Variation in hostplant preference and performance by the milfoil weevil, Euhrychiopsis lecontei Dietz, exposed to native and exotic watermilfoils

Exotic plants often displace native plants and thus alter the availability of native hostplants for specialist herbivorous insects. The submersed aquatic weevil Euhrychiopsis lecontei Dietz is endemic to North America, but there are now source populations on the exotic Eurasian watermilfoil (Myriophyllum spicatum L.) as well as on the weevil's ancestral host, northern watermilfoil (Myriophyllum sibiricum Komarov). This provides an opportunity to examine a host range expansion in progress. To further define the host range of the weevil and to determine how population source and rearing plant influence host plant preference and performance, we conducted a series of preference and rearing experiments with weevils from two source populations reared on northern milfoil, on Eurasian milfoil, switched late in larval development from northern to Eurasian milfoil, and vice versa. We also included two rearing treatments with milfoils on which the weevil has not been documented: the native M. verticillatum L. and the exotic M. aquaticum Verd. Preference by weevils in the switched rearing treatments was similar to preferences exhibited by weevils reared solely on the second (later) milfoil species and an increase in preference for Eurasian milfoil was induced by adult exposure to Eurasian milfoil for 2 weeks. In contrast, sizes and development times of weevils in the switched rearing treatments were similar to sizes and development times exhibited by weevils reared solely on the first (early) milfoil species. These results indicate that preference by the milfoil weevil is determined late in larval development or later and Hopkins' host selection principle is not supported. However, size and development time were most affected by hostplant quality during larval development when larvae must acquire the resources needed for pupation. Oviposition preference in the milfoil weevil was a population attribute, not a fixed individual attribute and there was no significant variation in preference among individuals reared on northern milfoil, but significant variation in preference was detected among weevils reared on Eurasian milfoil. Weevils oviposited on all four milfoil species and completed development on three of them, but did not develop beyond the larval stage on M. aquaticum. Weevils reared on Eurasian milfoil developed faster and reached larger adult sizes than weevils in any other rearing treatment. The smallest sizes and longest development times were for weevils reared on the natives, northern milfoil and M. verticillatum. The milfoil weevil oviposits on an array of milfoil species and is unable to distinguish an unsuitable host (M. aquaticum) within this genus. The influence of rearing plant and adult exposure to Eurasian milfoil on hostplant preference suggests that host range expansion to novel congeners may occur more rapidly than predicted by models which assume that genetic variation is required. Significant variation among individuals in hostplant preference suggests the potential for a host shift to a plant for which E. lecontei appears pre-adapted.     

Vision is Important for Plant Location by the Phytophagous Aquatic Specialist Euhrychiopsis lecontei Dietz (Coleoptera: Curculionidae)

The aquatic milfoil weevil Euhrychiopsis lecontei Dietz (Coleoptera: Curculionidae) is a specialist on Myriophyllum spp. and is used as a biological control agent for Eurasian watermilfoil (Myriophyllum spicatum L.), an invasive aquatic macrophyte. We show evidence that visual cues are important for plant detection by these weevils. Weevils had difficulty locating plants in dark conditions and were highly attracted to plant stems in the light, even when the plant sample was sealed in a vial. However, weevils were equally attracted to both M. spicatum and another aquatic macrophyte, coontail (Ceratophyllum demersum L.) in vials. Turbidity (0–100 NTU) did not significantly influence visual plant detection by the weevils. This work fills a void in the literature regarding visual plant location by aquatic specialists and may help lead to a better understanding of when and where these weevils will find, accept, and damage their target host-plants.     

Effects of milfoil weevils and weather on the control of Eurasian watermilfoil

We examined the response of Eurasian watermilfoil (Myriophyllum spicatum) coverage on Manistee Lake, Michigan (U.S.A.) in the presence of milfoil weevils (Euhrychiopsis lecontei). Among 150 sites, milfoil presence declined from 2008 levels of 34 (23%) sites to 2 (1%) sites by 2015 coincident with cumulative stocking of 259,500 weevils from 2007 to 2014. Severe winter temperatures also were associated with milfoil declines. Each 1°C decline in average low temperature during the preceding winter was associated with 3.4 (95% CI 0.8–6.1) fewer sites with milfoil. Impacts of weevil herbivory on watermilfoil may be accentuated by severe winter temperatures. Lake managers should, when possible, integrate weather conditions with weevil stocking regimes to control Eurasian watermilfoil.     

