment showed that defoliation significantly influenced growth and biomass accumulation of hygrophila. The empirical plant growth model accurately simulated plant growth response to herbivory across treatments. Based on the results of the mesocosm experiment, an insect defoliator that causes complete defoliation of hygrophila at least at monthly intervals may be able to reduce biomass and growth of hygrophila. The ability of the mathematical model to predict the effects of defoliation on hygrophila suggest that it could be a useful tool for the selection of effective biological control agents.     

Effect of herbivory on growth and biomass allocation of Brazilian peppertree (Sapindales: Anacardiaceae) seedlings in the laboratory

Brazilian peppertree (Schinus terebinthifolius Raddi), native to South America, is invading many ecosystems in south and central Florida. The defoliating tortricid moth Episimus unguiculus Clarke was selected as a potential biocontrol agent of Brazilian peppertree in Florida. The objective of this study was to examine the effect of different levels of herbivore damage on growth and biomass allocation of Brazilian peppertree seedlings in the laboratory. Three treatments were established: (1) no herbivory (control), (2) low herbivory (~4 larvae/plant), and (3) high herbivory (~12 larvae/plant). High levels of herbivory significantly reduced the number of leaflets, plant height, foliar biomass, foliar relative growth rate (RGR) and shoot: root ratio of Brazilian peppertree seedlings. Moreover, plants were not able to recover from herbivory after 2 months. The performance of Brazilian peppertree subjected to low herbivory levels did not differ from the control plants (no herbivory). The potential effectiveness of the biocontrol agent E. unguiculus to suppress this noxious weed is examined.     

Toxic effect of herbicides used for water hyacinth control on two insects released for its biological control in South Africa

The integrated control of water hyacinth, Eichhornia crassipes (Martius) Solms-Laubach (Pontederiaceae) has become necessary in South Africa, as biological control alone is perceived to be too slow in controlling the weed. In total, seven insect biological control agents have been released on water hyacinth in South Africa. At the same time, herbicides are applied by the water authorities in areas where the weed continues to be troublesome. This study investigated the assumption that the two control methods are compatible by testing the direct toxicity of a range of herbicide formulations and surfactants on two of the biological control agents released against water hyacinth, the weevil, Neochetina eichhorniae Warner (Coleoptera: Curculionidae) and the water hyacinth mirid, Eccritotarsus catarinensis (Carvalho) (Hemiptera: Miridae). A number of the formulations used resulted in significant mortality of the mirid and the weevil. Products containing 2,4-D amine and diquat as active ingredients caused higher mortality of both agents (up to 80% for the mirid) than formulations containing glyphosate. Furthermore, when surfactants were added to enhance herbicide efficiency, it resulted in increased toxicity to the insects. We recommend that glyphosate formulations should be used in integrated control programmes, and that surfactants be avoided in order to reduce the toxic nature of spray formulations to the insect biological control agents released against water hyacinth.     

Importation,releases, and establishment ofNeochetina spp. (Col.: Curculionidae) for the biological control of water hyacinth,Ecchhornia crassipes (Lil.: Pontederiaceae), in Benin,West Africa

Water hyacinth,Eichhornia crassipes (Martius) Solms-Laubach (Pontederiaceae) was first reported in Bénin in 1977 and about 10 years later became the major floating water weed in the south east, obstructing boat traffic and fisheries. Water hyacinth multiplies in permanently fresh water in the swampy upper reaches of the Sô River and in tributaries of the Ouémé River. From there it is moved by wind and water flow to the coastal lagoons. The coastal lagoons are brackish during the dry season and water hyacinth eventually dies. In 1991,Neochetina eichhorniae (Warner) (Col.: Curculionidae) of South American origin was imported from Australia via quarantine in Britain to Bénin. A small infestation of the fungusBeauveria bassiana (Bals.) Vuill. (Hyphomycetes) was eliminated from the colony before release by sterilizing eggs and rearing a fungus-free generation. Between late 1991 and mid 1993, about 23,900N. eichhorniae were released at 11 localities along the Ouémé River and in the head waters of the Sô River. Regular monitoring revealed feeding scars by adults on leaves and tunnelling by larvae in petioles at all release sites. By October 1993,N. eichhorniae had spread up to 20 km from some release sites.Neochetina bruchi Hustache was imported in 1992. A total of about 5,700 weevils has been released in six localities since mid 1992. Recoveries of offspring were made in all but one locality. Despite the negative impact of water flow, wind, penetration of salt water, and removal of infested water hyacinth by fishermen,N. eichhorniae andN. bruchi are established in Bénin in a situation typical for coastal West Africa.     

Effects of leaf and root herbivory by potential insect biological control agents on the performance of invasive Vincetoxicum spp.

