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Home , Eichhornia crassipes, Neochetina eichhorniae

Hydrobiologia (2018) 807:377–388 https://doi.org/10.1007/s10750-017-3413-y

PRIMARY RESEARCH PAPER

The contributions of biological control to reduced size and of water hyacinth populations

Roy W. Jones . Jaclyn M. Hill . Julie A. Coetzee . Martin P. Hill

Received: 15 June 2017 / Revised: 22 September 2017 / Accepted: 7 October 2017 / Published online: 20 October 2017 Ó Springer International Publishing AG 2017

Abstract Water hyacinth is invasive in many coun- plant cover. subject to herbivory tries, where it reduces aquatic biodiversity and limits demonstrated reductions in above and below surface water resource utilisation. Biological control of water biomass and had shorter petioles compared to - hyacinth has been successful in South , but has free plants. Dead biomass was also higher in biological suffered from a lack of empirical data to prove control treatments. Biological control strongly affects causation. Insect exclusion trials were conducted to plant size, biomass and vigour; however, further quantify the contribution of eichhorniae integrated control is required to facilitate reduction and N. bruchi to the integrated control of water in mat cover, which is the goalpost for successful hyacinth on the Nseleni River, . Insecti- control of floating aquatic plants. cide was not expected to induce phytotoxicity, but would prevent weevil damage in water hyacinth Keywords crassipes Á Weevil plants; and weevil herbivory was predicted to reduce herbivory Á Petioles Á Neochetina spp. Á Plant fitness Á plant length, and above/below surface bio- Invasion mass. Results showed that insecticide had no phyto- toxic effects and excluded for 3 weeks, providing a baseline for field applications. Biological control on the Nseleni River directly affected water Introduction hyacinth biomass and petiole length, but did not affect (Martius) Solms-Laubach (Pont- ederiaceae) (water hyacinth), is a free-floating inva- Handling editor: Andrew Dzialowski sive aquatic macrophyte of South American origin R. W. Jones Á J. M. Hill (&) Á M. P. Hill (Edwards & Musil, 1975; Barrett & Forno, 1982), that Department of Zoology and Entomology, Rhodes has been introduced to and become invasive in many University, PO Box 94, Grahamstown 6140, South Africa countries around the world, where it reduces aquatic e-mail: [email protected] biodiversity and limits water resource utilisation J. A. Coetzee (Center, 1994; Midgley et al., 2006; Villamagna & Department of Botany, Rhodes University, Murphy, 2010; Coetzee et al., 2014; Getsinger et al., PO Box 94, Grahamstown 6140, South Africa 2014). Water hyacinth’s ability to reproduce both sexually and asexually, along with its rapid reproduc- R. W. Jones Ezemvelo KZN Wildlife, PO Box 10416, Meerensee, tion rate, to the formation of dense interlocking Richards Bay 3901, South Africa mats with complex structures (Villamagna & 123 378 Hydrobiologia (2018) 807:377–388

