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Annals of the Entomological Society of America, 111(4), 2018, 144–153doi: 10.1093/aesa/say007

Review Special Collection: Pulse Crop Insect Pests and Their Management Strategies

Progress Toward Integrated Pest Management of Pea Leaf Weevil: A ReviewHéctor A. Cárcamo,1,5 Meghan A. Vankosky,2 Asha Wijerathna,3 Owen O. Olfert,2 Scott B. Meers,4 and Maya L. Evenden3

1Lethbridge Research and Development Centre, Agriculture and Agri-Food Canada, Lethbridge, AB, Canada, 2Saskatoon Research and Development Centre, Agriculture and Agri-Food Canada, Saskatoon, SK, Canada, 3Department of Biological Sciences, University of Alberta, Edmonton, AB, Canada, 4Southern Crop Development Centre, Alberta Agriculture and Forestry, Brooks, AB, Canada, and 5Corresponding author, e-mail: hector.cárcamo@agr.gc.ca

Subject Editor: Gadi V. P. Reddy

Received 12 December 2017; Editorial decision 22 February 2018

Abstract

The pea leaf weevil, Sitona lineatus (L.; Coleoptera: Curculionidae), is a significant pest of field peas (Pisum sativum L.) and faba bean (Vicia faba L.) in most temperate regions. Considerable research progress has been made towards understanding its basic life cycle, including flight patterns, plant host interactions, and geographic distribution throughout its native and invasive ranges in Europe and North America, respectively. Management tactics investigated include chemical insecticides and tillage, but less work has been done on biological control, host plant resistance, intercropping and trap crops. Future research should focus on better integration of tactics that utilize an ecostacking approach to maximize diversity at various scales to mitigate risks from insect pests and subsequently reduce the need for chemical interventions.

Key words: Sitona lineatus, field peas, faba bean, pulse crop entomology

Pulse crops such as field pea (Pisum sativum L.) (Fabales: Fabaceae) and

faba bean (Vicia faba L.) (Fabales: Fabaceae) are significant sources

of protein for humans and livestock worldwide (FAO 2017). Over 12

million metric tons of field peas (Government of Saskatchewan 2017)

and 2 million tons of faba beans (Pulse Canada 2017) are produced

annually in temperate countries. In addition to the financial value

to producers and local economies, pulse crops are valuable rotation

crops because they fix nitrogen from the air through symbiotic asso-

ciations with Rhizobium (Rhizobiales: Rhizobiaceae) bacteria (Vance

2001). Nitrogen fixation results in reduced input costs, less environ-

mental pollution from nitrates leaching through the soil and improved

soil fertility for future crops (Lupwayi and Soon 2016). A number of

biotic factors, however, can threaten successful pulse crop production.

These include diseases, weeds and insect pests that reduce yields and

pulse crop profitability. Among these, Sitona lineatus (L.; Coleoptera:

Curculionidae) is a key insect pest of field peas and faba beans because

the larvae feed on Rhizobium root nodules. The objective of this review

is to provide a summary of the distribution and biology of S. lineatus,

highlight recent advances towards its integrated pest management, and

identify knowledge gaps and directions for future research.

Distribution

S.  lineatus (Fig.  1) is native to Europe and North Africa where it is a well-known pest of field peas and faba beans. Its current dis-tribution and recent expansion in western North America (Fig. 2a) were reviewed in detail by Vankosky et al. (2009). Olfert et al. (2012) developed bioclimatic simulation models, (ecological niche mod-els), to predict the potential range and relative abundance of S. lin-eatus populations in Canada. Bioclimatic simulation tools, such as CLIMEX, predict the potential geographic distribution and establish-ment of insects in ecosystems, based on climate (Kriticos et al. 2015). CLIMEX derives an ecoclimatic index (EI) that gives an overall gauge (ranging from 0 to 100) of the ecological suitability of a geographic location for successful establishment, survival and reproduction of a target species. The climatic prerequisites of a target species are inferred from its known geographical distribution, relative popu-lation abundance and phenology. Model parameters include tem-perature, light, moisture, heat stress, cold stress, moisture stress, and diapause biology of the target insect. Additional data requirements can also be obtained from laboratory studies to further fine tune the ecological parameters. The EI provides an estimate of relative popu-lation abundance. The accuracy of these estimates depends on the use

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of appropriate growth rates for the study organism and weather data that are site and time specific (Legaspi and Legaspi 2010).

Olfert et al. (2012) sought to identify areas in Canada at risk for future establishment of S. lineatus, and to use the model to develop a better understanding of how a changing climate might potentially influence its range expansion across North America. Climex output predicted that its potential range could extend well beyond current distributions along the western and eastern seaboards in North America. At the time of the study in 2012, areas of Canadian pulse production included Quebec and Ontario in eastern Canada, and the three Prairie Provinces (Manitoba, Saskatchewan, and Alberta) (Pulse Canada 2017). Sensitivity analyses measured how the suitabil-ity index (EI) responded to changes in temperature and precipitation. Model output indicated that S. lineatus populations were more sensi-tive to changes in precipitation than temperature (Olfert et al. 2012).