The European leaf-feeding moth Abrostola asclepiadis and root-feeding beetle Eumolpus asclepiadeus are promising biological control agents for two European swallow-worts (Vincetoxicum rossicum and Vincetoxicum nigrum) in North America, however, their impact on plant performance is uncertain. Densities of each herbivore were manipulated in a common garden to determine whether leaf and root herbivory affect the performance of these plants. During the second year of the experiment, V. rossicum and V. nigrum unexpectedly became infected with the fungal pathogens Ascochyta sp. and Cercospora sp. (Ascomycota), respectively. Although pathogen infection mainly reduced shoot height and delayed reproduction, herbivore effects on plant growth were still evident. Leaf herbivory by A. asclepiadis had no effect on plant growth 1 year after defoliation. Root herbivory by E. asclepiadeus reduced shoot height and plant biomass and decreased the ability of plants to compensate for pathogen attack. Pathogen infection prevented detection of herbivore effect on reproduction. Due to its substantial impact on plant biomass, E. asclepiadeus should be further evaluated as a biological control agent against Vincetoxicum spp. populations invading open habitats in North America. Further research is needed to evaluate the impact of A. asclepiadis in combination with E. asclepiadeus and plant competition under high and low light conditions.     

No evidence for evolutionarily decreased tolerance and increased fitness in invasive Chromolaena odorata: implications for invasiveness and biological control

Tolerance, the degree to which plant fitness is affected by herbivory, is associated with invasiveness and biological control of introduced plant species. It is important to know the evolutionary changes in tolerance of invasive species after introduction in order to understand the mechanisms of biological invasions and assess the feasibility of biological control. While many studies have explored the evolutionary changes in resistance of invasive species, little has been done to address tolerance. We hypothesized that compared with plants from native populations, plants from invasive populations may increase growth and decrease tolerance to herbivory in response to enemy release in introduced ranges. To test this hypothesis, we compared the differences in growth and tolerance to simulated herbivory between plants from invasive and native populations of Chromolaena odorata, a noxious invader of the tropics and subtropics, at two nutrient levels. Surprisingly, flower number, total biomass (except at high nutrient), and relative increase in height were not significantly different between ranges. Also, plants from invasive populations did not decrease tolerance to herbivory at both nutrient levels. The invader from both ranges compensated fully in reproduction after 50?% of total leaf area had been damaged, and achieved substantial regrowth after complete shoot damage. This strong tolerance to damage was associated with increased resource allocation to reproductive structures and with mobilization of storage reserves in roots. The innately strong tolerance may facilitate invasion success of C. odorata and decrease the efficacy of leaf-feeding biocontrol agents. Our study highlights the need for further research on biogeographical differences in tolerance and their role in the invasiveness of exotic plants and biological control.     

Con‐specific neighbours may enhance compensation capacity in an invasive plant

Facilitation, both by inter‐ and intra‐specific neighbours, is known to be an important process in structuring plant communities. However, only a small number of experiments have been reported on facilitation in plant invasions, especially between invasive con‐specific individuals. Here, we focus on how con‐specific neighbours of the invasive alien plant alligator weed affect the tolerance of alligator weed to herbivory by the introduced biological control agent, Agasicles hygrophila. We conducted greenhouse and garden experiments in which invasive plant density and herbivory intensity (artificial clipping and real herbivory) were manipulated. In the greenhouse experiment, artificial clipping significantly reduced plant biomass when plants were grown individually, but when con‐specific neighbours were present in the same pot, biomass was not significantly different from control plants. Similarly, when compared to control plants, plants that were subjected to herbivory by A. hygrophila produced more biomass when grown with two con‐specific neighbours than when grown alone. Real herbivory also resulted in an increased number of vegetative buds, and again when two con‐specific neighbours were present this effect was increased (a 55.3% increase in buds when there was no neighbour, but a 111.6% increase in buds when two con‐specific neighbours were present). In the garden experiment, in which plants were grown at high density (6 plants per pot), alligator weed fully recovered from defoliation caused by insects at levels from 20–30% to 100%. Our results indicate that the con‐specific association may increase the compensatory ability to cope with intense damage in this invasive plant.     

Biological control of waterhyacinth in Sinaloa Mexico with the weevils Neochetina eichhorniae and N. bruchi

Water hyacinth (Eichhornia crassipes (Mart.) Solms.)creates severe problems in the irrigationdistricts of Mexico, particularly in westernSinaloa. Therefore water hyacinth weevils(Neochetina eichhorniae Warner and N. bruchi Hustache), imported from the USA in1993, were used to initiate a biologicalcontrol program. Precautionary screeningrevealed that some were infected with amicrosporidian so disease-free colonies wereproduced by eliminating infected breedinglines. To demonstrate effectiveness prior toopen field releases, weevils were firstreleased in cages at field sites. Weevilintensity increased to 6.3 weevils/plant after320 days when the plants were all dead ordying. More than 8,600 N. bruchi and14,500 N. eichhorniae were then releasedat various sites during January 1995 to August1996. Waterhyacinth coverage declined atBatamote reservoir (134 ha) from 95% to <3%by 1997; at the 12-ha Hilda reservoir from100% in May 1995 to 1% by March 1998; at the42.3-ha Arroyo Prieto reservoir from 100% to1% during the same interval; and at theMariquita reservoir (492 ha), the largestreservoir in the Humaya system, from 394 ha(80%)to 98.4 ha (20%).