Murphy, 2010). While it is limited to freshwaters, it by the continual cloudy weather during the El Nin˜o flourishes in systems with high nutrient loading (Heard event of 1997/1998. & Winterton, 2000; Xie et al., 2004; Villamagna & In rebuttal, Wilson et al. (2007) suggested that Murphy, 2010; Coetzee & Hill, 2012) and through while much of the evidence points to classical efficient nutrient utilisation, successfully outcompetes biological control as the major factor, the El Nin˜o native flora for space and sunlight (Cilliers, 1991). associated weather pattern of the last quarter of 1997 Globally, it is highly pervasive in the southeastern and the first half of 1998 confused the issue. Wilson USA, Southeast , Central America and central, et al. (2007) argued that the reductions in water western and southern Africa (Te´llez et al., 2008; hyacinth on were ultimately caused by Villamagna & Murphy, 2010) and although the the widespread and significant damage to plants by historical pathways of invasion are not clear, its Neochetina spp., although the increased and spread is attributed predominately to human actions wave action associated with El Nin˜o would have (Telle´z et al., 2008; Villamagna & Murphy, 2010). increased the mortality of insect-stressed plants. Although mechanical and chemical methods are Furthermore, there is mounting evidence that abiotic available for the control of water hyacinth, classical factors such as climate, extreme weather events and biological control has been applied in multiple coun- local environmental conditions play a substantial role tries around the world as a more sustainable option in the success or failure of biological control pro- (Julien & Griffiths, 1998), with varying degrees of grammes (see Cuda et al., 2008 for a comprehensive reported success (Hill & Cilliers, 1999; Jimenez et al., review). This example illustrates how the lack of 2001; Spencer & Ksander, 2004; Center & Dray, sound empirical data in the field undermines the 2010). The first record of water hyacinth in South scientific acceptance and validity of biological Africa was in 1900 (Jacot Guillarmod, 1979) and it is control. currently the most widespread invader in Quantifiable follow-up field evaluations and empir- the country (Hill & Coetzee, 2017). The control ical tests are thus imperative to improve the science programme in South Africa however, has largely supporting biological control (Cuda et al., 2008; relied on the use of biological control (Coetzee & Hill, Morin et al., 2009). By necessity, successful post- 2011). This programme, which started in the 1970s, release evaluations should have a long-term monitor- has reduced water hyacinth populations at a number of ing focus, identifying underlying causes of success or sites around the country (Coetzee & Hill, 2012). failure, which will promote the development of better Funding for post-release monitoring in biological management strategies (Cuda et al., 2008; Morin et al., control programmes has been limited, with funds 2009). Standardised procedures and objective evalu- largely restricted to screening, introduction and ations of success are needed to confirm the establish- establishment (Cuda et al., 2008; Morin et al., 2009). ment of agents and establish their effects on the target As a result, historically, weed biological control has weed and associated ecological community (Cuda suffered from a lack of empirical data to prove et al., 2008), which is particularly challenging at a causation of impact, relying on before and after landscape scale. One method of evaluating the efficacy scenarios (Ehler, 1976; Thomas & Reid, 2007; Carson of weed biological control agents is through insect et al., 2008; Cuda et al. 2008; Hajek et al., 2016). This exclusion experiments. While there has been some approach has been regularly criticised (e.g. Thomas & research carried out on insecticide exclusion trials Reid, 2007; Carson et al., 2008;Mu¨ller-Scha¨rer & (Tipping & Center, 2002; Tipping et al., 2008), this Schaffner, 2008) and most recently so in Africa has mainly been on terrestrial weeds. regarding the biological control programme on water In this study, we use the biological control hyacinth on Lake Victoria. Williams et al. (2005) programme on the Nseleni River in the KwaZulu- suggest that the Neochetina spp. weevils alone were Natal province of South Africa as a case study. Water not responsible for the rapid reduction in weed hyacinth was first recorded on the river in the early biomass on Lake Victoria, as the rapid decrease in 1970s and by 1982 there was a 16 km plug of the weed water hyacinth abundance in only 2 years was extending from the confluence of the Nseleni and extraordinarily fast. They suggested the decline was Mposa Rivers down to Lake Nsezi. Ad hoc control more likely due to decreased light availability caused efforts, which comprised aerial and boat side herbicide 123 Hydrobiologia (2018) 807:377–388 379 spraying at peak infestation levels, to manage water contributions of biological control to this management hyacinth populations, were practiced on the Nseleni plan have been hard to quantify and possibly under River between the late 1970s and 1994 (Jones, 2009) estimated. and in 1984 heavy floods alleviated the problem, as Therefore, the aim of this study was to investigate most of the water hyacinth was washed away. the following hypotheses (1) Actara SC insecticide Thereafter, little was done to the remaining island application will not have phytotoxic effects on water populations of water hyacinth, because the decreased hyacinth plants, but will be effective at preventing level of infestation was no longer considered a threat weevil damage, and (2) herbivory by Neochetina spp. (Jones, 2001). By 1995 however, the water hyacinth weevils will reduce petiole length, as well as above infestation had returned, with between 40 and 100% and below surface biomass of water hyacinth plants cover across the entire river. The response to this due to physical damage. These hypotheses were infestation in 1995 was an integrated control manage- investigated through a series of insect exclusion trials ment programme which included widespread chemi- to quantify the contribution of biological control to the cal application and biological control. Steel cables integrated control of water hyacinth on the Nseleni were erected across the river to prevent water hyacinth River system. mats being blown upstream and to accumulate mats at the cables, making chemical treatment easier and more cost effective. Finally, herbicide applications were Materials and methods followed by the release of multiple biological control agents (Table 1). By 2000, the implementation of this Site description integrated control management programme reduced water hyacinth populations to * 20% cover and was This study was conducted on the lower 16 km of the considered very successful (Jones, 2009). Recent Nseleni River, in the proximity of Lake Nsezi floods (2016–2017) have diminished water hyacinth (28°450000S; 31°5806000E), to the west of Richards infestations on the Nseleni River; however, popula- Bay on the north coast of KwaZulu-Natal, South tions have a rapid rebound rate, particularly in Africa (see Jones et al., 2013; Hill et al., 2015 for a eutrophic waters (Heard & Winterton, 2000; Xie detailed description of the Nseleni River), between et al., 2004; Villamagna & Murphy, 2010; Coetzee & November 2007 and November 2008. The sampled Hill, 2012). As such, the integrated control manage- section of the river is approximately 100 m wide and ment programme on the Nseleni River is still ongoing, 3 m deep, with muddy substrate and comprised large maintaining water hyacinth populations at a maximum stands of powder puff (Barringtonia racemosa) and fig of 10% cover throughout the system; however, the (Ficus spp.) trees along its riparian zone. The majority