Modeling the interaction between the exotic invasive aquatic macrophyte <Emphasis Type="Italic">Myriophyllum spicatum</Emphasis> and the native biocontrol agent <Emphasis Type="Italic">Euhrychiopsis lecontei</Emphasis> to improve augmented management programs

Mathematical modeling is used to investigate control of the invasive aquatic plant Myriophyllum spicatum L. by the native watermilfoil weevil Euhrychiopsis lecontei Dietz. An age-structured population model with discrete development class is used to separate the destructive activity of Euhrychiopsis lecontei Dietz larvae from the relatively benign activity of the other developmental stages. Empirical model behavior is evaluated and agrees with expected system characteristics. Simulation results demonstrate diminishing returns in the control impact of E. lecontei Dietz as a function of population stocking density. These results indicate that predictive modeling of this type may be used to optimize the utilization of Euhrychiopsis lecontei Dietz as a biological control agent.     

Visual Active Space of the Milfoil Weevil, <Emphasis Type="Italic">Euhrychiopsis lecontei</Emphasis> Dietz (Coleoptera: Curculionidae)

Euhrychiopsis lecontei Dietz (Coleoptera: Curculionidae), a native weevil, is used as a biological control agent for the invasive aquatic macrophyte, Eurasian watermilfoil (Myriophyllum spicatum L.). Because E. lecontei overwinters on land in the adult stage and must find plants in lakes each spring, plant finding behaviors are essential to eventually understanding and predicting long term biological control. Our research showed that E. lecontei is visually attracted to M. spicatum at up to 17.5 cm, and is more attracted to plants than other visual stimuli within 15 cm. We also showed that turbidity may affect visual plant finding at 15 cm. Using available data from this and other previous studies involving chemical cues and other life history traits, we propose a testable conceptual model for how E. lecontei finds plants each year, especially while underwater. This model may also be used to explain plant finding by aquatic phytophagous insects in general.     

High phenolic content fails to deter mesograzer consumption of <Emphasis Type="Italic">Myriophyllum spicatum</Emphasis> (Eurasian watermilfoil) in New England

Eurasian watermilfoil (Myriophyllum spicatum) is often considered one of the most aggressive macrophyte invaders in freshwater habitats throughout the USA. However, conditions leading to successful milfoil invasions are not well understood. This study sought to illuminate the role of herbivores in determining milfoil invasion success via the potential mechanisms of enemy release and biotic resistance. We determined feeding preferences of three herbivores native to the northeastern United States and measured macrophyte phenolic content, which may act as an herbivore feeding deterrent. We found that phenolic content in milfoil was more than two times higher than in the most abundant native macrophytes at our study sites, consistent with enemy release. However, laboratory feeding experiments demonstrated that milfoil phenolics did not deter amphipod (Hyalella azteca), snail (Physella sp.), or weevil (Euhrychiopsis lecontei) herbivory. Furthermore, amphipod consumption rates in our study were an order of magnitude higher than amphipod consumption rates reported in milfoil’s native range, contrary to the predictions of enemy release. Amphipods and snails from habitats invaded by milfoil consumed similar quantities of both milfoil and the low-phenolic native plant Elodea canadensis. In contrast, weevils consumed milfoil but not E. canadensis in choice experiments. Amphipods collected from milfoil-free habitats also readily consumed milfoil, and they consumed 2.5 times more milfoil than E. canadensis in a choice feeding trial. These results suggest that high phenolic levels do not prevent native herbivores from consuming invasive milfoil. Instead, native generalist grazers like amphipods and snails may limit milfoil proliferation and provide a measure of biotic resistance.     

Glycolate Metabolism in Eurasian Watermilfoil (Myriophyllum spicatum)

The metabolism of glycolate by Eurasian watermilfoil (Myriophyllum spicatum L.), a submersed angiosperm, was studied by feeding radioactive glycolate and glyoxylate and by analysis of glycolate and glycolic acid oxidase. Evidence for operation of the glycolate pathway is given. Glycolic acid oxidase occurs at levels comparable to amounts in species showing photorespiration. This species has a high affinity for CO₂ and a possible mechanism for it is described.     

Enumeration and Characterization of Bacterial Colonists of a Submersed Aquatic Plant, Eurasian Watermilfoil (Myriophyllum spicatum L.)

A simple procedure for enumerating and grouping the bacterial colonists of Eurasian watermilfoil (Myriophyllum spicatum L.) is described. Colony characteristics of bacteria associated with M. spicatum were better defined and more stable on nutrient-poor, diluted nutrient broth agar than on high-nutrient media. Acinetobacter, Cytophaga, Flavobacterium, Moraxella, Pseudomonas and/or Alcaligenes, and Vibrio/Aeromonas spp., as well as two highly fastidious unidentified bacterial groups (gram-negative rods and gram-negative cocci), were associated with cultured watermilfoil during January, February, May, June, July, and August 1988. In Lake Wingra (Madison, Wis.), Micrococcus spp. and enterobacters were also associated with Eurasian watermilfoil during July, August, and October 1987.     

Influence of host log age and refuge from natural enemies on colonization and survival of Phoracantha semipunctata

The pine cone weevil, Pissodes validirostris Gyll. (Coleoptera: Curculionidae), attacks seed cones of most Eurasian pine species, except these of Swiss stone pine (Pinus cembra L.). Behavioural responses of adult weevils to cone volatile emissions of Swiss stone pine and to those of a common host, mountain pine (Pinus uncinata Ram.), were compared in an olfactometer. Weevils were significantly attracted by the volatile blend emitted by mountain pine, but Swiss stone pine volatiles elicited an inverse response, with most weevils moving in the opposite direction to the odour source. However, the majority of second instar weevil larvae that were extracted from mountain pine cones and transferred into Swiss stone pine cones were capable of developing to the adult stage. This suggests that Swiss stone pine cones do not contain strong feeding deterrents that could prevent larval development. The possible factors involved in the absence of colonization of Swiss stone pine cones by cone weevils are discussed.     

Host range of Ceutorhynchus assimilis (Coleoptera: Curculionidae), a candidate for biological control of Lepidium draba (Brassicaceae) in the USA

Ceutorhynchus assimilis has been selected as a potential biological control agent of Lepidium draba, which is a Eurasian invasive weed in North America. Preliminary studies indicated specificity of this weevil collected in southern France on L. draba. This result was in discord with the pest status of C. assimilis found in the literature. Host-specificity tests based both on field and laboratory experiments showed heterogeneity in the host spectrum of the weevils reared from different host-plants as determined by larval development. However, no distinguishable morphological differences could be visually detected between the populations feeding on different host-plants. All sampled populations of weevils were polyphagous as adults. Weevils reared from L. draba were specific to this plant for their complete larval development. Conversely, populations living on other wild and cultivated Brassicaceae species were not able to use L. draba as a host plant. Such differentiation is further highlighted by other biological aspects such as plant infestation rates, sex-ratio, duration of larval development, and differences in the timing of their life cycles. These results demonstrate that C. assimilis, an insect species formerly considered as a pest of Brassicaceae, is characterized by its host-range variability, with one population being potentially useful in the biological control of L. draba. Moreover, this example points to the need to test multiple populations of biological control agents in assessing risk.     

Effect of arbuscular mycorrhizal fungi (Glomus intraradices) on the oviposition of rice water weevil (Lissorhoptrus oryzophilus)

Root-feeding insects are important drivers in ecosystems, and links between aboveground oviposition preference and belowground larval performance have been suggested. The root-colonizing arbuscular mycorrhizal fungi (AMF) play a central role in plant nutrition and are known to change host quality for root-feeding insects. However, it is not known if and how AMF affect the aboveground oviposition of insects whose offspring feed on roots. According to the preference–performance hypothesis, insect herbivores oviposit on plants that will maximize offspring performance. In a greenhouse experiment with rice (Oryza sativa), we investigated the effects of AMF (Glomus intraradices) on aboveground oviposition of rice water weevil (Lissorhoptrus oryzophilus), the larvae of which feed belowground on the roots. Oviposition (i.e., the numbers of eggs laid by weevil females in leaf sheaths) was enhanced when the plants were colonized by AMF. However, the leaf area consumed by adult weevils was not affected. Although AMF reduced plant biomass, it increased nitrogen (N) and phosphorus concentrations in leaves and N in roots. The results suggest that rice water weevil females are able to discriminate plants for oviposition depending on their mycorrhizal status. The discrimination is probably related to AMF-mediated changes in plant quality, i.e., the females choose to oviposit more on plants with higher nutrient concentrations to potentially optimize offspring performance. AMF-mediated change in plant host choice for chewing insect oviposition is a novel aspect of below- and aboveground interactions.     

Effects of eutrophication and snails on Eurasian watermilfoil (Myriophyllum spicatum) invasion

Exotic species can invade and establish new habitats both as a result of their own traits, and as a result of the characteristics of the environment they invade. Here, we show that the abundance of the invasive submerged aquatic plant, Myriophyllum spicatum (Eurasian watermilfoil) is highly dependent on the conditions of the environment in a mesocosm experiment. M. spicatum is allelopathic towards epiphytic algae, and in the absence of algivorous snails, we found that the abundance of both algae and M. spicatum significantly increased with experimentally increased nutrient loading, while the abundance of native submerged macrophytes declined. However, when snails were present, snail biomass increased with increasing nutrient loading, and M. spicatum biomass was consistently low while native submerged macrophyte biomass was consistently high. Our results stress the importance of the interaction between species traits and environmental conditions when considering the invasiveness of certain exotic species and the invasibility of certain environments.     

Host Range of Mycoleptodiscus terrestris, a Microbial Herbicide Candidate for Eurasian Watermilfoil, Myriophyllum spicatum

A native strain of the fungal plant pathogen Mycoleptodiscus terrestris is capable of causing under experimental conditions necrotic shoot lesions and a generalized decline and disintegration of Eurasian watermilfoil (Myriophyllum spicatum), an exotic submerged aquatic weed in North America. The potential of this fungus to cause disease on nontarget plants was evaluated on 33 species and cultivars in 11 families. The nontarget selection, intended as a Tier I group, was biased toward probable suscepts consisting of submerged, floating, and emergent aquatic species and terrestrial crop plants. The plants were exposed to the fungal mycelium formulated in alginate beads. Pathogenicity rather than phytotoxicity was the primary mode of attack by the fungus. Of the 16 nontarget aquatic species tested, the fungus was pathogenic to Hydrilla verticillata (hydrilla), Myriophyllum aquaticum (parrotfeather), and Ceratophyllum demersum (coontail), but only in hydrilla did it cause plant mortality comparable to that in Eurasian watermilfoil. The remaining 13 submerged, floating, and emergent aquatic species were unaffected. Of the 17 terrestrial species screened, none was significantly affected by the fungus in germination studies, but postemergent disease symptoms developed on seedlings of 10 species. Four of the 10, Medicago sativa (alfalfa), Lotus corniculatus (birdsfoot trefoil), Trifolium hybridum (alyce clover), and T. repens (white clover), developed disease affecting 26-50% of their tissues. Thus, this host range testing scheme, based on the concept of screening plants under the maximum hazard potential, helped to identify susceptible species. Nonetheless, it exaggerated the nontarget risk due to the small number of host species tested. Screening a taxonomically diverse and larger selection of plants as well as testing under conditions of less severe exposure to the fungal inoculum are necessary to obtain a more realistic view of the host range than presently indicated.     

Impact of azadirachtin on vine weevil (Coleoptera: Curculionidae) reproduction

Abstract 1 The dose–response of azadirachtin on vine weevil, Otiorhynchus sulcatus (Fabricius), reproduction is investigated by confining adults to feed on treated Taxus × media leaves, and by counting and evaluating development in the resulting eggs. 2 A dosage‐dependent reduction in oviposition is discovered for foliar surface residues of azadirachtin, with an EC₅₀ of 25–50 parts per million (p.p.m) and 99.2% inhibition of viable egg production with 100 p.p.m. 3 Switching weevils from treated to untreated foliage allows reproductive capability to be restored for weevils that cease egg laying after azadirachtin exposure of 50 p.p.m. Weevils that had already started laying eggs in untreated groups soon cease oviposition once switched to azadirachtin‐treated foliage. 4 A transovarial effect results in a decrease in the percentage of viable eggs as the azadirachtin concentration increases. 5 The amount of feeding on foliage does not appreciably decrease at these hormonally effective concentrations, and adult weevil mortality is only slightly greater in the azadirachtin‐treated groups. Therefore, the overall effect of azadirachtin on weevil populations in the field is difficult to assess, except by collecting weevils to determine whether they are able to lay viable eggs.     

Geographic distribution and genotypic composition of invasive hybrid watermilfoil (<Emphasis Type="Italic">Myriophyllum spicatum</Emphasis> × <Emphasis Type="Italic">M. sibiricum</Emphasis>) populations in North America

The recent recognition of invasive hybrid watermilfoil (Myriophyllum spicatum × M. sibiricum) in North America has necessitated a more thorough evaluation of its overall distribution and occurrence in natural populations. A comprehensive survey of watermilfoil populations was conducted in five Minnesota lakes, three of which were suspected a priori to contain hybrid watermilfoil. DNA sequence data verified that hybrid plants between the nonindigenous M. spicatum L. and indigenous M. sibiricum Kom. occurred in three of the five lakes sampled. Myriophyllum spicatum was not detected in lakes where hybrids were prevalent. Further sampling of lakes in Idaho, Michigan, Minnesota, Wisconsin and Washington identified 30 additional hybrid watermilfoil populations. In only three of these populations the hybrid watermilfoil was found to co-occur with M. spicatum. To facilitate the field identification of the two parental species and their hybrid, morphological data from watermilfoil specimens collected across the United States were evaluated. We determined that leaf segment/leaf length measurements can effectively distinguish M. spicatum and M. sibiricum; however, hybrids are intermediate for these characters and such measurements frequently overlap with respect to their parental taxa. By incorporating a combined molecular and morphological approach to identifying watermilfoils, the hybrids can be identified readily and their distributions elucidated both within and between lakes. Because hybrids may respond differently to local ecological conditions than their parents, information on their presence and distribution should be of particular importance to management and conservation programs.     

Hybrid watermilfoil (Myriophyllum spicatum × Myriophyllum sibiricum) exhibits traits associated with greater invasiveness than its introduced and native parental taxa

Hybridization has been associated with increased invasiveness in plants. In North America, the hybrid aquatic plant Myriophyllum spicatum?×?Myriophyllum sibiricum (hybrid watermilfoil, hereafter HWM) is a cross between non-native invasive Eurasian watermilfoil (M. spicatum, EWM) and native northern watermilfoil (M. sibiricum, NWM). Lab-based trials have demonstrated higher growth rates in HWM compared to EWM and NWM, but these patterns have not been systematically examined in the field. In this study, we compared the invasiveness of HWM to its parental taxa, EWM and NWM, by examining the amount and timing of: (1) flowering, (2) surface cover, and (3) biomass (using stem counts as a proxy). We conducted repeat surveys of Myriophyllum beds at eight lakes (2–3 lakes/taxon) in the Minneapolis–St. Paul Metropolitan area (Minnesota, USA) between June 2017 and November 2018. HWM produced more flower spikes earlier and overall, and maintained consistently more flower spikes throughout the growing season than EWM and NWM. In addition, surface cover reached greater annual peaks and was higher for longer throughout the growing season for HWM than for both parental taxa. We did not observe a significant difference in stem counts among the three taxa, but HWM did reach a higher maximum number of stems than either parental taxon. This study provides field-based evidence of increased invasiveness associated with hybridization between EWM and NWM; specifically, greater reproductive potential via flowering and greater surface cover may increase HWM spread, have greater impacts on native species, and pose more of a nuisance to lake users.

     

Gas chromatographic determination of flurprimidol in a submersed aquatic plant (Myriophyllum spicatum), soil, and water

Methods for the extraction and quantification of flurprimidol residues in Eurasian watermilfoil (Myriophyllum spicatum), soil, and water are described. The compound was detected and quantified by gas chromatography (GC) with a thermionic specific detector. Its identity was confirmed by gas chromatography-mass spectrometry (GCMS) with detection at m/e 40–320. Recoveries from samples spiked with flurprimidol at 10–10,000 ng ml^–1 or g^–1 averaged 86.8% for Eurasian watermilfoil shoots, 85.2% for roots, 79.3% for loam soil, and 93.3% for water. In a small-scale experiment under field conditions, approximately 88% of the applied flurprimidol dissipated in 4 weeks. The majority of recovered flurprimidol was found in the water and upper 5 cm soil layer. The half-life of the compound in water was 6.8–8 days during June/July 1989.     

Effects of Rhinoncomimus latipes on the growth and reproduction of Persicaria perfoliata,an invasive plant in North America

Native to Asia, mile-a-minute Persicaria perfoliata, is an invasive weed in North America, and the weevil Rhinoncomimus latipes is a host-specific insect agent which occurs widely in China. We conducted a common garden experiment to compare P. perfoliata plant responses of native and invasive populations to herbivory by the weevils from different origins. We found weevils from Hunan, Hubei and Heilongjiang Provinces had strong, moderate and weak ability to suppress host plant, respectively. Weevils from Hunan and Hubei Provinces had stronger impact on the growth of both native and invasive plant populations than the weevil from Heilongjiang Province. The losses in seed output of invasive plants were also significantly greater than natives in the weevil treatments. Our results suggested that the weevil population from Hunan Province may be the most suitable for the control of mile-a-minute, while the population from Heilongjiang Province may be the least suitable due to climate matching.     

Overwintering conditions affect cold hardiness,survival, and post-overwintering fitness of the pea leaf weevil

Overwintering conditions affect the physiological state of ectotherms, and therefore, their cold hardiness and survival. A measure of the lethal and sublethal impacts of overwintering conditions on pest populations is crucial to predict population dynamics and to manage pests the following spring. The impact of winter conditions can be most intense for invasive insects undergoing range expansion. Insect herbivores can display plastic host use behaviours that depend on their body condition following winter. The pea leaf weevil, Sitona lineatus L. (Coleoptera: Curculionidae), is an invasive pest of field peas, Pisum sativum L., and faba bean, Vicia faba L. (Fabaceae). Pea leaf weevil has expanded its range in North America to include the Prairie Provinces of Canada. This study investigated the effects of temperature and microhabitat on overwintering survival and cold hardiness of pea leaf weevil in its expanded range. Further, we investigated the sublethal effect of overwintering temperature and duration on post-overwintering survival, feeding, and oviposition of pea leaf weevil. We also investigated the role of juvenile hormone in modulating body condition of overwintering weevils. The overwintering survival of pea leaf weevil adults increased with soil temperature and varied with region and microhabitat. More weevils survived winters when positioned near tree shelterbelts compared to open alfalfa fields. The supercooling point of pea leaf weevil varied throughout its expanding range but did not differ for weevils held in the two microhabitats. The average threshold lethal temperature of pea leaf weevil at all three sites was −9.4 °C. Weevils that overwintered for a longer duration and at a higher temperature subsequently fed more on faba bean foliage and laid more eggs compared to those which overwintered for a shorter duration at a lower temperature. Our findings highlight that warm winters would increase overwintering survival and post-overwintering fitness, facilitating further pea leaf weevil invasion northward in the Prairie Provinces of Canada.     

Photosynthesis in Eurasian Watermilfoil (Myriophyllum spicatum L.)

Gas exchange of Eurasian watermilfoil (Myriophyllum spicatum L.) indicated a near-zero CO₂ compensation point and a high temperature optimum for photosynthesis. These properties are characteristic of plants fixing CO₂ by a β-carboxylation mechanism. Operation of the Calvin cycle was shown and no evidence for β-carboxylation was obtained. These results indicate that near-zero CO₂ compensation points are not dependent on a β-carboxylation mechanism.