Biological Control of Aquatic Plants: Review of a native watermilfoil herbivore

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1 Biological Control of Aquatic Plants: Review of a native watermilfoil herbivore Kallie Kessler Kallie.Kessler@colostate.edu Chemical Ecology, Spring 2016 Colorado State University 1

2 Abstract The exotic, submersed macrophyte, Eurasian watermilfoil (Myriophyllum spicatum), forms monotypic mats in lotic and lentic waterways, reducing the quality of invaded freshwater ecosystems throughout the majority of the U.S. Due to these detrimental effects, researchers have developed several chemical, cultural, mechanical and biological management methods that target the reduction of this ecologically and economically damaging species. A native milfoil weevil (Euhrychiopsis lecontei) exhibits the highest level of herbivory on watermilfoil of any native species evaluated. Studies have confirmed that the weevil is a specialist herbivore on Myriophyllum spp., preferentially feeding and ovipositing on Eurasian watermilfoil when compared to other submersed aquatic species. Most milfoil injury is due to vascular damage from larvae as they consume meristematic and stem tissue, eventually boring a chamber in the stem to pupate. Studies have shown that adult weevils are attracted to Myriophyllum spp. by both chemical and visual cues. Visual cues aid weevils in locating submersed aquatic hosts after emerging from overwintering habitat; while chemical cues, likely glycogen and uracil, guide weevils to the apical meristem of Eurasian watermilfoil preferentially over native watermilfoils within the same genus. Short term to long term studies conducted under laboratory and field conditions have consistently observed a decrease in milfoil population, density and/or biomass indicating that the weevil does decrease milfoil fitness; however, it has yet to be determined whether fitness is decreased enough to restore the ecological structure and function to invaded freshwater ecosystems. Early research focusing on trophic interactions has hypothesized that weevil population decline occurs in the presence of higher trophic level predators although results are currently inconclusive. Future research should focus on evaluating milfoil weevil preference and fitness on hybrid watermilfoil (M. spicatum x M. sibiricum). 2

3 Introduction The use of traditional biological control agents to manage problematic exotic species exploits the Enemy Release Hypothesis (ERH). The ERH hypothesis states that plant species introduced to a new range lack natural enemies, including specialist and generalist herbivores, which had previously coevolved with the introduced species within its native range. The lack of natural enemies may enable some introduced species to allocate more energy into growth and reproduction instead of defense mechanisms, causing an increase in fitness. Increased fitness may give introduced species a competitive edge, resulting in monotypic stands as the introduced species outcompetes native species and become invasive, creating new ecosystems with little ecological structure or function (Cogni, 2010). In biological control, highly specialized herbivores or predators that rely on the invasive species as a host plant may be released into invaded and degraded areas to reduce the fitness of the invasive plant, allowing native plants to successfully compete within invaded areas. Traditional biological control is expensive and difficult due to the amount of regulatory guidelines and testing required to obtain approval to release a nonindigenous species into a new range, thus native or naturalized species are increasingly evaluated as biological control agents (Madsen et al., 2000). The utilization and success of native or naturalized species is in opposition of the enemy release hypothesis; however, this new biological control strategy is becoming increasingly more common. The primary hypothesis is that the native predator and invasive host do not share an evolutionary history thus the invasive host has not evolved the defenses necessary to deter a native specialist predator (Parker and Hay, 2005). One of the most widely studied native aquatic biological control agents is a specialist milfoil weevil (Euhrychiopsis lecontei) that feeds on the invasive submerged aquatic plant, Eurasian watermilfoil (Myriophyllum spicatum)(newman, 2004). Eurasian watermilfoil forms dense monotypic stands, commonly outcompeting all submersed aquatic vegetation within a lake s water column. In addition to 3