Table 1 Biological control Date Agent Number released agents released by ARC- PPRI (Pretoria) on the 1985 1400 Nseleni River 1994 albiguttalis 150 Orthogalumna terebrantis 800 1996 Eccritotarsus catarinensis 550 1996 Eccritotarsus catarinensis 500 800 1996 Eccritotarsus catarinensis 10 infested plants 1997 Eccritotarsus catarinensis 300 1995 Cercospora rodmanii (piaropi) 5 9 20 l plastic bags with infested plants aIdentified on Eichhornia 2015 Megamelus scutellaris 24,000 crassipes without being aAcremonium zonatum intentionally introduced aAlternaria eichhornia (after Jones, 2009) 123 380 Hydrobiologia (2018) 807:377–388 of the aquatic vegetation includes submerged macro- weevils) and treatments 4–6 tested the residual effect phytes (Ceratophyllum demersum and Stuckenia of insecticide, in order to determine how often insec- pectinata), large copses of emergent papyrus (Cyperus ticide spraying would be required for the field papyrus) and substantial infestations of water hya- experiment (4 = insecticide ? 1 mating pair of wee- cinth. The water level of Lake Nsezi is maintained by a vils added after 1 week, 5 = insecticide ? 1 mating wall through an intra-basin transfer from the pair of weevils added after 2 weeks, 6 = insecti- Mhlathuze River. A detailed site description is cide ? 1 mating pair of weevils added after 3 weeks; provided in Jones et al. (2011) and Hill et al. (2015). Table 2). The insecticide used was 60 ml of Actara SCTM (active ingredient: thiamethoxam (neonicoti- Experimental set-up noid); a suspension concentrate systemic insecticide with stomach and contact action) combined with This study was carried out in two experiments; the first 60 ml of Nu-Film 17Ó, a non-ionic extender sticker- experiment was aimed at (1) confirming that the spreader (active ingredient: Di-1-p-Menthene) and 3 chosen insecticide excluded biological control agents, litres of water per 20 m2 water hyacinth plot (see (2) determining how long it was effective, and (3) below – field trial), applied using a fine spray nozzle in determining whether the insecticide had any phyto- calm, windless conditions and was applied once only toxic or stimulatory effects on water hyacinth plants. in each of treatments 3–5. All treatments ran for a total The second experiment was a large-scale field study of 4 weeks from the acclimation point. designed to quantify the damage by biological control agents and their impacts on water hyacinth growth. Data collection Although there are six biological control agents established on water hyacinth on the Nseleni River Measurements of the longest petiole length (cm) and (see Table 1), the weevils Neochetina eichhorniae the number of feeding scars on 2, (the second (pot and field trials) and N. bruchi (field trials only) youngest leaf on a water hyacinth plant, which is were chosen as the agents of interest because they are preferentially fed upon by adult weevils, reflecting the the most ubiquitous and damaging agents on the river most recent feeding activity; Wright & Center, 1984; (Coetzee & Hill, 2011). Center & Wright, 1991; Heard & Winterton, 2000) were recorded for each plant in each experimental Experiment 1: lab trial treatment after the 2-week acclimation at experimental

start (Ti = initial) and finish (Tf = 4 weeks later). Sixty 20 l plastic buckets were filled with water from Longest petiole length was measured in order to the Nseleni River, and 5 g of Multicote fertiliser investigate possible phytotoxic effects of insecticide (N:P:K ratio of 5:1:4) was added to each bucket along applications and the number of weevil feeding scars on with a single water hyacinth plant. Plants were leaf 2 is an indication of the efficacy of the insecticide. allowed 2 weeks for acclimation to ambient environ- These parameters are standard measurements used in mental conditions, during which plants were inspected the water hyacinth biological control programme at 19:00 and again at 21:00 every night and any throughout South Africa (see Byrne et al., 2010). biological control agents (see Table 1) were removed. In addition, weevil activity was determined by mark- Data analysis ing each feeding scar with Eco-blue, a water-soluble dye (EcoguardTM), followed by recording of leaf General linear model analyses of variance (GLM- scarring/weevil damage. After the 2-week acclimation ANOVA; ‘MASS’ package in R) were used to period, plants were divided into six experimental investigate changes in longest petiole length (GLM- treatments (each n = 10). Treatment 1 was the control ANOVA; Gaussian distribution with a log link) and (no insecticide ? no weevils); treatment 2 tested the the number of weevil scars on leaf 2 (GLM-ANOVA; effect of weevil herbivory on insecticide-free plants Gaussian distribution) with time (before and after) and (no insecticide ? 1 mating pair of weevils); treatment treatment (1–6) as categorical factors. Tukey’s pair- 3 tested the phytotoxicity of insecticide applications in wise post hoc comparisons (‘lsmeans’ in R; Lenth, the absence of weevil herbivory (insecticide ? no 2013) were then completed where appropriate. All 123 Hydrobiologia (2018) 807:377–388 381

Table 2 Breakdown of the six treatments used in the lab trial Treatment Insecticide application Weevil application