The study also assessed the potential impacts of a changing climate on S.  lineatus range expansion. A number of studies have predicted that changes in relative abundance, phenology and distribution may occur as a result of climate change (Olfert et al. 2017). When climate change projections (General Circulation Models) were applied to the bioclimatic model of S. lineatus, the output predicted a significant shift northward (Olfert et al. 2012). There was also a predicted increase in the geographic area designated as ‘favorable’ (EI > 20) to S. lineatus. Compared to the current climate, model output indicated that the area of the continent that will have EI > 20 could potentially increase by 33 to 76% under climate change scenarios. In an effort to provide advanced warnings of continued range expansion, a monitoring program was initiated across western Canada in 2012 (Western Committee on Crop Pests 2011). Since that date, populations of S. lineatus have continued to expand north as far as the Peace Region of Alberta and into east-ern Saskatchewan near the border with Manitoba in Canada (Prairie Pest Monitoring Network 2017) and in North Dakota, United States (https://www.ag.ndsu.edu/news/newsreleases/2017/july-10–2017/pea-leaf-weevil-detected-in-western-n-d) (Fig. 2a).

Biology

The life cycle of S. lineatus was studied in detail by Jackson (1920) and reviewed by Vankosky et al. (2009). S. lineatus has one genera-tion per year and adults spend the winter in a state of quiescence in field margins or forage fields (e.g., alfalfa) where they may feed and continue to develop slowly depending on temperature (Schotzko and O’Keeffe 1986). In the spring, adults fly when temperatures reach

12.5°C (Hamon et al. 1987). Pheromones and plant volatiles play an important role in mate and host finding (St. Onge et al. 2018) and are discussed in detail elsewhere in this issue (Evenden 2018). At emergence in the spring, adults are oligophagous on several Fabacea (Nielsen et al. 1993, Landon et al. 1995), but later during its reproduc-tive phase it has a clear preference for peas (Landon et al. 1995) and faba bean (Nielsen et  al. 1993). Under optimum laboratory condi-tions, females can produce a maximum of 3,299 and 855 eggs, when fed pea and alfalfa foliage, respectively (Schotzko and O’Keeffe 1986). The average rates of egg laying were around 10 and three eggs per day for weevils collected in May and fed peas and alfalfa, respectively (Schotzko and O’Keeffe 1986). The eggs are scattered on the ground or laid in crevices near the base of seedlings (Jackson 1920). Larvae develop through five instars and feed on Rhizobium nodules (Hamon et al. 1984, Jensen et al. 1989). Intraspecific competition for nodules is hypothesized as the primary mortality factor of S. lineatus feeding on V. faba (Nielsen 1990) and peas (Vankosky et al. 2011a), but the details of the interactions are unknown. Upon maturity, larvae pupate in the soil and the adults emerge to search for legume hosts to con-tinue feeding. In southern Canada, teneral adults start emerging in late July (Cárcamo and Vankosky 2011). At this time, they are oligopha-gous and will feed on a variety of Fabaceae until late in the summer when they fly to perennial leguminous crops such as alfalfa or to field margins to overwinter (Schotzko and O’Keeffe 1986).

Host Plants, Adult and Larval Damage

Peas and faba bean are the preferred reproductive hosts of S.  lin-eatus (Landon et  al. 1995), but egg laying has also been reported for females fed alfalfa (Schotzko and O’Keeffe 1986). During the non-reproductive phases of their life cycle they feed on several other Fabacea species (Jackson 1920, Fisher and O’keeffe 1979, Hamon et al. 1987, Greib and Klingauf 1976). Larval development in rela-tion to plant hosts has not been studied rigorously. Because adults maximize egg laying on faba beans and peas, there is an assump-tion that larvae require these hosts to reach maturity. Adult S. lin-eatus are considered pests of field vetch (Vicia sativa L.) (Fabales: Fabaceae) (Nikolova 2016) and lupins (Cantot and Papineau 1983, Ferguson 1994) in Europe. Only Ferguson (1994) reported that lar-vae were not found in the roots of lupins. Host plants influence wee-vil longevity; weevils collected from faba bean cultivars live longer than those collected from peas (Jaworska 1998). Adult weevils, how-ever, feed less (leaf area) on faba beans compared to peas when pre-sented with a choice of excised leaf tissues (Jaworska 1998).

Adult S. lineatus feed on above ground foliage creating character-istic ‘U’ shape notches along the leaf margins (Jackson 1920). Rarely, adult damage can destroy young shoots during a severe infestation (Havlickova 1982, Williams et al. 1995). Pea and faba bean have a symbiotic relationship with the nitrogen fixing bacterium, R. legumi-nosarum biovar viciae associated with the root nodules. S.  lineatus larvae feed on the nitrogen fixing bacteria within root nodules and, therefore, reduce the nitrogen availability for the plant (Cárcamo et al. 2015). Larva damage nodules of all stages of the legume plants, how-ever, damage is highest at the flowering stage (Jackson 1920) when nodulation and larval populations peak. The damage is more promin-ent on the main roots compared to lateral roots (Verkleij et al. 1992), but can completely destroy the nodules under a severe infestation (Jackson 1920, Cantot 1986). Larval densities can reach up to 5,000 per m2 in field plots in southern Alberta and destroy 90% of nodules (Cárcamo and Vankosky 2011). Under greenhouse conditions larvae destroyed 40–98% of the nodules (El-Dessouki 1971, Verkleij et al. 1992) and reduced the number of older nodules (Cárcamo et al. 2015).