4 detrimental ecological impacts, it has been documented that lakes infested with Eurasian watermilfoil have decreased property values, as recreational activities like swimming, boating and fishing can be negatively impacted (Eiswerth et al., 2000). These ecological and economical impacts have resulted in the development of chemical, cultural, mechanical and biological management methods that target Eurasian watermilfoil. As the species continues to spread across North America, successful biological control agents are becoming more appealing to water managers as they should not require yearly labor and monetary expenditures (Sheldon and Creed, 1995). Previous to the introduction of Eurasian watermilfoil, the milfoil weevil was a specialist herbivore on a native species within the same genus with overlapping habitat requirements, northern watermilfoil (Myriophyllum sibiricum) (Solarz and Newman, 2001). Much research has been conducted on the milfoil weevil including: distribution and life history studies, host selection and population establishment studies that show preferences based on chemical and visual attractants, and evaluation of potential trophic interactions that may cause a decline in milfoil weevil abundance. Euhrychiopsis lecontei Life History and Distribution Milfoil weevils have two primary life stages. First, fully developed adults that overwinter on soil and litter along the shoreline in terrestrial habitats and secondly, in-lake development and reproduction that occurs entirely while submersed in the water column. The majority of research has focused on the inlake development life stage because it is during this stage that damage to Eurasian watermilfoil stems occurs. During the spring, milfoil weevils emerge from overwintering habitat and enter the lake by flying and/or walking into an adjacent waterway. Immediately, they locate and begin to feed on the top of watermilfoil plants, typically targeting apical meristems. Herbivory continues until water temperatures reach 15 C. At this point, females complete egg development and begin oviposition on watermilfoil apical meristems (Newman et al., 2001). During this period, females are capable of ovipositing 1 to 4 4

5 eggs on one or more meristems daily (Sheldon and Jones, 2001). Under constant water temperature, milfoil weevil larvae mine stems for 7 to 8 days, mining approximately 15 cm of stem until their development is completed. After larval development, it takes an additional 21 days before adult development is complete and reproduction begins. Due to this rapid development time, it is possible to have six generations of the weevil produced in one summer, with an average of three to four generations (Mazzei et al., 1999). In late summer, likely triggered by day length shortening, adults stop oviposition and allocate energy to the development of flight muscles after females have mated. Milfoil weevils then fly to the shoreline, overwintering in the top 5 cm of soil and litter (Newman and Inglis, 2009). Recent research has focused on the importance of overwintering habitat as it is a potential indicator of in-water densities over a course of several years. Milfoil weevils have been found within two meters of the shoreline but prefer drier soils with abundant leaf litter. Additionally, no parasitoids were observed to emerge from overwintering adults contributing to a 60% overwintering survival rate (Newman et al., 2001) Survey studies have attempted to quantify milfoil weevil density and distribution throughout North America, with most surveys focusing on the northern regions of the United States, within the milfoil weevil s temperature regime and where Eurasian watermilfoil has been the most successful and problematic (Creed, 2000). Based on laboratory studies, the milfoil weevil is not predicted to survive in waters above 34 or 35 C, limiting the possible range of this biological control agent (Sheldon and Obryan, 1996). These same researchers evaluated water quality parameters to better predict the presence of milfoil weevils. They found that milfoil weevils were more likely to be found in waterbodies with a ph 8.2 and a specific conductance 0.2 ms cm -1 (Tamayo et al., 2000). While it is important to understand how water quality parameters affect milfoil weevil success, more information on current milfoil weevil distribution is needed. Most traditional biological control agents are not ubiquitous in the environment and require several introductions into invaded areas and regions. As this biological control 5

6 agent is a native species, understanding its current distribution for Eurasian watermilfoil is vital. A larger, more complete survey of the northern United States would provide a better understanding of whether this species requires further introduction into invaded waterways. Population Establishment and Host Specificity Although it is predicted that the milfoil weevil coevolved with the native watermilfoil species, northern watermilfoil, observational studies suggest that milfoil weevils preferentially choose to consume and oviposit on invasive Eurasian watermilfoil (Sheldon and Jones, 2001, Solarz and Newman, 1996). Studies have shown empirical evidence that milfoil weevils are more strongly attracted to Eurasian watermilfoil than other species within the Myriophyllum genus. These studies have focused on elucidating both chemical and visual cues and it is likely that both aid in the milfoil weevil s ability to locate and chose Eurasian watermilfoil plants as a host. Marko et al. (2005) conducted choice bioassays that revealed milfoil weevils were attracted to the chemicals glycerol and uracil. Interestingly, these compounds are ubiquitous in both plants and aquatic environments. In fact, both glycerol and uracil were present in exudates from all species within the study (M. sibiricum, M. spicatum, M. alterniflorum, M. tenellum, and Ceratophyllum demersum); however, Eurasian watermilfoil released higher concentrations of both uracil and glycerol than all other species tested. Glycerol is a general osmolyte produced by both terrestrial and aquatic plants. In this study, weevils were attracted to synthetic glycerol up to a concentration of 10 µmol. In choice studies, synthetically produced uracil attracted milfoil weevils at much lower concentrations then glycerol. Specifically, 55% of weevils were attracted to nmol uracil. Uracil is a plant metabolite that is likely costly to exude into the environment. It is vital to the production of uridine nucleosides that are found at higher concentrations in young tissue, such as the apical meristem (Schmidt et al., 2004). As previous studies have reported, milfoil weevils graze the apical meristems of watermilfoil plants. Oviposition also 6