1 (control) No No 2No19 mating pair 3 Yes No 4 Yes 1 9 mating pair; 1 week after insecticide 5 Yes 1 9 mating pair; 2 weeks after insecticide 6 Yes 1 9 mating pair; 3 weeks after insecticide All treatments were left to acclimate for 2 weeks prior to experimental start. Treatments 3–6 were sprayed with insecticide immediately after the 2-week acclimation period using 60 ml of Actara SC [active ingredient: thiamethoxam (neonicotinoid)] combined with 60 ml of Nu-Film 17Ó, a non-ionic extender sticker-spreader (active ingredient: Di-1-p-Menthene) and 3 l of water analyses were completed in R version 3.3.1 (R Core Data collection Team 2016). Data were collected every 3 weeks for a total of 10 Experiment 2: field trial sampling events over a 30-week time period, with an initial collection (Ti; experimental start) occurring A total of 10 plots: each 10 9 20 m2, were demar- immediately following the 2-week acclimation period cated in the Nseleni River using 4.8 m poles sunk into and T1 occurring 3 weeks after the first insecticide the river bed spaced 6 m apart. Nylon string was tied spray application. Each sampling event occurred prior to the poles around the plot at multiple heights to to insecticide applications and data were collected ensure future containment and plots were filled with from 10 mature water hyacinth plants from each plot, water hyacinth plants from surrounding mats. These which were removed without replacement. Data were constructed water hyacinth plots were then left for collected 1–2 m from the edge of each treatment mat 2 weeks to acclimate to local environmental condi- to minimise edge effects and spray drift and included: tions. After the 2-week acclimation period, plots were % cover, longest petiole length (cm), number of divided in two treatments; insect exclusion (n = 5) weevil feeding scars on leaf 2 [which represents the and biological control (n = 5) plots, all with 100% most recent weevil feeding activity; (Wright & Center, cover, with a 2 m space between treatments. Insect 1984; Center & Wright, 1991; Heard & Winterton exclusion plots were sprayed with insecticide every 2000)] and thus provides a comparative estimation of 3 weeks (as experiment 1 indicated that the insecticide weevil herbivory, total wet biomass (kg) per m2, above excluded for up to 3 weeks after application; surface biomass (kg), below surface biomass (kg) and see results below for experiment 1). Insecticide was dead material biomass (kg). There is a strong corre- applied using a fine spray nozzle in calm, windless lation between wet and dry water hyacinth biomass conditions, using a 16 l back sprayer from a boat, (T.D. Center, unpublished data), thus, fresh weight please see experiment 1 for insecticide formulation. was measured as it was the more expedient measure. Biological control plots were not sprayed and popu- While all the measured parameters (including lations of agents were not manipulated, thus popula- % cover, petiole length, feeding scars and biomass) tion levels were representative of the ambient can be influenced by variation in hydrology and biological control populations found in the Nseleni nutrient dynamics (Hill, 2014), the physico-chemistry River, which would include some damage by the mite of the water column in all plots was similar (Jones, Orthogalumna terebrantis and the sap-sucking mirid, 2015), and allowed for valid ecological comparisons. Eccritotarsus catarinensis, but more importantly an average of two to eight adult Neochetina weevils per Data analysis plant (Roy Jones pers obs). Collected data met assumptions of normality and homogenous variances, with the exception of the

123 382 Hydrobiologia (2018) 807:377–388 number of feeding scars on leaf 2, which was 2, a significantly lower number of weevil feeding scars subsequently square root transformed. A general on leaf 2 was seen within treatments, between linear model repeated measures analysis of variance experimental start and finish. Both longest petiole was completed, with treatment (insect exclusion and length and feeding scars clearly showed that insecti- biological control) as the categorical predictor, time cide applications precluded weevil damage for up to

(Ti = initial and T10 = experimental finish at week 3 weeks after application; however, feeding scars 30) as the repeated measure and longest petiole length were a better indicator of insect exclusion than petiole and the number of feeding scars on leaf 2 as the length. dependent variables. This was followed by Tukey’s HSD post hoc tests where appropriate. The remaining Experiment 2: field trial morphological measurements taken at experimental start (total biomass, above surface biomass, below At experimental start, the length of the longest petiole surface biomass and dead biomass) were analysed first was significantly longer for plants in the insect using a general linear model one-way analysis of exclusion plots compared with those in the biological variance (GLM-ANOVA); with treatment type (insect control plots (F1,196 = 2510.88, P \ 0.001; Figs. 2A, exclusion and biological control) as the categorical D, E, 3A). At experimental finish, after 33 weeks of predictor and all biomass parameters (see above) as growth, plants in biological control plots showed small the dependent variables. This was completed to increases in petiole length (* 4.0 cm increase) rela- confirm there were no statistical differences between tive to initial lengths, while plants in insect exclusion measurements of plants in all plots prior to experi- plots showed dramatic increases in petiole length mental start. As the dataset of interest is how between experimental start and finish, gaining biological control plots compare with insect exclusion * 55.0 cm (Fig. 1C). Comparisons of longest petiole plots after experimental finish (T10 = experimental length between plants from biological control and finish at week 30), the T10 dataset was analysed using a insect exclusion plots after experimental finish also general linear model, one-way analysis of variance clearly indicate significant effects of weevil herbivory (GLM-ANOVA). Treatment type (insect exclusion (Fig. 3A). and biological control) was the categorical predictor The number of weevil feeding scars on leaf 2 also and the biomass measurements (see above) were the differed statistically between biological control and dependent variables. This was followed by Tukey’s insect exclusion plots at both experimental start and

HSD post hoc tests where appropriate. All statistics finish (F1, 196 = 158.58, P \ 0.001; Figs. 2B, C,3B). were completed in STATISTICA v13.0 (Statsoft More importantly, the number of feeding scars 1984–2015). increased dramatically in the biological control plot over the course of the experiment, while no significant increase was seen in feeding scars on plants in the Results insect exclusion plots (Fig. 3B). There were no statistical differences in any biomass Experiment 1: lab trial measurements between biological control and insect exclusion plots at experimental start (total biomass:

No statistical differences were measured in longest F1,8 = 0.72, P = 0.42, above surface biomass: petiole length among treatments over time, or within F1,8 = 0.82, P = 0.55, below surface biomass: treatments between experimental start (Ti) and finish F1,8 = 0.80, P = 0.78 and dead biomass: 2 (Tf = 4 weeks) (Fig. 1A, all P [ 0.05). The number F1,8 = 1.07, P = 0.33). However, total biomass/m of weevil feeding scars on leaf 2 had comparatively (F1,8 = 227.95, P \ 0.001), above surface biomass/ different results; there were no statistical differences per 10 plants (F1,8 = 1951.48, P \ 0.001) and below among treatments at experimental start; however, surface biomass/per 10 plants (F1,8 = 5.66, P \ 0.05) among treatments at experimental finish there was a of plants grown in insect exclusion plots were significantly higher number of weevil feeding scars on significantly higher than those from plants grown in leaf 2 in treatment 2 (no insecticide ? weevils; biological control plots after 33 weeks of growth.

Fig. 1B, P \ 0.01). With the exception of treatment Biomass of dead material/per 10 plants (F1,8 = 53.44, 123 Hydrobiologia (2018) 807:377–388 383

Fig. 1 A Phytotoxicity of insecticide applications (Actara SCTM ? Nu-Film 17Ó combination) measured as the mean length of the longest petiole (cm) of Eichhornia crassipes plants and B efficacy of insecticide applications measured as the number of weevil feeding scars on leaf 2 of Eichhornia crassipes plants in the pot trials. Lowercase letters denote homogenous groups (P \ 0.05) between treatments after experimental finish (Tf = 4 weeks) and * denotes statistical differences (P \ 0.01) between time (before and after) among treatments

P \ 0.001) was higher in biological control than Discussion insect exclusion plots (Figs. 2E, 3B, C); however, percent cover never fell below 100% at any plot, The results of the laboratory experiment showed that treatment or time throughout the entire experiment. insecticide application neither inhibited nor promoted water hyacinth growth and thus demonstrated no phytotoxicity. However, biological control agents were successfully excluded for a period of 3 weeks, which provided a baseline for foliar applications in the field.

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Fig. 2 Clear visual differences in water hyacinth plants scars, D shows a single plant from an insecticide exclusion plot between treatments. A shows the longest petiole length of with long petioles, short , no weevil damage and very little plants in insecticide exclusion (left) and biological control dead material, compared to (E) a single plant from a biological (right) plots, B shows within an insecticide exclusion control plot with short, stressed leaves and petioles and a high plot, with no weevil feeding scars and C shows leaves within a percentage of weevil feeding damage and dead material biological control plot, showing substantial weevil feeding

Biological control has been reported to be highly lack of empirical evidence linking cause and effect. In effective for controlling invasive aquatic weeds, such some cases, the success of water hyacinth control has as water hyacinth (Hill, 2003), but has suffered from a been measured by a reduction in surface area covered

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(A) (B)

(C) Total Biomass/m2 9.00 Above Surface Biomass/10 plants Below Surface Biomass/10 plants d 8.00 Biomass Dead Material/10 plants b 7.00 a 6.00 5.00 c 4.00 3.00 Biomass (kg) 2.00 f e g 1.00 h 0.00 Biological Control Insect Exclusion Treatment

Fig. 3 A The mean length of the longest petiole (cm) of * denotes statistical differences (P \ 0.01) between treatments. Eichhornia crassipes plants and B the number of weevil feeding C Mean values of biomass for E. crassipes after experimental scars on leaf 2 at experimental start (after a 2-week acclimation finish (33 weeks). Letters denote different homogenous groups period) and after experimental finish in the field trials, (P \ 0.05) for total biomass (a, b), above surface biomass (c, d), comparing biological control and insecticide exclusion treat- below surface biomass (e, f) and dead material biomass (g, ments. Lowercase letters denote homogenous groups (P \ 0.01) h) between biological control and insecticide exclusion treat- among biological control treatments; upper case letters denote ments. Error bars indicate ? 1SE homogenous groups among insecticide exclusion treatments and by the weed (Albright et al., 2004). However, cover- reductions in plant fitness which are substantial age can be considered an arbitrary metric, particularly enough to reduce percent cover. After 33 weeks of in relation to floating weeds subject to dispersion growth in the Nseleni River, plants exposed to weevil (Tipping et al., 2014). Notwithstanding this however, herbivory demonstrated substantial reductions in for water hyacinth, percent cover remains the goal of above and below surface biomass as well as a decrease the efficacy of biological control (Tipping et al., in total biomass when compared to populations in the 2014). In the current study, the application of biolog- insect exclusion treatments, with visibly smaller plants ical control had a direct influence on the biomass of in poorer condition. These results mimic those water hyacinth populations but did not alter percent reported by Tipping et al. (2014), where unconstrained cover. This is perhaps not surprising as weevils lay weevil herbivory resulted in more than a 50% eggs in leaf tissue and the larvae mine the thick leafed reduction in biomass and fewer inflorescences, but petioles and crown (Center, 1994; Center & Dray, had little effect on percent cover, even over a 1–3 year 2010), which would result in significant short-term time frame. The biomass of dead plant material was damage (reducing plant size and biomass), but may however higher in the biological control treatment, take years and/or multiple growing seasons to result in indicative of weevil activity and substantial reductions

123 386 Hydrobiologia (2018) 807:377–388 in plant health. Post-release monitoring evaluations of (2012) showed that some regularly used herbicides are the success of biological control of water hyacinth toxic to biological control agents and suggested that should therefore have both short- and long-term goals, the establishment of biological control reserves, which which focus on initial biomass reduction and reduction would remain untreated with herbicides, could allevi- of plant vigour (within 1 year), followed by longer- ate challenges associated with low insect numbers and term assessments of percent cover (1–5 years). act as a reservoir for established biological control Herbivory by biological control agents, particularly agents. A very successful integrated control pro- Neochetina weevils which mine petioles and root gramme for the Nseleni River, South Africa was stock, has been documented to induce smaller, water- developed in 2001 (Jones, 2001); using herbicides, logged plants which sit lower in the water column collection booms and biological control. Furthermore, (Wilson et al., 2007). These mats then often require it is the only site in South Africa where all released wind and/or wave action to break up and sink (Hill & agents (N. eichhorniae, N. bruchi, O. terebrantis, Olckers, 2001; Wilson et al., 2007). The biological Niphograpta albigutallis, E. catarinensis, and the control of water hyacinth in South Africa has not been pathogen, Cercospora piaropi) have established. In as successful (with a few exceptions, see Hill & 2015, the delphacid leaf hopper Megamelus scutellaris Cilliers, 1999) as it has on the large tropical lakes and was approved for release and was added to the rivers elsewhere in Africa (see Cock et al., 2000; complement of biological control agents on Nseleni Ajuonu et al., 2003; Wilson et al., 2007). This lack of River, and the next few years will decide its utility in success has been ascribed primarily to eutrophic controlling water hyacinth populations. waters (Hill & Cilliers, 1999; Hill & Olckers, 2001; As water hyacinth proliferates in highly impacted Moran, 2006; Center & Dray Jr, 2010; Coetzee & Hill, systems (Heard & Winterton, 2000; Xie et al., 2004; 2012) and a temperate climate which impacts the life Villamagna & Murphy, 2010; Coetzee & Hill, 2012), histories of the released biological control agents (Hill integrated control programmes, when completed & Cilliers, 1999; Byrne et al, 2010; May & Coetzee, appropriately, offer the best opportunity for the 2013). However, Hill & Olckers (2001) also suggested management of persistent and high-density popula- that the relatively small size of the water bodies in tions, both in South Africa and globally. However, South Africa, most of which are also impounded, has successful post-release monitoring and the evaluation reduced the natural flow regimes and/or the wind/ of success or failure of the implementation of biolog- wave action required to break up and sink large mats. ical control should be a two-step process, focussing on Thus, while the application of biological control both short (reduction in biomass and plant vigour) and clearly reduces plant size, biomass and vigour, it long (percent cover) term goals. Teasing apart the may not be a flawless standalone technique for water drivers underpinning ultimate reductions in plant hyacinth control, particularly in eutrophic systems. cover, such as climate, hydrology, wind etc. will help Rather, further intervention using integrated control to further develop management plans to effect sub- methods (mechanical control, herbicides, hydrological stantial environmental and economic change. and nutrient control along with biological control) may be ultimately required to remove mats and reduce Acknowledgements This work was funded by the percent cover (Hill & Coetzee, 2008; Jones, 2009; Department of Environmental Affairs: National Resource Management Programme, Working for Water Programme and Byrne et al., 2010). It is unlikely however, given water the South African Research Chairs Initiative of the Department hyacinth growth rates and its reproductive capacity, of Science and Technology and the National Research that manual and/or mechanical control would be Foundation of South Africa. Logistical assistance was successful in the absence of biological control. provided by Ezemvelo KwaZulu-Natal Wildlife. Funding for this work was provided by the South African Research Chairs While integrated pest management plans to combat Initiative of the Department of Science and Technology and the water hyacinth infestations have recently been receiv- National Research Foundation of South Africa. Any opinion, ing more attention (e.g. Hill & Olckers (2001); Jones, finding, conclusion or recommendation expressed in this 2001; Byrne et al., 2010) have warned against the material is that of the authors and the NRF does not accept any liability in this regard. large-scale and injudicious use of herbicide, which often disrupts the plant/insect interactions on which biological control depends. Furthermore, Hill et al. 123 Hydrobiologia (2018) 807:377–388 387

References advances in biological control of submersed aquatic weeds. Journal of Aquatic Plant Management 46: 15–32. Ajuonu, O., V. Schade, B. Veltman, K. Sedjro & P. Neuen- Edwards, D. & C. J. Musil, 1975. Eichhornia crassipes in South schwander, 2003. Impact of the weevils Neochetina eich- Africa – a general review. Journal of the Limnological horniae and N. bruchi (Coleoptera: Curculionidae) on Society of Southern Africa 1: 23–27. water hyacinth, Eichhornia crassipes () in Ehler, L. E., 1976. The relationship between theory and practice Benin, West Africa. African Entomology 1: 153–162. in biological control. Bulletin of the Entomological Society Albright, T. P., T. G. Moorhouse & T. J. McNabb, 2004. The rise of America 22: 319–321. and fall of water hyacinth in Lake Victoria and the Kagera Getsinger, K. D., E. D. Dibble, J. H. Rodgers & D. F. Spencer, River Basin, 1989–2001. Journal of Aquatic Plant Man- 2014. Benefits of Controlling Nuisance Aquatic Plants and agement 42: 72–84. Algae in the . Council on Agricultural Sci- Barrett, S. C. H. & I. W. Forno, 1982. Style morph distribution in ence and Technology, Ames: 12. new world populations of Eichhornia crassipes (mart.) Hajek, A. E., B. P. Hurley, M. Kenis, J. R. Garnas, S. J. Bush, M. Solms-Laubach (water hyacinth). Aquatic Botany 13: J. Wingfield, J. C. van Lenteren & M. J. W. Cock, 2016. 299–306. Exotic biological control agents: a solution or contribution Byrne, M., M. P. Hill, M. Robertson, A. King, A. Jadhav, N. to invasions. Biological Invasions 18: 953–969. Katembo, J. Wilson, R. Brudvig & J. Fisher, 2010. Inte- Heard, T. A. & S. L. Winterton, 2000. Interactions between grated Management of water hyacinth in South Africa: nutrient status and weevil herbivory in the biological development of an integrated management plan for water control of water hyacinth. Journal of Applied Ecology 37: 117–127. hyacinth control, combining biological control, herbicidal 15 control and nutrient control, tailored to the climatic regions Hill, J. M., 2014. Investigations of growth metrics and d of South Africa. Water Research Commission Report TT N values of water hyacinth (Eichhornia crassipes, (Mart.) 454/10: 302. Solms-Laub) in relation to biological control. Aquatic Carson, W. P., S. M. Hovick, A. J. Baumert, D. E. Bunker & T. Botany 114: 12–20. H. Pendergast, 2008. Evaluating the post-release efficacy Hill, J. M., R. W. Jones, M. P. Hill & O. L. F. Weyl, 2015. of invasive plant biocontrol by insects: a comprehensive Comparisons of isotopic niche widths of some invasive and approach. Arthropod-Plant Interactions 2: 77–86. indigenous fauna in a South African river. Freshwater Center, T. D., 1994. Biological control of weeds: Water hya- Biology 60: 893–902. cinth and water lettuce. In Rosen, D., F. D. Bennett & J. Hill, M. P., 2003. Impact and Control of alien aquatic vegetation L. Capinera (eds), Pest Management in the Tropics, Bio- in South African aquatic . African Journal of logical Control – A Florida Perspective. UK, Intercept: 28: 19–24. 481–521. Hill, M. P. & C. J. Cilliers, 1999. A Review of the Arthropod Center, T. D. & F. A. Dray Jr., 2010. Bottom–up control of water Natural Enemies, and the Factors That Influence Their hyacinth weevil populations: do the plants regulate the Efficacy, in the Biological Control of Water Hyacinth, insects? Journal of Applied Ecology 47: 329–337. Eichhornia crassipes (Mart.) Solms-Laubach (Pontederi- Center, T. D. & A. D. Wright, 1991. Age and phytochemical aceae), in South Africa. In: Olckers, T. & M. P. Hill, (eds), composition of water hyacinth (Pontederiaceae) leaves Biological Control of Weeds in South Africa (1990–1998). determine their acceptability to Neochetina eichhorniae African Entomology Memoirs 1: 103–112. (Coleoptera: Curculionidae). Environmental Entomology Hill, M. P. & J. A. Coetzee, 2008. Integrated control of water 20: 323–334. hyacinth in Africa. The Authors Journal compilation. Cilliers, C. J., 1991. Biological control of water hyacinth, OEPP/EPPO Bulletin 38(3): 452–457. Eichhornia crassipes (Pontederiaceae) in South Africa. Hill, M. P. & J. Coetzee, 2017. The biological control of aquatic Agriculture, Ecosystems and Environment 37: 207–217. weeds in South Africa: current status and future challenges. Cock, M., R. Day, H. Herren, M. P. Hill, M. H. Julien, P. Bothalia 47(2): a2152. Neuenschwander & J. Ogwang, 2000. Harvesters get that Hill, M. P. & T. Olckers, 2001. Biological control initiatives sinking feeling. Biocontrol News and Information 21: 1–8. against water hyacinth in South Africa: constraining fac- Coetzee, J. A. & M. P. Hill, 2011. The role of in tors, success and new courses of action. In: Julien, M. H., the biological control of water hyacinth, Eichhornia cras- M. P. Hill, T. D. Center & D. Jianqing (eds) Biological and sipes, in South Africa. BioControl 57: 247–261. integrated control of water hyacinth, Eichhornia crassipes. Coetzee, J. A. & M. P. Hill, 2012. The role of eutrophication in Proceedings of the 2nd Meeting of the Global Working the biological control of water hyacinth, Eichhornia cras- Group for the Biological and Integrated Control of water sippes, in South Africa. Biological Control 57: 247–261. hyacinth, Beijing, China, 9–12 October 2000. Australian Coetzee, J. A., R. W. Jones & M. P. Hill, 2014. Water hyacinth, Centre for International Agricultural Research, Canberra: Eichhornia crassipes (Pontederiaceae), reduces benthic 33–38. macroinvertebrate diversity in a protected subtropical lake Hill, M. P., J. A. Coetzee & C. Ueckermann, 2012. Toxic effect in South Africa. Biodiversity and Conservation 23: of herbicides used for water hyacinth control on two insects 1319–1330. released for its biological control in South Africa. Bio- Cuda, J. P., R. Charudattan, M. J. Grodowitz, R. M. Newman, J. control Science and Technology 22: 1321–1333. F. Shearer, M. L. Tamayo & B. Villegas, 2008. Recent Jacot Guillarmod, A., 1979. Water weeds in South Africa. Aquatic Botany 6: 377–391.

123 388 Hydrobiologia (2018) 807:377–388

Jimenez, M. M., E. G. Lopez, R. H. Delgadillo & E. R. Franco, Moran, P. J., 2006. Water nutrients, plant nutrients, and indi- 2001. Importation, rearing, release and establishment of cators of biological control on water at texas field sites. Neochetina bruchi (Coleoptera Curculionidae) for the Journal of Aquatic Plant Management 44: 109–114. biological control of water hyacinth in Mexico. Journal of Mu¨ller-Scha¨rer, H. & U. Schaffner, 2008. Classical biological Aquatic Plant Management 39: 140–143. control: exploiting enemy escape to manage plant inva- Jones, R. W., 2001. Integrated control of water hyacinth on the sions. Biological Invasions 10: 859–874. Nseleni/Mposa Rivers and Lake Nsezi in KwaZulu-Natal, Spencer, D. F. & G. G. Ksander, 2004. Do tissue carbon and South Africa. In: Julien, M. H., M. P. Hill, T. D. Center & limit population growth of weevils introduced to D. Jianqing (eds) Biological and Integrated Control of control water hyacinth at a site in the Sacramento-San Water Hyacinth, Eichhornia crassipes. Proceedings of the Joaquin Delta, California. Journal of Aquatic Plant Man- 2nd Meeting of the Global Working Group for the Bio- agement 42: 45–48. logical and Integrated Control of water hyacinth, Beijing, Te´llez, T. R., E.-M. de Rodrigo Lo´pez, G. L. Granado, E. China, 9–12 October 2000. Australian Centre for Interna- A. Pe´rez, R. M. Lo´pez & J. M. S. Guzma´n, 2008. The water tional Agricultural Research, Canberra, : hyacinth, Eichhornia crassipes: an invasive plant in the 123–129. Guadiana River Basin (Spain). Aquatic Invasions 3: 42–53. Jones, R. W., 2009. The impact on biodiversity, and integrated Thomas, M. B. & A. M. Reid, 2007. Are exotic natural enemies control, of water hyacinth, Eichhornia crassipes (Martius) an effective way of controlling invasive plants? Trends in Solms-Laubach (Pontederiaceae) on the Lake Nsezi – Ecology and Evolution 22: 447–453. Nseleni River System. MSc Thesis, Rhodes University: Tipping, P. W. & T. D. Center, 2002. Evaluating acephate for 1–116. insecticide exclusion of Oxyops vitiosa (Coleoptera: Cur- Jones, R. W., 2015. Aquatic Invasions of the Nseleni River culionidae) from Melaleuca quinquenervia. Florida Ento- System: Causes, Consequences and Control. PhD Thesis, mologist 853: 458–463. Rhodes University: 1–179. Tipping, P. W., M. R. Martin, P. D. Pratt, T. D. Center & M. Jones, R. W., O. L. F. Weyl, E. R. Swartz & M. P. Hill, 2013. B. Rayamajhi, 2008. Suppression of growth and repro- Using a unified invasion framework to characterize Afri- duction of an exotic invasive tree by two introduced ca’s first loricariid catfish invasion. Biological Invasions insects. Biological Control 44: 235–241. 15: 2139–2145. Tipping, P. W., M. R. Martin, E. N. Pokorny, K. R. Nimmo, D. Julien, M. H. & M. W. Griffiths, 1998. Biological control of L. Fitzgerald, F. A. Dray Jr. & T. D. Center, 2014. Current weeds: a world catalogue of agents and their target weeds, levels of suppression of water hyacinth in Florida USA by 4th ed. CABI Publishing, Wallingford: 223. classical biological control agents. Biological Control 71: Lenth, R. V., 2013. lsmeans: least-squares means. R package 65–69. version 1.10–01. http://CRAN.R-project.org/package= Villamagna, A. M. & B. R. Murphy, 2010. Ecological and socio- lsmeans. economic impacts of invasive water hyacinth (Eichhornia May, B. & J. A. Coetzee, 2013. Comparisons of the thermal crassipes): a review. Freshwater Biology 55: 282–298. physiology of water hyacinth biological control agents: Williams, A. E., H. C. Duthie & R. E. Hecky, 2005. Water predicting establishment and distribution pre- and post- hyacinth in Lake Victoria: why did it vanish so quickly and release. Entomologia Experimentalis et Applicata 147: will it return? Aquatic Botany 81: 300–314. 241–250. Wilson, J. R. U., O. Ajuonu, T. D. Center, M. P. Hill, M. Midgley, J. M., M. P. Hill & M. H. Villet, 2006. The effect of H. Julien, F. F. Katagira, P. Neuenschwander, S. W. Njoka, water hyacinth, Eichhornia crassipes (Martius) Solms- J. Ogwang, R. H. Reeder & T. Van, 2007. The decline of Laubach (Pontederiaceae), on benthic biodiversity in two water hyacinth on Lake Victoria was due to biological impoundments on the New Year’s River, South Africa. control by Neochetina spp. Aquatic Botany 87: 90–93. African Journal of Aquatic Science 31: 25–30. Wright, A. D. & T. D. Center, 1984. Predicting population Morin, L., A. M. Reid, N. M. Sims-Chilton, Y. M. Buckley, K. intensity of adult Neochetina eichhorniae (Coleoptera: Dhileepan, G. T. Hastwell, T. L. Nordblom & S. Raghu, Curculionidae) from incidence of feeding on leaves of 2009. Review of approaches to evaluate the effectiveness water hyacinth Eichhornia crassipes. Environmental of weed biological control agents. Biological Control 51: Entomology 13: 1478–1482. 1–15. Xie, Y., M. Wen & D. Yu, 2004. Growth and resource allocation of water hyacinth as affected by gradually increasing nutrient concentrations. Aquatic Botany 79: 257–266.

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