BioControl DOI 10.1007/s10526-011-9393-3 Biological control of invasive aquatic and wetland plants by arthropods: a meta-analysis of data from the last three decades Justin L. Reeves • Patrick D. Lorch Received: 2 February 2011 / Accepted: 4 July 2011 Ó International Organization for Biological Control (IOBC) 2011 Abstract Results from the last three decades of more years) and non-target effect studies could also aquatic and wetland plant biological control by be performed in the future. arthropods were combined using meta-analytical techniques to provide an objective, quantitative Keywords Meta-analysis Á Biological control Á understanding of control efficacy that cannot be Aquatic Á Wetland Á Plant Á Insect provided by available narrative reviews. Analyses were performed to determine if differences exist in how well diverse biocontrol agents perform, and if Introduction experimental design can impact study results. Across all analyses, biocontrol of the included plants was Classical biological control can provide the most generally successful. Though little heterogeneity in ecologically and economically sound methodology efficacy was seen between the individual biocontrol for controlling invasive plants and their negative agents used, all experimental design analyses showed impacts (McFadyen 1998). Recent evaluations of significant differences between respective study biological control of plants (both terrestrial and types. Thus, study design can significantly impact aquatic) have identified a range of factors correlated the results of biocontrol studies. From these results, with effectiveness, but these studies have either been we suggest that field studies with controls be qualitative (e.g., Andres and Bennett 1975; McFa- performed using subsamples of an area (quadrats, dyen 1998; others listed in Cuda et al. 2008)or transects, etc.), with biomass or density being the quantitative but did not compare data within or plant variable measured. More long-term (two or between individual invasive plant and control agent species (Stiling and Cornelissen 2005). Particularly for biological control of invasive aquatic plants, Handling Editor: John Scott many general factors have been shown to influence biological control of a wide range of plant species. J. L. Reeves Á P. D. Lorch Abiotic factors such as climate, habitat conditions, Department of Biological Sciences, Kent State University, Kent, OH 44242, USA and concurrent management tactics such as mechan- ical harvesting or pesticide application have been Present Address: shown to influence biological control efficacy in & J. L. Reeves ( ) multiple systems. Similarly, biotic factors such as Department of Biology, Colorado State University, Fort Collins, CO 80523, USA host-plant quality or genotype, biological control e-mail: [email protected] agent density, and agent mortality factors such as 123 J. L. Reeves, P. D. Lorch predation, parasitism, or disease can also influence reviews of aquatic plant biological control (e.g., control efficacy. More specifically, successful bio- Andres and Bennett 1975; Cuda et al. 2008). Both logical control of water hyacinth (Eichhornia crass- aquatic and wetland plants were included here pies), may be dependent on control agent (larval) because it can be difficult to differentiate between density as well, while larval density is in turn the two plant types (Cuda et al. 2008). Heterogeneity impacted by plant status (Wilson et al. 2006). A between arthropod agents was tested to determine if qualitative review of all of these factors, along with there are any differences in how well the various an overview of the field of biological control of biological control agents have performed when submersed aquatic plants, is provided by Cuda et al. compared to one another (which may help decide (2008). which agents to use for which plants), or at least Though the many factors above have been found which agents have had a significant effect on their to potentially impact biological control efficacy of target plant. Further, because of the wide variety of plants in general, much work still needs to be done, methods that have been used to quantify effects of particularly for aquatic plants (Cuda et al. 2008). biological control agents on their target plants, it was Quantitative reviews of the literature may help to hypothesized that experimental design may influence more fully understand control efficacy and go beyond biological control efficacy. To test this, we quantified the general claims of successful biological control of differences in effect across agents based on experi- aquatic plants that have come from narrative reviews mental design factors such as use of one versus two such as McFadyen (1998). This may be especially biological control agents, experimental (with con- true for understanding how differences in control trols) versus observational (without controls) studies, efficacy depend on which agent is used, or on lab versus field studies, the response variable mea- experimental design, both of which are factors on sured (e.g., plant density, biomass, percent cover, which little or no work (especially quantitative work) weight change, leaf area grazed), the type of replicate has been done on aquatic plants. used (whole lake, subsample of an area, aquaria, or Meta-analysis provides a method for quantitatively individual plants), and finally the study duration. Data synthesizing the results of independent experiments to from the last three decades of biological control work draw general conclusions (see Cooper and Hedges published in a wide variety of journals were used to 1994; Gurevitch and Hedges 2001). Because meta- empirically test these hypotheses and provide a more analysis can be a useful tool for understanding patterns objective exploration of aquatic plant biological across multiple studies, it has been used in many control efficacy than can be provided by narrative ecological fields, including biological control (Stiling reviews. and Cornelissen 2005). Though the meta-analysis performed by Stiling and Cornelissen (2005) included a categorical analysis of weed biological control that Materials and methods showed general control success, it was not specific to aquatic or wetland invasive plants (the plant species Standard meta-analysis techniques were used for this included were not listed), nor were invasive plants the study following Gurevitch and Hedges (2001). Liter- main focus of the study (the study covered the entire ature search methods, data inclusion methods, and field of biological control of all types of organisms). measures to avoid non-independence of data are often There were also no analyses performed to specifically underreported in meta-analysis papers, so included compare individual biological control agent species, below are specific sections to detail these aspects of which can be important in deciding which agents to this study. use for which plants, or at least in examining which agents have worked and which have not. Literature search The purpose of the work presented here was to broadly quantify the efficacy of biological control An extensive list of specialist arthropod biological agents specifically of invasive aquatic and wetland control agents (both candidate agents and currently plants using meta-analytical techniques. This effort employed agents) and their corresponding target was designed to improve on previous narrative invasive aquatic and wetland plants was built through 123 Biological control of invasive aquatic and wetland plants 0.4 history even if no plant data were reported), 126 181 articles reported some sort of agent effects on plants 0.3 (any plant effect measured was included at this stage; some papers in Fig. 1 were included in both lab and field categories when necessary). Of these 126 111 0.2 103 91 articles, 53 articles provided 62 data points appro- 76 priate for meta-analysis (Appendix Table 3) using the 53 data inclusion and analysis methods described below. 0.1 44 38 Proportion of Studies The large discrepancy between the total number of 20 papers and papers with appropriate data for analysis 0.0 ) t t s was a result of searching by agent names rather than n lab rs) ition men nces s p e me ts: +y lo u vipo e fl fec (2 t effect o blish ts e control-type terms like ‘‘biological control’’. This host range) ev c in a ffects: field c . d ti st e fe arg d e f -t (incl. bio n e r an a o term ef on o y / ti rm n was done to make sure papers were not excluded due i it ic la te av nd iot u short g h b op short-term be p lon fecu to the choice of search terms (Cooper and Hedges life history (incl d Study Category 1994), giving as broad an overview of the literature as dist. an possible (as in Stiling and Cornelissen 2005). For the Fig. 1 Categories used to organize papers from literature articles with appropriate data, the models used here search and their overall proportion of the entire set of papers tested for differences in control efficacy based on the (n = 541). Categories were not mutually exclusive, and studies were placed in all appropriate categories. The numbers above biological control agent used (Appendix Table 2). each bar represent the number of studies associated with that Similarly, to examine the impact of experimental respective category design on biological control efficacy across agents, the models used here quantified and compared the intensive internet and literature searches and cross effects of whether one or two biological control referenced with Julien and Griffiths (1998) to make agents were used concurrently in the study, the type sure no agents (or at least agents with published of control used [initial value (observational studies) articles containing biological control data) were or ‘‘real’’ control (experimental studies)], whether the missed. Once the list of agents and plants was study was performed in the lab or field, the response compiled (Appendix Table 2), the literature search variable measured (biomass, density, percent cover, for studies to be used for the meta-analyses was or other related measures), the replicate type used performed in two well-known, comprehensive dat- (individual plant, aquarium, sub-samples of an area, abases: ISI Web of Science and Biological Abstracts.