Fig.  1. Dorsal habitus of Sitona lineatus illustrating the characteristic light and dark stripes extending from the thorax to the elytra. Image by Michael Dolinski.

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Larval damage can affect plant yield (Hunter 2001, Corre-Hellou and Crozat 2005). Plants infested with 100 S. lineatus eggs lost 27% of the yield compared to un-infested plants (El-Dessouki 1971). Further, root nodule damage can increase the plant susceptibility to secondary infections (Hunter 2001), reduce the nitrogen con-tent of the seeds and lower the nitrogen input to the soil (Doré and Meynard 1995, Corre-Hellou and Crozat 2005). In a greenhouse study, presence of larvae reduced the soil nitrogen availability for plants and plant nitrogen content at the early flower stage (Cárcamo et  al. 2015). The relative yield effects of adult foliage damage is believed to be much smaller than the effect of nodule damage by larvae, but this remains to be quantified.

Monitoring

Monitoring tools are a necessary part of pest management of S. linea-tus in agroecosystems where populations are established (Vankosky et al. 2009) and in areas of active range expansion (St. Onge et al. 2018). Adults are the most mobile and accessible life stage to tar-get for direct monitoring. Although S. lineatus is univoltine (Jackson 1920), predictable adult movement occurs three times per year when the weevils are in different physiological states (Schotzko and O’Keeffe 1986). Monitoring adult activity can take place when wee-vils are leaving overwintering sites (Nielsen and Jensen 1993, Biddle et al. 1996) in a reproductively immature state (Hamon et al. 1987) in early spring. Adult monitoring is also possible after the spring

Fig. 2. (a) Invasion chronology of Sitona lineatus in western North America. (1) 1930s: British Columbia, Canada and Pacific North West of the United States, (2) 1990s: Alberta; (3) 2000s: Saskatchewan; (4) 2016: North Dakota. For references, refer to the text. (b) Distribution of S. lineatus in the Prairie Provinces of western Canada as of 2017. The color scale ranges from little foliar damage (green = 0–1 notches per plant) to high levels of foliar damage of greater than 27 notches per plant (red).

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migratory flight within pea of faba bean fields when weevils are mat-ing and laying eggs (Nielsen and Jensen 1993). Monitoring efforts could also target the movement of newly emerged weevils away from senesced or harvested host plants toward perennial legumes in late summer or fall when weevils are reproductively immature (Fisher and O’Keeffe 1979, Hamon et  al. 1987, Evenden et  al. 2016, St. Onge et  al. 2018). Direct assessment of weevil activity requires a method to capture and count weevils as they move between habi-tats. Most research has focused on traps to either passively capture or actively attract S.  lineatus during the spring. In addition, there is some research on the development of monitoring tools to target newly emerged weevils in the late summer and fall (Hanavan et al. 2008, St. Onge et al. 2018).

To develop an effective trapping system, it is important to under-stand how S.  lineatus move through the environment throughout the season. Adult weevils move away from overwintering sites in a synchronous manner (Schotzko and O’Keeffe 1986) in early spring when ambient temperatures are above the flight threshold of 12.5°C (Hamon et al. 1987) regardless of whether their reproductive hosts have germinated. If weevils do not find peas or faba beans the first time, they will fly a second time to find one  of these hosts (Fisher and O’Keeffe 1979, Nielsen and Jensen 1993). Initial migratory flights in the spring occur downwind at heights well above the crop in the boundary layer 7–10 m above the ground (Hamon et al. 1987). At peak spring flight, unidirectional yellow traps positioned near pea fields high above the ground (152 and 183 cm) capture more weevils than low traps positioned 61–122 cm above the ground (Fisher and O’Keefe 1979). Once weevils locate fields of pea or faba bean, their flight muscles degenerate (Schotzko and O’Keeffe 1986) and they dis-perse within the crop mainly by walking (Hamon et al. 1987). Traps positioned at crop height do not efficiently capture weevils within pea and faba bean fields throughout the spring activity period (Hamon et  al. 1987, Glinwood et  al. 1993) unless weevil density is high (Nielsen and Jensen 1993). Ground-based traps including pitfall traps and modified Leggett traps (Leggett et al. 1975) capture S. lineatus as they walk within pea (Quinn et al. 1999, Evenden et al. 2016, St. Onge et al. 2018) and bean (Blight and Wadhams 1987) fields in the spring.

At the end of summer, newly emerged S.  lineatus move out of pea and bean fields when annual legume crops senesce or are har-vested (Fisher and O’Keeffe 1979, Hamon et  al. 1987). Although newly emerged weevils can fly, they have smaller wing muscles than overwintered weevils (Schotzko and O’Keeffe 1986) and they dis-perse both by walking (Hamon et al. 1987) and flying (Fisher and O’Keeffe 1979) to find perennial legumes for feeding and overwin-tering. Although unbaited sticky traps capture dispersing weevils at up to 183 cm above the ground in the fall (Fisher and O’Keeffe 1979), pheromone-baited traps only capture S. lineatus when posi-tioned on the ground during the fall activity period (St. Onge et al. 2018). The activity period of newly emerged weevils is longer than the spring migration and weevil capture is higher in late summer and fall than during the spring (Fisher and O’Keeffe 1979).