7 occurs on the apical meristem so it is likely that uracil exudation from the apical meristem is a strong attractant for both the feeding larva and reproducing femals. It would be beneficial to repeat this study by extracting exudates from only the apical meristem instead of full stems to better identify the location of uracil secretion and its potential effect as a milfoil weevil attractant. Additionally, this study claimed to support an earlier study by Solarz and Newman (1996) where milfoil weevils were attracted to Eurasian watermilfoil under both light and dark conditions (Marko et al., 2005). In Solarz and Newman (1996) study they came to some interesting conclusions. They studied two sequential generations of milfoil weevils. If the first generation was reared on northern watermilfoil, there was no difference in offspring oviposition preference between northern watermilfoil or Eurasian watermilfoil; however, if the first generation was reared on Eurasian watermilfoil, the milfoil weevils had a strong preference to oviposit on Eurasian watermilfoil instead of northern watermilfoil in the second generation. This study has been supported by more recent oviposition choice trials in which milfoil weevils reared on Eurasian watermilfoil did not only preferentially oviposit on Eurasian watermilfoil, but also exhibited greater fecundity than when reared on northern watermilfoil (Sheldon and Jones, 2001). Additional studies have provided evidence that milfoil weevils use visual cues to locate and select Eurasian watermilfoil. It was hypothesized that because adult milfoil weevils overwinter on land visual cues likely play a role in the adult flying to or walking into adjacent lakes and/or waterways and locating submersed plant hosts. Additionally, the physical structure of milfoil weevils indicates that visual cues may be vital in locating Myriophyllum spp. hosts as they have large eyes relative to their head size and are poor swimmers with narrow legs (Reeves et al., 2009). Researchers reported that in light-dark experiments, milfoil weevils were much more likely to locate sealed vials of Eurasian watermilfoil in the light than the dark. Additionally, the weevils preferred vials containing Eurasian watermilfoil over empty vials. During these trials milfoil weevils did not preferentially choose Eurasian watermilfoil over C. demersum, a native submersed aquatic species. In contrast, during a follow-up 7

8 study, Reeves and Lorch (2009) reported that milfoil weevils actually did preferentially choose Eurasian watermilfoil over C. demersum in modified choice experiments. They cite a flaw in the original experimental design as the reason their previous results were neither statistically significant nor repeatable. In previous studies, where Eurasian watermilfoil was not preferentially chosen, vials were placed too far away from the weevil and the milfoil weevils likely swam towards the first plant they saw, regardless of species, due to their poor swimming ability. As Reeves and Lorch (2009) postulated, species within the Myriophyllium genus are structurally quite different from C. demersum but the majority of species within the genus Myriophyllium are structurally very similar. In fact, the majority of the time researchers are unable to visually differentiate between some members of the Myriophyllum genus. Specifically, northern and Eurasian watermilfoil individuals are so similar that genetic tests have been developed to differentiate between these two species rather then relying on morphological polymorphisms (Moody and Les, 2002). Future research should focus on defining the interaction between both visual and chemical cues as they are likely both involved in ensuring that the weevil is able to locate a potentially distant host plant within large bodies of water. Trophic Interactions Trophic interaction are often unaccounted for in laboratory and field choice experiments and it often further complicates the evaluation of the milfoil weevil s success as a biological control agent. Researchers have suggested that the reason milfoil weevils provide variable Eurasian watermilfoil reduction is due to the presence of weevil predators in invaded lakes (Creed, 2000, Parker and Hay, 2005, Sutter and Newman, 1997, Ward and Newman, 2006). Early field studies focused on the dominant macroinvertebrate predator in some lake ecosystems, yellow perch (Perca flavescens). They reported that within and outside of perch exclosures, milfoil weevil abundance did not differ. Additionally, no milfoil weevils were found within the stomachs of perch feeding within Eurasian 8

