Biological Control 32 (2005) 90–96 www.elsevier.com/locate/ybcon Impact of the biocontrol agent Eccritotarsus catarinensis, a sap-feeding mirid, on the competitive performance of waterhyacinth, Eichhornia crassipes Julie A. Coetzeea,*, Ted D. Centerb, Marcus J. Byrnea, Martin P. Hillc a Ecophysiological Studies Research Group, School of Animal, Plant and Environmental Sciences, University of the Witwatersrand, Private Bag X3, Johannesburg 2050, South Africa b US Department of Agriculture, Agricultural Research Service, Invasive Plant Research Laboratory, 3205 College Ave., Fort Lauderdale, FL 33314, USA c Department of Zoology and Entomology, Rhodes University, P.O. Box 94, Grahamstown 6140, South Africa Received 4 December 2003; accepted 6 August 2004 Available online 25 November 2004 Abstract The mirid, Eccritotarsus catarinensis, was released in South Africa to aid in the biological control of waterhyacinth (Eichhornia crassipes). Post-release evaluations are needed to quantify the miridÕs impact on the weed in South Africa. The subtle feeding dam- age that it causes is not easily measured, but studies have shown that interactions with other plant stresses, e.g., plant competition, can often magnify impacts of plant-feeding insects. The impact of the mirid was therefore evaluated using an additive series analysis of competition between waterhyacinth and waterlettuce (Pistia stratiotes), as influenced by mirid herbivory. Competitive abilities of waterlettuce and waterhyacinth were determined using an inverse linear model with plant weight as the yield variable. In the absence of herbivory, waterhyacinth was 23 times more competitive than waterlettuce, but only 10 times more competitive when exposed to mirid feeding. Waterlettuce was only 0.9 times as aggressive as waterhyacinth that was free of herbivory, but 1.5 times as competitive when mirids were impacting waterhyacinth. Most importantly, in the presence of herbivory on waterhyacinth, interspecific compe- tition coefficients from waterhyacinth on waterlettuce were no longer statistically significant. These results show that the mirid desta- bilizes waterhyacinthÕs competitive interactions between these two floating plant species, although impacts were subtle. This insect is unlikely to be an effective agent by itself, but it will be a useful complement to the existing biological control agents in South Africa. Ó 2004 Elsevier Inc. All rights reserved. Keywords: Eccritotarsus catarinensis; Eichhornia crassipes; Pistia stratiotes; Biological control; Competition; Herbivory; Risk assessment 1. Introduction worldwide (Julien and Griffiths, 1998). Some have suc- cessfully controlled waterhyacinth in tropical regions, Waterhyacinth (Eichhornia crassipes (Mart.) Solms- such as Papua New Guinea (Julien and Orapa, 1999) Laub (Pontederiaceae)) has achieved international noto- and Lake Victoria in Uganda (Cock et al., 2000). How- riety as the worldÕs worst aquatic weed (Holm et al., ever, additional agents are being considered for release 1977), and has, as a result, been targeted for biological in more temperate regions, such as South Africa and control in several countries (Harley, 1990). At least se- North America, where results have been more variable ven natural enemies have been used for this purpose (Cordo, 1999; Stanley and Julien, 1999). Five arthropod natural enemies of waterhyacinth * Corresponding author. Fax: +27 11 403 1429. have been released in South Africa, and more are being E-mail address: [email protected] (J.A. Coetzee). considered (Hill and Cilliers, 1999). The mirid Eccrito- 1049-9644/$ - see front matter Ó 2004 Elsevier Inc. All rights reserved. doi:10.1016/j.biocontrol.2004.08.001 J.A. Coetzee et al. / Biological Control 32 (2005) 90–96 91 tarsus catarinensis (Carvalho) (Heteroptera: Miridae) et al., 1999). Because no biocontrol agent comes without was introduced in 1996 (Hill et al., 1999) and, although risks, and because of doubts as to potential benefits of populations have established, its performance has yet to the mirid, we employed competition studies to magnify, be assessed. Inasmuch as each new biocontrol agent and thereby quantify, subtle sublethal effects of its feed- might present additional risk to the native flora (Sim- ing. The mirid does not feed on waterlettuce (Hill et al., berloff and Stiling, 1996), assessments of the perfor- 1999), another floating species that commonly coexists mance of existing agents are needed to determine with waterhyacinth, so it was chosen as the competing whether further introductions are warranted. species. Even though it is fundamentally important to under- This study follows the protocol employed by Pantone stand the effects of biological control agents on native et al. (1989), who suggested competition experiments flora, typically, their effectiveness is almost always as- using an additive series, and the application of the in- sessed by measuring their direct effects on the target verse linear model as effective methods for evaluating weeds (Callaway et al., 1999). However, impacts are of- the efficacy of potential control agents. These methods ten sublethal and experiments fail to detect subtle effects provide biologically meaningful competition coeffi- that accrue over time and provide significant long-term cients, which will allow for direct comparison with other control. Furthermore, feeding damage by sap-feeding in- similar competition studies. sects is often inconspicuous and without overt symp- toms. Attention has therefore recently focused on exploiting the interaction between herbivory and plant 2. Materials and methods competition, and their combined effects on plant perfor- mance, as a means of assessing the value of new agents Waterhyacinth and waterlettuce were grown out- (e.g., Ang et al., 1994; Story et al., 2000; Van et al., 1998). doors in plastic tubs at the University of the Witwaters- The effects of biological control agents that do not in- rand, Johannesburg, to determine competitive flict direct mortality on the target plant can be difficult interactions between the two plant species. Both plants to measure. It has been suggested that the impact of were obtained from stock cultures maintained at the invertebrate herbivory will become more noticeable university. The experimental design employed an addi- when grazed plants are competing with other plants tive series (Spitters, 1983) of factorial combinations of for resources, due to a gradual reduction of the host different densities of the two species in a randomized plantÕs vigor (Center et al., 2001). Therefore, any reduc- block design. The waterhyacinth:waterlettuce densities tion in the competitive ability of grazed plants may be were 0:3, 0:9, 3:0, 3:3, 3:9, 9:0, 9:3, and 9:9 plants per sufficient to increase their susceptibility to competition container. The waterhyacinth:waterlettuce density from other plants (Cottam, 1986; Whittaker, 1979). matrices were repeated twice—one series as a control Thus, a fundamental justification for using biological without insects and the other with the mirid E. catarin- control agents to suppress invasive plants is that by ensis in a randomized block design. The two matrices weakening the invader, indigenous species may gain a were repeated three times, resulting in 48 tubs of differ- competitive advantage (Callaway et al., 1999). Further- ent plant combinations. more, Crawley (1989) noted that the principal effect of The plastic tubs (51 cm by 40 cm and 28 cm deep) herbivores is not caused by them eating the plants to were filled with 23 L water. Nitrogen and phosphorus extinction, but more often from their feeding modifying were added as potassium nitrate (KNO3) and potassium the relative competitive abilities of the plants with one dihydrogen orthophosphate (KH2PO4), respectively, at another. concentrations of 50.5 mg N/L and 2.56 mg P/L, the Biological control studies conducted to determine the concentrations at which maximum N storage occurs in combined effect of herbivory and plant competition on waterhyacinth (Reddy et al., 1989, 1990). A commercial plant performance have shown that by combining iron chelate (13% Fe) was also added to the water at a strong plant competitors with biological control agents, concentration of 2 g/23 L of water. Water and nutrients the control obtained exceeds that exerted by either were replaced weekly. Each plastic tub was enclosed by mechanism alone (e.g., Ang et al., 1994; Story et al., a net canopy. 2000; Van et al., 1998). When grown together in the ab- Two weeks later, all daughter ramets were removed sence of natural enemies, waterhyacinth dominates wat- from the plants to reestablish the prescribed stocking erlettuce in nutrient enriched waters (Agami and Reddy, densities. Thereafter, 15 insects per waterhyacinth plant, 1990). Therefore, if this interaction changes in the pres- collected randomly from the Plant Protection Research ence of herbivory, we can assume that the biological Institute in Pretoria, South Africa, were released into control agent has reduced the vigor, and therefore the each cage. The male:female ratio was not controlled as competitive ability, of waterhyacinth. the mirid exhibits a 50:50 sex ratio. Feeding damage to Eccritotarsus catarinensis, a sap-sucking mirid, pro- the waterhyacinth plants and mirid numbers were mon- duces damage that is not usually lethal to the plant (Hill itored visually for the first 4 weeks to ensure that the 92 J.A. Coetzee et al. / Biological Control 32 (2005) 90–96 mirids had established and were feeding on waterhya- culated