The identification of a male-produced aggregation pheromone of S. lineatus, 4-methyl-3,5-heptanedione (Blight et al. 1984), allowed for the development of a monitoring trap baited with a synthetic version of the pheromone (Blight et al. 1991, Glinwood et al. 1993). Pheromone lures were first deployed in modified Leggett traps to monitor weevils during the spring in the United Kingdom (Glinwood et al. 1993, Biddle et al. 1996), Denmark (Nielsen and Jensen 1993) and the United States (Quinn et al. 1999). Pheromone-baited traps capture more adult weevils than unbaited traps (Blight et al. 1991, Quinn et al. 1999), but inter-trap variation at a single site is large and multiple traps per site are recommended (Biddle et  al. 1996).

Although adults are only active during the day (Hamon et al. 1987), visual cues provided by differently colored modified Legget traps do not influence weevil capture in pheromone-baited traps (Glinwood et  al. 1993). The utility of monitoring S.  lineatus in pheromone-baited traps in the spring may be limited to timing agronomic activi-ties such as planting and insecticide application, as the number of weevils captured does not reflect seedling damage near the traps or throughout the field (Biddle et al. 1996, Quinn et al. 1999).

Recent studies tested the attractiveness of pheromone-baited traps to attract and retain weevils during the migration away from pea fields in the late summer and fall (Evenden et al. 2016, St. Onge et  al. 2018). Although newly emerged male weevils do not prod-uce aggregation pheromone, the antennae of newly emerged males and females respond electrophysiologically to pheromone (Blight et  al. 1991). Pheromone-baited pitfall traps attract more weevils than unbaited traps in the fall and this response can be enhanced by the addition of synthetic host plant volatiles to the pheromone lure (Evenden et al. 2016, St. Onge et al. 2018). Assessment of pre-overwintering weevil populations using pheromone-baited traps in the fall could aid producers with pest management decisions such as whether to plant insecticide-treated seed the following spring (St. Onge et al. 2018).

In western Canada (Alberta and Saskatchewan) a survey is car-ried out every year in late May through early June to determine the geographic distribution of S.  lineatus. Maximum damage occurs at this time when peas are in the critical growth stage before the sixth node. Within the known range of S. lineatus in Alberta, Canada, five fields are surveyed in each Alberta municipality. In areas outside the known range of the S.  lineatus three fields are surveyed per muni-cipality. As range expansion of the weevil is documented, the area surveyed expands the following year. Damage is assessed in five loca-tions in each field. The first location is 10 meters from the access point to the field to avoid areas with poor growth associated with compacted soils. The other samples are 25 m apart and within 2 m of the field margin. At each location, the number of crescent-shaped feeding notches are counted on each node of the 10 plants selected. The legal location and GPS coordinates are recorded for each field. Where possible, farmer name, seeding date and variety are recorded. The results are mapped using ArcGIS software and a color-contoured provincial map (Fig. 2b) is published using the following scales: green (0–1 notches/plant), yellow (2–3), light orange (4–9), dark orange (10–27), red (>27). The maps are available on the provincial agri-cultural department web sites where producers and agronomists can consult them to make decisions about relative regional annual risks of S. lineatus damage to field peas or faba beans (Brook and Cutts 2017, Saskatchewan Ministry of Agriculture 2017).

S.  lineatus sampling to make control decisions in the Canadian Prairies is currently based on plant damage of the spring crop rather than weevil population densities. Adult weevils have the habit of falling to the ground where they blend with the plant residue mak-ing them difficult to count. Despite these challenges, Antonelli et al. (1985) recommended a nominal threshold of 0.3 to 1 weevil per seed-ling of peas in Washington, United States. Sweep net catches of 1–3 adults per sweep have also been recommended (Quisenberry et  al. 2000), even though pea seedlings are often too short for this tech-nique to be accurate. A more practical action threshold was suggested earlier by El-Lafi (1977). In northern Idaho, populations of about 0.5 weevils per seedling resulted in more than 30% of seedlings hav-ing defoliation on the terminal leaflet and a yield reduction (El-Lafi 1977). Thus, he recommended an action threshold of 30% of seed-lings with terminal leaf damage during the second and third node stages. The sampling method in El-Lafi’s study relied on counting the

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number of seedlings with and without damage in a quadrant of 0.84 m2. In France where the weevil is a native pest, a semi-quantitative damage scale based on degree of leaf notching has been developed (Cantot 1986). The scale consists of four levels (0–3) with 0 being the lowest damage and 3 representing severe damage of 15 or more notches on the foliage in the first node. Severe levels of defoliation resulted in populations of about 12 larvae per plant and destruction of 90% of Rhizobium nodules (Cantot 1986). In southern Alberta, Canada, Cárcamo, Vankosky and colleagues conducted a number of studies with field peas to validate insect–plant interactions and action thresholds from the United States and Europe (Cárcamo and Vankosky 2011, Vankosky et al. 2011a,b). In caged trials they reported significant relationships between the proportion of seedlings with terminal leaf damage and total nodulation or nodule damage depending on the sites (Vankosky et  al. 2011a), which were simi-lar to Cantot’s results (1986). Using plots with various inputs they also noted a significant, albeit weak, negative regression of yield on seedling defoliation expressed as proportion of plants with terminal leaf damage (Vankosky et al. 2011b). Using an aggregated analysis of the plots studied in southern Alberta across years (excluding outliers) these authors were able to confirm that plots with more than 30% of seedlings with damage had lower yield than plots with less than 30% damage (Cárcamo and Vankosky 2011).

Pest Management

The Role of NitrogenNitrogen soil content has a pivotal role in determining the pest sta-tus of S. lineatus. Adding enough nitrogen to the soil at planting to meet plant requirements results in reduced nodulation (Vankosky et al. 2011a), thereby decreasing larval food resources, which in turns reduces weevil recruitment (Cárcamo et al. 2015). Furthermore, nitro-gen input can replace insecticide as a management tool, though likely not economical because its cost would exceed that of the insecticide application. In a field plot study, Vankosky et  al. (2011b) showed higher yields for peas in plots that received nitrogen amendment compared to those with thiamethoxam seed treatment, although the results were significant only in one of the three study years. In a related cage study, S.  lineatus reduced yield by 17% in treatments without nitrogen inputs and only by 3% when urea nitrogen was added at planting (Cárcamo and Vankosky 2011). This means that for organic farmers, adding manure may be a nonchemical tool for yield loss miti-gation. Research is needed to separate the direct effects of nitrogen on plant yield and indirect nitrogen effects on weevil populations expected from the reduction in plant nodules.

The interaction of S.  lineatus with nitrogen-fixing legumes may have multi-year residual fertilizer impacts on future crops in the rota-tion. In a study conducted in northern Alberta, barley and wheat yields (but not canola) in plots preceded by field pea or faba bean 3 yr earlier were higher than those in plots preceded by barley (Lupwayi and Soon 2016). These authors also found evidence that the main pathway of nitrogen transfer from legume residues to future crops was belowground rather than above ground. In general, S. lineatus larval damage to nodules affects plant and soil nitrogen (Corre-Hellou and Crozat 2005, Lohaus and Vidal 2010, Cárcamo et al. 2015). Thus, the residual nitrogen fertility advantage of legumes in crop rotations could be compromised due to weevil feeding. This hypothesis remains to be tested in a long-term (4 yr minimum) field crop rotation study.

Chemical InsecticidesAll major insecticide chemistries have been evaluated for manage-ment of S.  lineatus populations since the 1980s (summarized in

Vankosky et  al. 2009). Foliar insecticide active ingredients that have been evaluated include phorate (King 1981, Bardner et  al. 1983), cyhalothrin-lambda (also known as lambda-cyhalothrin; Steene et al. 1999), permethrin (McEwan et al. 1981, Bardner et al. 1983, Griffiths et al. 1986), and imidacloprid (Steene et al. 1999). Cyhalothrin-lambda is registered in several jurisdictions in North America and also in Europe (Seidenglanz et al. 2010). Cyhalothrin-lambda is currently undergoing re-evaluation in Canada, and its availability in the future is contingent on the results of that process (Government of Canada 2017). Several other compounds such as carbaryl, cyfluthrin, phosmet, cypermethrin, are available depending on the jurisdiction. For example, in North Dakota as of 2017 the list included over 10 active ingredients or mixtures (Knodel et al. 2017).

Foliar insecticides can reduce adult weevil populations and foliar damage, but may not protect yields (Vankosky et al. 2009). Cyhalothrin-lambda treatment reduced adult weevils by 56% (Steene et al. 1999). Application of permethrin (pyrethroid insecti-cide) decreased larval populations by approximately 50% (Bardner et  al. 1983), likely due to mortality of adult females, as contact foliar insecticides have no direct impacts on eggs or larvae (Steene et al. 1999). Some products have improved yields only slightly. For example, plots treated with permethrin yielded 2.4% more than untreated plots (Bardner et al. 1983). Properly timing the applica-tion of foliar insecticides is difficult, as they must be applied imme-diately following the detection of weevil invasion to prevent adult females from laying eggs in the host crop (King 1981, Bardner et al. 1983, Ester and Jeuring 1992). To ensure adequate plant protection, multiple foliar applications may be required over the course of the dispersal period of S. lineatus, depending on the residual time of the insecticide product and rainfall events. For these reasons, producers generally favor the use of systemic insecticides for management of this pest. The efficacy of cyhalothrin-lambda against S.  lineatus is currently being evaluated in Saskatchewan (M.A. Vankosky, unpub-lished data). Preliminary results indicate that foliar application of cyhalothrin-lambda does not result in significant yield gains com-pared to the untreated control (M.A. Vankosky, unpublished data).

Seed coating with systemic insecticides for S.  lineatus manage-ment in field peas has been studied in some detail. There is consensus that systemic insecticides are more effective than foliar applications (Vankosky et  al. 2009, Seidenglaz et  al. 2010). Many of the seed treatments such as carbofuran or related compounds, effective in Europe 30 yr ago are no longer available in most jurisdictions. Over the last two decades, these compounds were replaced by neonico-tinoids, which in turn have been restricted in some jurisdictions or phased out. In western Canada and the United States, for now, neo-nicotinoids are still used in field peas and its mechanism of crop protection is well known at least for thiamethoxam (Cárcamo et al. 2012). This chemical only kills around 30% of the adults, but there is a significant reduction in adult feeding damage (50%), less ovi-position by survivors, and only about half of the larvae survive in plants grown from seeds coated with this chemical (Cárcamo et al. 2012). The authors cautioned that under situations of high weevil outbreaks the surviving larvae still cause damage to reduce yields of peas and this may explain the inconsistent yield protection observed in some studies (e.g., Vankosky et al. 2011b). Current studies with faba bean in western Canada appear to show better yield responses to thiamethoxam than past studies with peas (Wijerathna, Cárcamo, Reid, Tidemann and Evenden, unpublished data).

Biological ControlBiological control agents of S.  lineatus include parasitoids, preda-tors, entomopathogenic fungi, and entomopathogenic nematodes

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(Table 1; reviewed by Vankosky et al. 2009, Cárcamo and Vankosky 2013). None of the biological control agents identified to date are specialists of S. lineatus. A few species of parasitoid attacking S. linea-tus in its native range have been released in North America for man-agement of other Sitona spp. and other weevil species [e.g., Hypera postica (Gyllenhal) Coleoptera: Curculionidae]; however, their estab-lishment was variable (Loan 1971, Loan 1975). The most promis-ing was Anaphes diana (Girault; Hymenoptera: Mymaridae), an egg parasitoid of Sitona weevils that established in the eastern United States (Dysart 1990). No parasitoids attacking S.  lineatus have yet been found in Alberta where the pest has been present since at least 1997 (Vankosky et al. 2009). There is no biological control program for any Sitona species, in Canada (Cárcamo and Vankosky 2013).

The impact of generalist predators on S. lineatus populations is not well documented. Laboratory experiments have shown that the large, adventive ground beetle, Pterosticus melanarius (Illiger; Coleoptera: Carabidae) consumes S.  lineatus adults (Hanavan 2008), and that the small and widespread species Bembidion quadrimaculatum (L.; Coleoptera: Carabidae) consumes its eggs (Vankosky et al. 2011c). Experiments are needed to quantify the impact of these species in field or semi-field conditions. In addition, a more comprehensive survey of generalist predators found in field pea or faba bean fields is needed to identify the full range of predators that contribute to S. lineatus mor-tality. Finally, the efficacy of entomopathogenic fungi and nematodes needs to be evaluated more thoroughly in North America, as these biocontrol agents could be important sources of S. lineatus mortality in integrated pest management programs. Currently there are no field examples where nematodes are used to manage S. lineatus.

Cultural ControlA number of cultural control options for S. lineatus management have been investigated. Crop rotation is traditionally used as a key com-ponent of cultural control of insect pests (Yates 1954, Bullock 1992). However, S. lineatus adults are highly mobile during their dispersal periods in spring and fall, such that considerable distance between fields of the primary host would be required between seasons for this

method to be effective (Vankosky et al. 2009). Irrigation can reduce populations of S.  lineatus larvae, leading McEwan et al. (1981) to conclude that larvae are intolerant to consistently wet soils.

The impacts of conservation tillage and no-till practices on S. lin-eatus colonization, larval populations, and subsequent adult popula-tions have recently been investigated in the Pacific Northwest of the United States. Conventional tillage plots were prepared for planting by plowing and harrowing, resulting in almost complete incorporation of crop residues into the soil (Hanavan et al. 2008, 2010; Hanavan and Bosque-Perez 2017). No-till plots were direct seeded (Hanavan et al. 2008, 2010; Hanavan and Bosque-Pérez 2017), which leaves over 60% of the soil undisturbed (Veseth 1999), and crop residues intact. Number of adult S. lineatus moving into emerging spring pea crops, measured using flight traps and pitfall traps, was greater in conven-tional till plots than no-till plots (Hanavan et al. 2008, 2010; Hanavan and Bosque-Pérez 2017). This resulted in earlier foliar damage to seed-lings emerging from conventional till plots than those from reduced till plots (Hanavan et al. 2008). Larval population densities and subse-quent new generation adult emergence were also lower in no-till than in conventional till plots (Hanavan et al. 2010). For example, Hanavan et al. (2010) observed that 18 adults m−2 colonized conventional till plots and 32 adults m−2 emerged from the same plots. In contrast, 16 adults m−2 colonized no-till plots and only 13 adults m−2 emerged from those plots (Hanavan et al. 2010). The impacts of conservation and no-till practices were also observed using the same measurement techniques in large-scale field pea production systems in the Pacific Northwest (Hanavan and Bosque-Pérez 2012). Hatten et al. (2010) also reported similar plot experiments, with similar results.

Dispersal and reproduction of S.  lineatus in conventional and no-till field pea plots was likely influenced by a combination of fac-tors. Seedling emergence in no-till plots was delayed relative to con-ventional till plots, by about 4 d on average (Hanavan et al. 2008). When seedlings emerged in no-till plots they were hidden by the resi-dues from the previous crop, and were less apparent that seedlings in conventional till plots for about 3 wk (Hanavan et al. 2008). Both of these factors likely impacted dispersal activity into these plots or

Table 1. Natural enemies of Sitona lineatus reported from its native range (Europe/North Africa) and its invasive range (North America)

Taxa Species References

Hymenoptera: Braconidae Allurus muricatus (Haliday) Loan 1971, 1975Microctonus aethiopoides (Loan) Aeschlimann 1980Perilitus rutilus (Nees) Aeschlimann 1980Pygostolus falcatus (Nees) Aeschlimann 1980

Hymenoptera: Mymaridae Anaphes diana Girault Aeschlimann 1980(=Patasson) A. lameerei (Debauche) Dysart 1990

Coleoptera: Carabidae Pterostichus madidus (Fabricius) Hamon et al. 1990Pterostichus melanarius (Illiger) Hamon et al. 1990

Hanavan 2008Pterostichus cupreus (L.) Ropek and Jaworska 1994Bembidion properans (Stephens) Ropek and Jaworska 1994Bembidion quadrimaculatum (L.) Vankosky et al. 2011

Entomopathogenic Fungi Beauveria bassiana (Vuilleman) Poprawski et al. 1985Müller-Kögler and Stein 1970

Metarhizium flavoviride (Metschn.) Poprawski et al. 1985Metarhizium anisopliae (Metschn.) Poprawski et al. 1985

Verkleij et al. 1992Paecilomyces farinosus (Holmsk.) Poprawski et al. 1985Paecilomyces fumosoroseus (Wize) Poprawski et al. 1985

Entomopathogenic Nematodes Steinernema carpocapsae (Weiser) Jaworska 1998Steinernema feltiae (Filipjev) Jaworska 1998Heterorhabditis bacteriophora (Poinar) Wiech and Jaworska 1990

Jaworska 1998

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fields (Hanavan et al. 2008, 2010; Hanavan and Bosque-Pérez 2012, 2017). The mean number of root nodules found on field pea roots also differed between tillage treatments, with plants harvested from conventional till plots having more nodules than plants harvested from no-till plots (Hanavan et al. 2010). Therefore, plants in no-till plots would support less larval development, and subsequently, the emergence of fewer new generation adults than in conventional till plots (Hanavan et al. 2010). This is likely to reduce overall regional populations in the long term. In the southern prairies of Canada where the majority of fields are no-till, seeding date is a more rele-vant risk factor than tillage regime.

Planting the host crops of S. lineatus later in the spring has effects similar to planting in no-till plots. For example, Hanavan and Bosque-Pérez (2017) observed that delaying seeding by at least 9 d led to emergence of seedlings after the period of peak weevil dispersal and to less foliar damage to late seeded plants. These results are similar to those observed by Doré and Meynard (1995) in France. Delayed seeding of field pea may not be an appropriate option for S. lineatus management in areas with short growing seasons (Teetes 1981).

Agronomic practices that enhance plant stand health may help to mitigate the damaging effects of S.  lineatus. Seedlings are most sus-ceptible to S. lineatus damage when they are first emerging (Williams et al. 1998). Actions that hasten seedling development (e.g., fertiliza-tion, planting in conventional till soils that are warmer and increase growth rates; Doré and Meynard 1995), or that affect the synchrony of seedling emergence with S.  lineatus dispersal (e.g., soil residues, no-till, delayed seeding date; Schotzko and Quisenberry 1999) may all help protect seedlings from S.  lineatus. In field plot experiments conducted in Lethbridge and Vauxhall, Alberta, Canada, inocula-tion of field pea seedlings with Rhizobium leguminosarum bacteria increased root nodulation, root biomass, foliar biomass, and subse-quent plant yield (Vankosky et  al. 2011b). Inoculation of field pea seeds and application of thiamethoxam seed treatments had a syn-ergistic effect on root nodulation, such that these plants had more root nodules than plants treated with only one product (Vankosky et  al. 2011b). Plants with more root nodules may be able to with-stand more below-ground feeding damage by S. lineatus larvae before yield loss is recorded by increasing the carrying capacity of host plants (McEwan et al. 1981, Vankosky et al. 2011a). If intraspecific compe-tition limits larval survivorship, additional nodules may simply feed a larger population of weevil larvae and contribute to S. lineatus popu-lation growth. For example, Hanavan et  al. (2010) observed lower adult weevil recruitment from no-till plots in which plants had fewer root nodules compared to conventional till plots in which plants had more root nodules. The effects of tillage regime and nodule number have to be teased apart to determine which factor plays a larger role in reducing adult weevil recruitment. In faba bean, higher larval popu-lations and a greater yield response to seed coating with thiameth-oxam relative to field peas has been observed (Wijerathna, Cárcamo, Evenden, Tidemann and Reid, unpublished data), which may support this hypothesis.

Trap cropping is a management strategy with potential to reduce S. lineatus damage in pulse crops. Only one published study was found on the use of trap crops for this pest, though the concept has been tested successfully in several temperate systems (Hokkanen 1991). Smart et al. (1994) demonstrated in small plots that a push-pull tac-tic reduced larval and adult damage in faba beans. Plots with phero-mone baited traps attracted more weevils than those sprayed with neem, which acted as a repellent. In an unpublished study in southern Alberta, Coles, and Cárcamo, planted winter pea in the fall along the borders of commercial fields planted to peas in the spring to assess damage by S. lineatus. They also experimented with the same spring

cultivar planted on the border about a week earlier than the rest of the field. Poor survivorship of the winter peas constrained use of this trap crop although damage was much higher and concentrated along the trap border relative to the main crop during the early invasion phase of the weevil. Their results from the spring trap crop planted earlier than the main crop were also promising, but logistically challenging because the farmers were not able to spray foliar insecticides on the trap crop more than once on a timely basis to protect the main crop. They concluded that the technique is promising, but requires timely monitoring and actions that growers managing very large farms may not be able to complete during the busy spring season. Trap crop-ping weevils at the end of the summer may provide another tactic to reduce regional populations in the long term. Field observations in Alberta suggest that faba bean is an attractive late season host in humid regions or under irrigation and may serve this purpose.

Intercrops add plant diversity to cropping systems and can reduce damage by oligophagous pests like S.  lineatus. Baliddawa (1984) reported reduced foliage damage and higher emigration rate of weevils from an intercrop of faba beans with oats conducted in England (United Kingdom). Neither nodule damage nor yield were measured in this work. The choice of the intercrop plants likely affects the outcome. In a study conducted in Poland, plant-ing Phacelia tanacefolia Benth (Boraginales:  Boraginaceae) with faba beans did not reduce foliar damage relative to the monocul-ture (Wnuk and Wojciechowicz-Żytko 2010). Alignier et al. (2013) studied the predation rates of Sitona eggs (lineatus?) in an intercrop of peas and wheat and the respective pea monocultures. There was a trend towards higher egg predation in the intercrop relative to the pea monoculture. Such patterns may result from higher activity of carabid beetles in intercrops of pulse crops with cereals than in monocultures (Cárcamo and Spence 1994) that are known predators of S. lineatus eggs (Vankosky et al. 2011c). More work needs to be done to better understand and implement habitat management strat-egies to improve the resistance of pulse cropping systems to insect pests such as S. lineatus.

Host Plant ResistanceFew studies have investigated crop plant resistance to manage S. lin-eatus in the past 20 yr. Field pea varieties have varying amount of wax layers on leaves due to genotypic variation (White and Eigenbrode 2000, Chang et al. 2004) and manipulation of these genotypes may have potential in producing resistant varieties. S.  lineatus prefers leaves and stipules with thinner wax layer compared to those that have thicker wax layer (White and Eigenbrode 2000). In Europe and elsewhere, a significant amount of work was done in an effort to identify and develop field pea with S.  lineatus resistance in the 1960s, 1970s, and 1980s (Tulisalo and Markkula 1970, Nouri-Ghanbalani et al. 1978, Auld et al. 1980, Havlickova 1982, Wnuk and Wiech 1983), but these efforts met with limited success (reviewed by Vankosky et al. 2009). New field pea and faba bean varieties and new tools for screening and introducing genetic-based resistance into plant populations may allow plant breeders to overcome past hur-dles. Other avenues of investigation with respect to host plant resist-ance may include studying the effects of plant volatiles that modify pest behavior. Further work on morphological characteristics of the host plant, such as waxy bloom and trichomes should also be done.

Conclusion and Research Gaps

Field peas and faba beans are two major sources of protein for an increasing world population, but pests such as the S.  lineatus rep-resent a major threat to production. Hence, it is not surprising that

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this insect has attracted the attention of many researchers and that we have made progress along many fronts. Its basic life cycle and phenology including dispersal flights are well known in most areas where it has become an established pest. Its plastic behavior in terms of host plant interactions depending on reproductive status are also relatively well known. Action thresholds have been developed and validated in a number of regions. Like most major insect pests, management relies mainly on chemical insecticides, particularly seed coated neonicotinoids (where still allowed). In regions with a mixture of conventional tilled and reduced or no-tilled fields, grow-ers can reduce damage risk by practicing no-till, but this option is limited in regions where most growers are already practicing no-till such as the southern Prairies of western Canada. A similar result to reduced or no tillage, can be obtained by delaying seeding as long as neighboring fields are planted earlier. Little research has been published on trap crops, intercrops, or biological control. With new screening molecular tools and biochemical advancements, develop-ing host plant resistance to S.  lineatus could be revisited. In addi-tion to increasing research efforts in these areas, there is a need to stack various tactics that incorporate higher diversity at the level of the landscape (see Hokkanen’s article in this collection), and within specific habitats to achieve a higher level of integrated pest manage-ment. This approach is necessary to improve the resilience of crop-ping systems to reduce pest risk given current trends that restrict the use of chemical insecticides as a standard control option.

AcknowledgmentsWe gratefully acknowledge financial support from the Alberta Pulse Growers Commission and Saskatchewan Pulse Growers, the Alberta Crop Industry Development Fund, Western Grains Research Foundation, Agriculture and Agri-Food Canada, in-kind contributions of Syngenta Crop Protection Canada and technical support from C. Herle, S. Daniels, C. Cheryl, R. Brandt, and numerous undergraduate students and interns. We thank Ross Weiss (AAFC-Saskatton) for graphic support and Michael Dolinski (Edmonton) for the weevil image.

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