9 watermilfoil populations where the milfoil weevil was present (Creed, 2000, Sutter and Newman, 1997). Studies focusing on a different fish species, bluegill sunfish (Lepomis macrochirus), have observed some adult milfoil weevils in bluegill sunfish stomachs prompting the authors to conclude that in lakes with high sunfish densities and low milfoil weevil abundances, predation may decrease the weevil s success as a biological control agent (Sutter and Newman, 1997). Subsequent studies investigated this conclusion using a combination of field experiments and multiple-lake surveys. In field experiments, milfoil weevils were predated by several species of sunfish, resulting in a decrease of milfoil weevil abundance outside of sunfish exclosures compared to within the sunfish exclosures. The multiple-lake survey s results further supported these conclusions as herbivore abundance was negatively corrected to sunfish density (Ward and Newman, 2006). The majority of these studies have focused on fish predation; however, observational evidence suggests that future studies should focus on other invertebrate predators (e.g. damselflies and dragonflies) as larvae may be more vulnerable to predation by carnivorous insects (Creed, 2000). Additionally, none of these species differentiated between species of watermilfoil so multi-trophic level studies are still needed. Future Challenges While a strong foundation for the evaluation and success of the native milfoil weevil has been laid, there are still arguably more questions than answers as the field of aquatic plant management is ever evolving. Current research suggests that hybrids between Eurasian watermilfoil and northern watermilfoil are more prevalent than previously expected (LaRue et al., 2013). Many of the choice bioassays conducted in the research discussed did not include northern watermilfoil and almost all studies did not evaluate milfoil weevil preference towards hybrid watermilfoils. Currently, there are few studies that focused on milfoil weevil herbivory on hybrid watermilfoils (Borrowman et al., 2014, Borrowman et al., 2015, Roley and Newman, 2006). Preliminary results are positive, indicating that 9

10 milfoil weevils may be more attracted to hybrid watermilfoil individuals than Eurasian watermilfoil. The results of a laboratory study evaluating survivorship on northern watermilfoil, Eurasian watermilfoil and hybrid watermilfoil showed increased survivorship on hybrid watermilfoil stems when compared to survivorship observed on stems of both parents (Borrowman et al., 2015). To my knowledge, none of the classical chemical ecology studies targeting elucidating chemical and/or visual cues have been repeated using hybrid watermilfoils providing an open avenue for an entirely novel area of research. Overall, as our knowledge base of native or naturalized aquatic biological control agents increases, it is likely that milfoil weevils will play an important role in reducing the fitness of Eurasian watermilfoil and hybrid watermilfoil populations within invaded waterway, helping to restore both the structure and function of these vital ecosystems. 10

11 Literature Citations Borrowman, K., E.P.S. Sager, and R. Thum Distribution of biotypes and hybrids of myriophyllum spicatum and associated euhrychiopsis lecontei in lakes of central ontario, canada. Lake and Reservoir mmanagement 30: Borrowman, K.R., E.P. Sager, and R.A. Thum Growth and developmental performance of the milfoil weevil on distinct lineages of eurasian watermilfoil and a northern x eurasian hybrid. Journal of Aquatic Plant Management 53: Cogni, R Resistance to plant invasion? A native specialist herbivore shows preference for and higher fitness on an introduced host. Biotropica 42: Creed, R.P The weevil-watermilfoil interaction at different spatial scales: What we know and what we need to know. Journal of Aquatic Plant Management 38: Eiswerth, M.E., S.G. Donaldson, and W.S. Johnson Potential environmental impacts and economic damages of eurasian watermilfoil (myriophyllum spicatum) in western nevada and northeastern california. Weed Technology 14: LaRue, E.A., M.P. Zuellig, M.D. Netherland, M.A. Heilman, and R.A. Thum Hybrid watermilfoil lineages are more invasive and less sensitive to a commonly used herbicide than their exotic parent (eurasian watermilfoil). Evolutionary Applications 6: Madsen, J.D., H. Crosson, K. Hamel, M. Hilovsky, and C. Welling Panel discussion-management of eurasian watermilfoil in the united states using native insects: State regulatory and management issues. Journal of Aquatic Plant Management 38: Marko, M., R. Newman, and F. Gleason Chemically mediated host-plant selection by the milfoil weevil: A freshwater insect plant interaction. Journal of Chemical Ecology 31:

