Biology and management of Ceutorhynchus obstrictus (Coleoptera: Curculionidae) in spring-planted canola on the Northern Great Plains

Abstract

The cabbage seedpod weevil, Ceutorhynchus obstrictus (Marsham) (Coleoptera: Curculionidae), is an invasive pest infesting canola (Brassica napus L. and B. rapa L. (Brassicales: Brassicaceae)) crops in North America. Larval feeding causes significant damage leading to yield losses of 5–30%. Native to the Palearctic region, the species was accidentally introduced to North America over 90 yr ago, and now occupies most temperate regions of Canada and the United States. Currently, the species has been projected to continue its range expansion to potentially infest most canola producing regions in North America. Here, we review the taxonomic nomenclature, distribution, biology, pest status, and management of the cabbage seedpod weevil in North America with an emphasis on spring-planted canola crops in the Great Plains and highlight areas for future research to develop a comprehensive integrated pest management program against this debilitating pest.

Globally, canola (oilseed rape) (Brassica napus L. and B. rapa L. (Brassicales: Brassicaceae)) is one of the most important oilseed crops due to its use as a vegetable oil and protein source for animal feed. Canada is the world’s largest canola producer, averaging over 18.4 million metric tons annually produced on ca. 8.7 million hectares from 2017 to 2022 (Statistics Canada 2023a). Over 99% of Canadian canola production occurs in the prairie provinces of Alberta, Saskatchewan, and Manitoba (Statistics Canada 2023a). Canola is Canada’s most valuable crop, with average cash receipts of over 10 billion CAD from 2017 to 2022, which accounted for 25% of Canada’s total crop cash receipts (Statistics Canada 2023b). In the United States, the leading canola producing states include North Dakota, Montana, Washington, Minnesota, Oklahoma, and Kansas (United States Department of Agriculture (USDA) National Agricultural Statistics Services 2022). In 2022, over 1.7 million metric tons were produced on ca. 770,000 hectares directly contributing over 500 million USD to the US gross domestic product (GDP) (USDA Economic Research Service 2023).

The cabbage seedpod weevil, Ceutorhynchus obstrictus, is native to the Palearctic region where it has been recorded as an oligophagous pest of several brassicaceous seed crops, including oilseed rape, since the early 1800s (Baker 1936, Hoffman 1954, Bonnemaison 1957, Dmoch 1965, Scarisbrick and Daniels 1986). The species was first reported in North America in the early 1930s near Vancouver, British Columbia, Canada, and adjacent areas of Washington State, USA (Baker 1936, McLeod 1953). Subsequently, it spread throughout the Pacific Northwest (Hanson et al. 1948, Homan and McCaffrey 1993), California (Hagen 1946, Carlson et al. 1951, Crowell 1952), the US Southeast (Boyd and Lentz 1994, Buntin et al. 1995, Sangireddy et al. 2015), and the Prairie Provinces (Butts and Byers 1996, Dosdall et al. 2002) presumably via movement from neighboring colonized regions (Laffin et al. 2005). A second introduction in Quebec detected in 2001 (Brodeur et al. 2001, Laffin et al. 2005) resulted in the establishment in several eastern provinces in Canada (Mason et al. 2004, Gariepy et al. in press). As recently as the late 2010s, it has continued its expansion into canola producing regions in Manitoba, Canada (Western Committee on Crop Pests 2021) and North Dakota, USA (Knodel et al. 2017). Its expansion has made it a serious pest in a large portion of both the winter and spring-planted canola production regions in North America (Cárcamo et al. 2001, Dosdall and Cárcamo 2011, Cárcamo and Brandt 2017), and threatens the Peace River Region of Alberta and British Columbia, Canada’s most northern canola production region (Dosdall et al. 2002). Here, we review the current knowledge of C. obstrictus taxonomic nomenclature, distribution, biology, pest status, and management with an emphasis on spring-planted canola crops in the Great Plains of North America.

Taxonomic Nomenclature

The cabbage seedpod weevil, C. obstrictus, is a member of the subfamily Ceutorhynchinae Gistel, 1848 and the tribe Ceutorhynchini Gistel, 1848 (Alonso-Zarazaga et al. 2017). The genus Ceutorhynchus Germar, 1824, is a species-rich genus with a Holarctic distribution, with members almost exclusively associated with cruciferous hosts (Colonnelli 2004).

The nomenclature of this species, which had been known in the literature under the name Ceutorhynchus assimilis (Paykul), was revised following a detailed review of the name-bearing type specimens for this and related species by Colonnelli (1993). Consequently, C. assimilis (Paykull) was shown to be a senior synonym of the species known until then as Ceutorhynchus pleurostigmata (Marsham) and the correct name for the cabbage seedpod weevil was determined to be C. obstrictus (Marsham) (Colonnelli 1993). The incorrectly applied name C. assimilis was in wide use, including in North America, and as a result much of the older literature refers to the cabbage seedpod weevil as C. assimilis (e.g., Lindroth 1957, O’Brien and Wibmer 1982, Campbell et al. 1989, McNamara 1991, Williams 2006). A petition to conserve the name of C. assimilis for the cabbage seedpod weevil was submitted by Alford (2006) and reviewed by the International Commission of Zoological Nomenclature (ICZN). The Commission, which had already ruled on the validity of Ceutorhynchus assimilis and its status as the type species of Ceutorhynchus (ICZN 1989), subsequently closed Alford’s petition (ICZN 2007), confirming that C. obstrictus remained the correct name for the cabbage seedpod weevil. Thus, any records in North America for Ceutorhynchus assimilis, currently the valid name of a root-galling weevil of Lepidium draba L. (Brassicaceae) (Lesieur et al. 2018), refer to C. obstrictus. The Palearctic species C. assimilis is not known to be established in North America.

Insect Biology and Life Cycle

Adult cabbage seedpod weevils are ash-gray to black, approximately 3–4 mm long and have a distinct curved snout (Fig. 1). The grayish coloration, 7-segmented funicle, untoothed hind femora, and simple tarsal claws help distinguish this species from other possible Canadian congenerics (Blatchley and Leng 1916, Bonnemaison 1957). Males and females are similar in appearance and can be identified by examining the depressions on their last ventral abdominal segment (Fig. 2). Males have a wider concave depression, whereas females have a much narrower and shallower depression, sometimes visible as a “slit” or a “pinch” (Harmon and McCaffrey 1997a, Cook et al. 2006). Additionally, males have a spine-like projection, typically called a mucro, at the apex of their mid and hind tibiae (Fig. 2).

The cabbage seedpod weevil is univoltine (Fig. 3) (Dosdall et al. 2002). Sexually immature adult weevils overwinter beneath the soil, primarily in tree shelterbelts and leaf litter (Dmoch 1965, Ulmer and Dosdall 2006a). Adults have an obligatory diapause and require a cold period of at least 16 wk at 4 °C (Ni et al. 1990). Overwintering mortality of adults often limits population growth, accounting for 50% mortality per generation in Europe (Haye et al. 2010). Survival decreases significantly at −5 °C and increasingly negative temperatures will further reduce survivorship as the average threshold lethal freezing temperature (supercooling point) has been estimated to be only −7.2 °C (Cárcamo et al. 2009). In spring on the Northern Great Plains, adults begin to emerge as soil temperatures reach 9–12 °C and peak emergence occurs when average soil temperature reaches 15 °C (Ulmer and Dosdall 2006a). Adults are strong fliers and capable of sustained flight when the temperature exceeds 12 °C but fly most often at temperatures of 22 °C and low windspeeds (<0.5 m/s) (Dmoch 1965, Kjær-Pedersen 1992, Tansey et al. 2010a). Reduction in flight height and dispersal distance has been noted with increased relative humidity (Tansey et al. 2010a). After emergence, adults disperse to feed on various early-season Brassicaceae including field penny-cress (Thlaspi arvense L.), wild mustard (Sinapis arvensis L.), flixweed (Descurainia sophia (L.) Webb ex Prantl), and volunteer canola (B. napus L. and B. rapa L.) (Fox and Dosdall 2003, Dosdall and Moisey 2004) for several weeks before they initiate egg laying (Doucette 1947, Ni et al. 1990).

Adults migrate into canola crops at the bud and flowering stage (Fig. 3) (Dmoch 1965, Dosdall and Moisey 2004). Adults orient to the crop based on large concentrations of several glucosinolate-derived host plant volatiles (Free and Williams 1978, Bartlet et al. 1993, Smart and Blight 1997, Evans and Allen-Williams 1998, Moyes and Raybould 2001). Visual cues, in particular the yellow color and spectral quality of the crop, may also enhance attraction (Görnitz 1956, Smart et al. 1997, Tansey et al. 2010b). Females experience limited egg development before dispersing to canola, but this increases rapidly after they begin to feed (Dmoch 1965, Ni et al. 1990, Fox and Dosdall 2003). Adults feed primarily on pollen, flower buds, flower parts, and developing pods, but they can also feed on young leaves and the upper stem in canola (Dmoch 1965, Dosdall and Moisey 2004).

Following a period of feeding on canola, mating occurs throughout flowering (Fig. 3) (Dosdall and Moisey 2004). The use of a dedicated sex or aggregation pheromone in cabbage seedpod weevil has not been documented yet (Evans and Bergeron 1994), however, unmated overwintering females produce volatile chemicals that attract both males and females from a distance of at least 20 m over open ground in the spring (Evans and Allen-Williams 1992). Oviposition activity occurs while canola is still flowering, but pods on the lower raceme are elongating (Dosdall and Moisey 2004). Females select pods that are at least 2 mm in diameter (40–60 mm long) laying single eggs in feeding punctures (Doucette 1947, Kozlowski et al. 1983, Dosdall and Moisey 2004). After oviposition the female marks the pod with an oviposition-deterring pheromone, which prevents oviposition for 1–2 h (Kozlowski et al. 1983, Ferguson and Williams 1991, Ferguson et al. 1999), however, under outbreak conditions 2 or more eggs can be found developing in a single pod (Cárcamo et al. 2001). A single female lays up to 141 smooth, opaque white, and approximately spherical eggs (0.3–0.5 mm diameter) over 37 days as determined in field cages (Dosdall and McFarlane 2004, Haye et al. 2010). Eggs hatch approximately 1 wk after oviposition (Dosdall et al. 2002).

Larvae are yellowish-white, C-shaped, legless grubs with a brown head capsule and a body length of 3–4 mm (Figs. 3 and 4) (Dosdall and McFarlane 2004, Dosdall and Moisey 2004). Larvae progress through 3 instars feeding on seeds in the developing pod (Dmoch 1965, Dosdall and McFarlane 2004, Dosdall and Moisey 2004). Each larva may consume up to 6 seeds during their development (Dmoch 1965), which spans 2–4 wk depending on site temperature (Dosdall and McFarlane 2004). Larval feeding may lead to misshapen pods as some seeds are consumed whereas others are undamaged. When the larvae mature, they chew circular exit holes with jagged edges (~1–1.5 mm in diameter) (Figs. 3 and 6), drop to the ground, and burrow in the soil to pupate (Dmoch 1965). Pupation occurs 1–2 cm below the soil surface in earthen cells. Pupae are white, approximately 4 mm long with pigmentation noticeable in the compound eyes (Dosdall and McFarlane 2004).

Approximately 10 days after pupation, mature weevils emerge and start feeding on any green portion of Brassicaceae plants to prepare for overwintering (Dmoch 1965, Dosdall and Moisey 2004). To build up fat reserves before overwintering, the new adults can potentially disperse several km or more in search of food, especially to late-maturing crucifers (Doucette 1947, Buntin et al. 1995). When temperatures decline, weevils migrate to shelterbelts where they remain in diapause until soil temperatures warm the following spring (Ulmer and Dosdall 2006a).

Host Range and Damage

Host Plants

In western Canada, potential spring food sources for overwintered cabbage seedpod weevil include many species within the Brassicaceae: field penny-cress, wild mustard, flixweed, volunteer canola, wild mustard (Sinapis arvensis L.), hoary cress (Lepidium draba L.), shepherd’s purse (Capsella bursapastoris (L.) Medik.), and radish (Raphanus spp.) (Dmoch 1965, Fox and Dosdall 2003, Dosdall and Moisey 2004). Reproductive hosts, however, only include Brassicaceae species that produce larger pods to support all stages of larval development (Doucette 1947) such as B. napus (Dosdall and Mason 2010, Haye et al. 2013) and wild mustard (Doucette 1947, Dmoch 1965, Fox and Dosdall 2003). Yellow mustard (Sinapis alba L.) is not a host of cabbage seedpod weevil as it has antixenotic and antibiotic properties (Free and Williams 1978, Kalischuk and Dosdall 2004, Ulmer and Dosdall 2006b, Cárcamo et al. 2007, Ross et al. 2008).

Crop Damage

Crop injury, yield losses, and the consequent economic losses by cabbage seedpod weevil have been categorized based on plant growth stages. At the bud to flowering stage, mating pairs aggregate to feed, which may lead to the abortion of buds and flowers (“bud blasting”) (Coutin et al. 1974, Dosdall and Moisey 2004, Cárcamo 2012). The most significant damage to crops is caused by larval feeding that can reduce yield by an estimated 5–30% depending on seeding dates, region, and pest density (Dmoch 1965, McCaffrey et al. 1986, Buntin 1999, Cárcamo et al. 2019). If environmental conditions are humid after larvae bore exit holes, the pods can be invaded by secondary fungal pathogens that may damage additional seeds within the pods (Hong et al. 2021). In Europe, weevil damage is exacerbated by the pod midge, Dasineura brassicae Winnertz (Diptera: Cecidomyiidae) which uses the weevil damage to enter the pods (Free et al. 1983). To date, D. brassicae has not been found in North America. Additionally, under very dry conditions, the pods with exit holes may be predisposed to premature shattering, adding to yield losses (Cárcamo et al. 2001, Dosdall et al. 2001). Cultivars resistant to pod shatter may mitigate this damage. Newly emerged adults can cause further direct loss in yield and quality by feeding on seeds through the pod walls (Buntin et al. 1995). Feeding can also cause a loss in total seed weight and oil content (Buntin et al. 1995) but has not been shown to effect oil quality (Brown et al. 1999). The financial impact of larval feeding has been estimated at 3.7 USD million per annum in Alberta alone (Colautti et al. 2006) and the analysis does not consider indirect economic impacts or other sources of yield loss due to cabbage seedpod weevil.

Management

While most management of cabbage seedpod weevil relies on chemical control, there has been significant progress investigating alternative management strategies as part of an overall integrated pest management program.

Monitoring & Economic Thresholds

Several different monitoring techniques have been used for cabbage seedpod weevil. Yellow pan traps have been used to monitor seasonal activity periods and test attractiveness of host plant volatiles (Bonnemaison 1957, Free and Williams 1978). Similarly, flight intercept traps (Ferguson et al. 2000) and bowl traps (Dosdall et al. 2006a, Blake et al. 2010) have been used to study the spatial distribution and phenology of cabbage seedpod weevil.

Sweep nets are the most commonly recommended tool for monitoring cabbage seedpod weevil to assess their geographic distribution, relative population abundance, and to determine if local population densities meet the economic thresholds for insecticide application in North America (McCaffrey 1992, Dosdall et al. 2001, Blodgett and Johnson 2006, Cárcamo et al. 2019). The Prairie Pest Monitoring Network (PPMN) and its many collaborators from Alberta, Saskatchewan, and Manitoba, Canada, have monitored the distribution and relative abundance of cabbage seedpod weevil in canola fields since 1997 using sweep net samples. Distribution maps for cabbage seedpod weevil (Fig. 5) developed by the PPMN are available online (PPMN 2023a). These maps can be used by farmers and agronomists to identify regions at risk of cabbage seedpod weevil infestation, where scouting efforts should be focused.

Scouting should begin when the canola crop enters the bud stage and should continue through flowering; a protocol outlining scouting techniques developed for western Canada is available online from the PPMN (PPMN 2023b). Initially, it was recommended that 10 locations within the crop (half along the field border) be sampled using ten 180° sweeps of a standard (38 cm diameter) sweep net (Dosdall et al. 2001) as insects tend to be clustered at field edges during their migration into the crop (Free and Williams 1979). Recently, Cárcamo et al. (2019) determined that as few as 4 sample locations per field could be used given that 1 sample was collected along the field border and 1 sample collected from 50 m into the interior of the crop and with both repeated at least 500-m distance. Initially, a nominal threshold of 3–4 weevils per sweep at the early flowering stage (20% bloom, 70% of canola plants with 3–10 open flowers) of canola was recommended in Canada (Dosdall et al. 2001, Dosdall and Moisey 2004) and 3–6 weevils per sweep in the US Great Plains and Pacific Northwest (McCaffrey 1992, Blodgett and Johnson 2006). Recently in Canada, the nominal threshold was validated and the economic injury level was calculated at 20 weevils per 10 sweeps (2 weevils per sweep) at early flower (10–20% bloom), but the economic threshold set to 25–40 weevils per 10 sweeps (2.5–4 weevils per sweep) because sampling usually occurs along the field edge where weevils are concentrated (Dosdall et al. 2006a, Cárcamo et al. 2019). If beneficial insects are present a higher threshold is recommended (i.e., 4 weevils per sweep). In other parts of the world, various thresholds have been developed, but differences in crop type (e.g., spring vs. winter oilseed rape) and growth stage sampled (Sylven and Svenson 1975, Tulisalo et al. 1976, Free et al. 1983) do not make them comparable to those used in North America.

The percentage of pods with exit holes (Fig. 6) at harvest time can be used to assess the efficacy of control measures. Keeping the percentage of pods with exit holes below 25% has been suggested by various studies as a guideline to avoid yield losses (Lerin and Rivault 1984, Buntin 1999, Cárcamo 2012).

Chemical Control

Although a large body of research has been conducted on alternative pest management strategies, the use of insecticides for control of cabbage seedpod weevil remains the main management tactic. Various foliar-applied insecticides belonging to 2 different classes of chemical compounds (e.g., pyrethroids and anthranilic diamides) are used in North America to manage cabbage seedpod weevil populations (Buntin 2015, The Blue Book 2023). However, recent labeling changes by Pest Management Regulatory Agency (2021) in Canada have reduced the number of insecticide active ingredients available for cabbage seedpod weevil management. Currently, in western Canada only pyrethroids with the active ingredient deltamethrin are labeled for use in canola, while US producers still have options including several foliar applied products within the pyrethroids and diamides (Whaley et al. 2016). In the United States, some neonicotinoid-seed treatments are also registered for cabbage seedpod weevil control (Whaley et al. 2016); however, in Alberta, research found seed treatments containing neonicotinoids coatings did not provide sufficient control (Cárcamo et al. 2005, Dosdall 2009). The lack of potential insecticide chemistries that can be rotated as part of a resistance management program in Canada is troubling as resistance to some pyrethroids (e.g., lambda-cyhalothrin) has been found in cabbage seedpod weevil in Germany (Heimbach and Müller 2013). To date, no insecticide resistance has been noted in cabbage seedpod weevil populations in North America and no active resistance management programs are in place; however, several of the Authors are actively pursuing research to determine the current susceptibility/resistance levels across the Canadian Prairies.

To reduce the use of insecticides and to protect parasitoids and other nontarget species, it may be possible to exploit the aggregation of cabbage seedpod weevils. At moderate densities throughout early flowering, weevils have been reported to be more abundant along the edges of fields (Free and Williams 1979, Ferguson et al. 2000, Dosdall et al. 2006a), and Jourdheuil et al. (1974) demonstrated in France that spraying the borders provided adequate crop protection and maintained the parasitoid population in the rest of the field. This natural aggregation pattern of cabbage seedpod weevil has the potential to be developed into an effective trap crop system.

Cultural Control

Trap cropping has been investigated in several regions for management of cabbage seedpod weevil with varying levels of success (Buechi 1990, Buntin 1998, Cárcamo et al. 2007). Earlier studies experimented with trap crops for cabbage seedpod weevil in canola or related crops in plots, but the mobility of the weevil made it difficult to demonstrate benefit of the trap crop (Buechi 1990, Buntin 1998). Cárcamo et al. (2007) demonstrated the potential to manage cabbage seedpod weevil with trap crops in large commercial fields (ca. 1.6 km²). It requires planting a perimeter of canola or another closely related species that flowers before the rest of the main crop during the migration of the weevil. Large numbers of weevils aggregated on the trap crop border where they were killed with insecticides (Cárcamo et al. 2007). However, trap crops were less effective when fields are smaller or narrower, and when weevil population densities are high because the main crop is overwhelmed by the weevils (Cárcamo et al. 2007). Establishing a trap crop system (as per Cárcamo et al. 2019) should be more feasible than past attempts given the recent developments including widespread adoption of pod shatter resistant cultivars that can be harvested directly with a combine later in the trap crop border as well as increased availability of early maturing cultivars for the main crop. Several studies have been conducted to highlight the importance of the spatial arrangement of trap crop around the main crop (Potting et al. 2005). Field margin manipulation, identifying more attractive trap plants, and potential integration with bee biovectoring of microbial insecticides (Kevan et al. 2020) may prove both financially and ecologically beneficial.

Other cultural strategies have been investigated for cabbage seedpod weevil management, but their efficacy is less understood. Removal of brassicaceous weeds to prevent early-season hosts may reduce weevil abundance (Dosdall et al. 2001). Crop rotation is a recommended agronomic practice for growing canola but is expected to have minimal short-term impact on cabbage seedpod weevil given their high dispersal ability (Kjær-Pedersen 1992, Cárcamo et al. 2001). However, other landscape scale characteristics, such as noncrop areas providing refugia for parasitoid communities, have been shown to affect the numbers of cabbage seedpod weevils and their parasitoids (Kovács et al. 2019, D’Ottavio et al. 2023). Soil fertility can also impact the distribution of cabbage seedpod weevil throughout canola fields. Blake et al. (2010) found a complex relationship between the distribution of weevil adults and larvae and plant nutrients. Adult and larval abundance was correlated with nitrogen and sulfur, with egg-laying females preferring plants with low nitrogen, but high sulfur levels. However, the relationships with other plant nutrients were less consistent. This attraction seems to at least partially be mediated by changes in the foliar and floral appearance of plants (Blake et al. 2014). These changes in plant nutrition can also contribute to resistance through antibiosis, with larval development times increasing with increasing nitrogen fertilization (Blake et al. 2011). As a result of the attraction of female weevils to plants with low nitrogen and high sulfur levels (Blake et al. 2010), and sulfur fertilization alone increasing infestation levels by cabbage seedpod weevil (Aljmli 2007), balanced nitrogen and sulfur fertilization is suggested.

Seeding date and rate can affect infestation levels of cabbage seedpod weevil. Plants seeded below the typical rate of 3–5 kg/ha and seeded in mid-May both exhibited lower infestation rates than plants seeded at a lower rate and earlier in the season (Dosdall et al. 2006b). It is well recognized that early planted canola crops, typically late-April on the southern Canadian prairies, are the first to flower and are highly attractive to cabbage seedpod weevil (Brown et al. 1999, Cárcamo et al. 2019). Delayed planting may reduce the likelihood of infestations but must be balanced with the agronomic benefits of seeding early (e.g., higher soil moisture) and increasing risks to other pests such as flea beetles (Knodel et al. 2008, Cárcamo et al. 2009) or lygus bugs (Cárcamo et al. 2019).

Host Plant Resistance

Host plant resistance is another potential strategy to sustainably manage cabbage seedpod weevil populations (Ulmer and Dosdall 2006b). However, host plant resistance does not differ significantly among commercial lines of canola (B. napus and B. rapa), B. juncea, and many other mustards (Williams 1989, McCaffrey et al. 1999, Kalischuk and Dosdall 2004). Sinapis alba is almost immune to cabbage seedpod weevil damage (Free and Williams 1978, Kalischuk and Dosdall 2004, Ulmer and Dosdall 2006b, Cárcamo et al. 2007, Ross et al. 2008), but is commercially unsuitable for oil and meal production (Brown et al. 1997). To overcome some of these issues, introgressed lines of S. alba × B. napus have been developed (Brown et al. 1999, Dosdall and Kott 2006), as well as experimental lines of S. alba with near canola-quality like properties with high levels of resistance to seedpod weevil (Cárcamo et al. 2007).

Various experiments assessing B. napus, S. alba, and introgressed lines found lower levels of weevil damage and fewer larvae completing development on several introgressed lines compared to B. napus and that resistance is conferred in the form of both antibiosis and antixenosis (Dosdall and Kott 2006, Tansey et al. 2010c). For example, the presence of p-hydroxybenzyl glucosinolate in S. alba seeds and the introgressed lines correlated with reduced weevil growth and longer development time (McCaffrey et al. 1999, Ulmer and Dosdall 2006b). Similarly, the lack of 2-phenylethyl glucosinolate in tissues of S. alba and the introgressed lines correlated with reduced larval development (Tansey et al. 2010c). In another study, the reduced attraction of adult weevils to S. alba tissues and the introgressed lines was linked to the lack of 2-phenylethyl glucosinolate, however, volatile organic compounds released from the plants were not analyzed (Tansey et al. 2010c). Additionally, the identity of 2-phenylethyl glucosinolate was predicted by retention time shifts and not determined directly (Tansey et al. 2010d). Reduced attraction was also attributed to reductions in floral reflectance of yellow and UV wavelength bands (Tansey et al. 2010b). Furthermore, Tansey et al. (2010d) suggested that resistance was conferred in the introgressed lines by the toxic or antifeedant effect of 1-methoxy-3-indolylmethyl glucosinolate which was later identified to be the flavonoid, kaempferol 3-O-sinapoyl-sophoroside 7-O-glucoside (KSSG) (Lee et al. 2014). Rather than using introgressed lines, Cárcamo et al. (2007) investigated the potential of near canola-quality lines of S. alba from the Saskatoon Research and Development Centre (Katepa-Mupondwa et al. 2006). These lines maintained significant resistance to cabbage seedpod weevil relative to B. napus or B. rapa. To date, no commercial quality introgressed lines have been developed, but research continues into their host plant resistance properties for potential future use (Hervé 2017).

Biological Control

A number of parasitoids have been identified to attack cabbage seedpod weevil throughout its native and invasive range (summarized in Cárcamo and Brandt 2017 and Gariepy et al. in press). In the invaded North American range, biological control via parasitoids has been less effective against cabbage seedpod weevil populations than in Europe (Harmon and McCaffrey 1997b, Williams 2003, Dosdall et al. 2009). Although an estimated 15 parasitoid species in western Canada have extended their host range to attack cabbage seedpod weevil, their attack rates are insufficient to control the pest (<15%; Dosdall et al. 2006a, Blake et al. 2010, H. Cárcamo, unpublished data).

In Europe, parasitoids are more effective in controlling the cabbage seedpod weevil. Trichomalus perfectus (Walker) (Hymenoptera: Pteromalidae) and Mesopolobus morys (Walker) (Hymenoptera: Pteromalidae) have parasitism rates of 52–90% (Buntin 1998, Murchie and Williams 1998, Williams 2003, Haye et al. 2010). Due to higher parasitism rates in Europe, classical biological control has been examined as a potentially effective strategy to manage cabbage seedpod weevil populations in North America. Trichomalus perfectus has established in Quebec and Ontario, Canada (Mason et al. 2011, Haye et al. 2013). Haye et al. (2015) noted that in Europe, T. perfectus will attack other Ceutorhynchus weevils, but only in the siliques of Brassicaceae plants. Studies have been undertaken to explore the potential of introducing T. perfectus from eastern to western Canada by examining parasitism rates and nontarget effects in the east. Studies in Quebec found parasitism rates from 5 to 25% and suggest that T. perfectus has limited impact on nontarget weevils in uncultivated habitats (D’Ottavio et al. 2023, