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Interactions Within Pairs of Biological Control Agents on Water Hyacinth, Eichhornia Crassipes ⇑ Danica Marlin A, , Martin P

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Interactions Within Pairs of Biological Control Agents on Water Hyacinth, Eichhornia Crassipes ⇑ Danica Marlin A, , Martin P Biological Control 67 (2013) 483–490 Contents lists available at ScienceDirect Biological Control journal homepage: www.elsevier.com/locate/ybcon Interactions within pairs of biological control agents on water hyacinth, Eichhornia crassipes ⇑ Danica Marlin a, , Martin P. Hill a, Marcus J. Byrne b a Department of Zoology and Entomology, Rhodes University, P.O. Box 94, Grahamstown 6140, South Africa b School of Animal, Plant and Environmental Sciences, University of the Witwatersrand, Private Bag X3, Wits 2050, Johannesburg, South Africa highlights graphical abstract Water hyacinth was exposed to pair- wise combinations of three biocontrol agents. + = SYNERGISTIC The mite O. terebrantis alone had the EFFECT least impact on plant growth. The mirid E. catarinensis and weevil N. eichhorniae each had negative + = EQUIVALENT EFFECT impacts on plant growth. The mite performed poorly in the presence of mirids and weevils. EQUIVALENT + = EFFECT The mite possibly enhanced the performance of the other two agents. article info abstract Article history: Water hyacinth, Eichhornia crassipes, is an invasive aquatic plant in South Africa where seven biological Received 3 May 2013 control agents have been released on the weed. Combined herbivory by these multiple agents may cause Accepted 11 October 2013 greater damage than any of the agents acting alone. This study examined the effects of herbivory by the Available online 21 October 2013 water hyacinth mite Orthogalumna terebrantis, the mirid Eccritotarsus catarinensis, and the weevil Neoche- tina eichhorniae, singly or in paired combinations, on the weed’s growth. Plants were subjected to herbiv- Keywords: ory and plant growth parameters e.g. production of leaves, and the percentage of the leaf surface area Herbivory damaged by herbivory, were measured every 14 days. Plants subjected to herbivory by mirids only, or Insect interactions weevils only, produced significantly fewer ramets than the control (herbivory-free) plants. Plants sub- Invasive weed Multiple agents jected to mirids only, or a combination of mites with weevils, produced the least number of leaves. Plant Plant–insect interactions petioles were shortest on plants subjected to a combination of mites with weevils, and increases in plant biomass were lowest in plants fed on by weevils or the combination of weevils with mirids. The combi- nation of mites with mirids caused the greatest damage to the leaf surface area. The results suggest that different plant growth parameters are not impacted equally by herbivory, but are dependent on the agent or combination of agents causing damage. Ó 2013 Elsevier Inc. All rights reserved. 1. Introduction forts having been initiated against the weed more than 20 years ago (Cilliers, 1991). To date, seven biocontrol agents have been re- Water hyacinth, Eichhornia crassipes (Martius) Solms-Laubach leased on water hyacinth in South Africa (Coetzee et al., 2011). Pre- (Pontederiaceae), is considered to be the worst aquatic weed in vious studies have investigated the interactions of various South Africa (Hill and Cilliers, 1999), despite biological control ef- biocontrol agents of water hyacinth (Delfosse, 1978a; Caunter and Mohamed, 1990; Moran, 2005; Ajuonu et al., 2009). In general, ⇑ Corresponding author. Present address: Department of Zoology and Entomol- these studies found the use of multiple agents increases stress on ogy, University of Pretoria, Private Bag X20, 0028, South Africa. Fax: +27 12 362 the plant, which reduces its growth more so than when a single 5242. agent is used E-mail addresses: [email protected], [email protected] (D. Marlin). 1049-9644/$ - see front matter Ó 2013 Elsevier Inc. All rights reserved. http://dx.doi.org/10.1016/j.biocontrol.2013.10.006 484 D. Marlin et al. / Biological Control 67 (2013) 483–490 Interspecific interactions influence the performance and fitness Adults of all three species feed on water hyacinth leaves and the of phytophagous insects (Kaplan and Denno, 2007) and also play females of the three species oviposit in the leaf blades (Warner, an important role in structuring insect communities (Denno 1970; Perkins, 1973; Hill et al., 1999), where the mite and mirid et al., 2000). A key manner in which phytophagous insects interact eggs can potentially be removed by the feeding of adult weevils, is through indirect effects involving shared host plants (Kaplan and increasing the possibility of agent interaction. The overall aim Denno, 2007). Herbivore damage may induce plant resistance was thus to examine the interactive effects of O. terebrantis, mechanisms such as the release of toxic secondary metabolites, N. eichhorniae and E. catarinensis on water hyacinth growth. which can indirectly reduce herbivore populations as well as a species preference for that plant (Karban and Baldwin, 1997; 2. Materials and methods Rodriguez-Saona and Thaler, 2005). Insect and mite induced responses of plants to herbivory have been studied in various 2.1. Experimental set-up systems, including water hyacinth, and have yielded a range of conclusions (Karban and Carey, 1984; Agrawal, 1998; Bounfour Healthy, agent-free and undamaged water hyacinth plants of and Tanigoshi, 2001; Coetzee et al., 2007a). similar size were selected from stock cultures of the Agricultural The use of multiple agents occupying different niches to control Research Council – Plant Protection Research Institute (PPRI), Pre- an invasive plant species has been supported both in theory and in toria, South Africa, and used in the experiment. The maintenance of practice (Delfosse, 1978a; Hoffmann and Moran, 1998; Jiménez the plant stock cultures is described elsewhere (Marlin et al., and Balandra, 2007), but also has been criticised as opportunistic 2013). The trial was conducted during summer inside a glasshouse and unscientific (Myers, 1985; Denoth et al., 2002; Crowe and Bou- at the PPRI. The average day and night temperatures in the glass- chier, 2006). A meta-analysis of 51 papers revealed that in only house were 30.72 ± 6.74 °C and 20.65 ± 2.66 °C, respectively. one-quarter of cases was plant performance reduced more by mul- All plants had between four to six leaves at the beginning of the tiple enemies than was predicted from each enemy alone (Ste- experiments. All daughter plants (ramets) and dead matter were phens et al., 2013). However, Denoth et al. (2002) found that in removed from the plants before they were weighed and placed the majority of projects for the biological control of weeds, the like- in pairs into plastic tubs (70 Â 40 Â 35 cm depth). The plants were lihood of control increased as more species of agents were re- held upright by wire rings attached by hooks to the sides of the tub. leased, even though in some instances there might be The tubs were filled with 16 L of water. Potassium nitrate (KNO ) competition between herbivore species on the same plant. In addi- 3 and potassium dihydrogen orthophosphate (KH PO ) were added tion, competition between biocontrol agents used against weeds is 2 4 to each tub as nitrogen (2.5 mg LÀ1) and phosphorous bases not common because the biocontrol agents do not represent the (0.4 mg LÀ1), respectively. These concentrations of KNO and KH full suite of natural enemies present in the country of origin, and 3 2- PO were used because they are representative of the high nutrient because the weed often provides a variety of host niches, which 4 concentrations that are common in many South African fresh may potentially reduce competition for space and food (Denoth water systems (Holmes, 1996). Commercial iron chelate (13% Fe) et al., 2002). also was added to each tub at 1.4 g/16 L water. The water and In comparing the damage caused by multiple agents to that of nutrients in each tub were replaced weekly. individual agents, Hatcher (1995) classified four levels of interac- After four weeks of acclimation to the experimental conditions, tions as follows: (a) synergistic, where the interaction causes a sig- both plants in each tub were randomly selected for infestation nificantly greater reduction in a plant variable than would the with one of the following combinations of agents (namely the mite damage of a single agent, (b) additive, where the interaction causes O. terebrantis, the weevil N. eichhorniae, and the mirid E. catarinen- the same reduction in a plant variable as would the combined sis), as either: (1) only mites, (2) only weevils, (3) only mirids, (4) damage of the agents, (c) equivalent, where the interactions causes mites and weevils, (5) mites and mirids, and (6) weevils and mir- an equivalent reduction in a plant variable as would the damage of ids. No agents were added to the control plants. Each treatment either agent alone, and (d) inhibitory, where the interaction causes was replicated seven times. Prior to introducing the agents, the a significantly lower reduction in a plant variable as would damage weevils and mirids were sexed to ensure a 1:1 sex ratio. Male of the weaker of two agents. The additive classification was ad- and female O. terebrantis are morphologically indistinguishable justed by Turner et al. (2010) so that an interaction is additive if (Perkins, 1973) and were therefore not sexed. In natural field pop- the impact of multiple agents is greater than that of the most dam- ulations, mites occur in approximately equal proportions of adult aging agent acting alone but less than or equal to the added im- females and males (Walter, 2009), so a 1:1 sex ratio was assumed. pacts of each agent acting alone. Mites were added at 150 mites/plant, weevils were added at 2 For water hyacinth, the interactions between the sap-sucking adult pairs/plant and mirids were added at 15 adult pairs/plant. mirid Eccritotarsus catarinensis (Carvalho) (Hemiptera: Miridae) These insect stocking densities were sufficient to cause visible and the petiole-mining weevils Neochetina eichhorniae Warner damage to the plant and reduce some of the plant growth param- and Neochetina bruchi Hustache (Coleoptera: Curculionidae) have eters (Marlin, 2011).
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