12 Mazzei, K.C., R.M. Newman, A. Loos, and D.W. Ragsdale Developmental rates of the native milfoil weevil, euhrychiopsis lecontei, and damage to eurasian watermilfoil at constant temperatures. Biological Control 16: Moody, M.L., and D.H. Les Evidence of hybridity in invasive watermilfoil (myriophyllum) populations. Proceedings of the National Academy of Sciences 99: Newman, R Invited review: Biological control of eurasian watermilfoil by aquatic insects: Basic insights from an applied problem. Hydrobiology 159: Newman, R.M., D.W. Ragsdale, A. Milles, and C. Oien Overwinter habitat and the relationship of overwinter to in-lake densities of the milfoil weevil, euhrychiopsis lecontei, a eurasian watermilfoil biological control agent. Journal of Aquatic Plant Management 39: Parker, J.D., and M.E. Hay Biotic resistance to plant invasions? Native herbivores prefer nonnative plants. Ecology Letters 8: Reeves, J., P. Lorch, and M. Kershner Vision is important for plant location by the phytophagous aquatic specialist euhrychiopsis lecontei dietz (coleoptera: Curculionidae). Journal of Insect Behavior 22: Reeves, J.L., and P.D. Lorch Visual plant differentiation by the milfoil weevil, euhrychiopsis lecontei dietz (coleoptera: Curculionidae). Journal of Insect Behavior 22: Roley, S.S., and R.M. Newman Developmental performance of the milfoil weevil, euhrychiopsis lecontei (coleoptera : Curculionidae), on northern watermilfoil, eurasian watermilfbil, and hybrid (northern x eurasian) watermilfoil. Environmental Entomology 35: Schmidt, A., Y.-H. Su, R. Kunze, S. Warner, M. Hewitt, R.D. Slocum, U. Ludewig, W.B. Frommer, and M. Desimone Ups1 and ups2 from arabidopsis mediate high affinity transport of uracil and 5- fluorouracil. Journal of Biological Chemistry 279:

13 Sheldon, S., and R. Creed Use of a native insect as a biological control for an introduced weed. Ecological Applications 5: Sheldon, S.P., and K.N. Jones Restricted gene flow according to host plant in an herbivore feeding on native and exotic watermilfoils (myriophyllum: Haloragaceae). International Journal of Plant Sciences 162: Sheldon, S.P., and L.M. Obryan Life history of the weevil euhrychiopsis lecontei, a potential biological control agent of eurasian watermilfoil. Entomological News 107: Solarz, S.L., and R.M. Newman Oviposition specificity and behavior of the watermilfoil specialist euhrychiopsis lecontei. Oecologia 106: Solarz, S.L., and R.M. Newman Variation in hostplant preference and performance by the milfoil weevil, euhrychiopsis lecontei dietz, exposed to native and exotic watermilfoils. Oecologia 126: Sutter, T.J., and R.M. Newman Is predation by sunfish (lepomis spp.) an important source of mortality for the eurasian watermilfoil biocontrol agent euhrychiopsis lecontei? Journal of Freshwater Ecology 12: Tamayo, M., C.E. Grue, and K. Hamel Relationship between water quality, watermilfoil frequency, and weevil distribution in the state of washington. Journal of Aquatic Plant Management 38: Ward, D., and R. Newman Fish predation on eurasian watermilfoil (myriophyllum spicatum) herbivores and indirect effects on macrophytes. Canadian Journal of Fisheries and Aquatic Sciences 63: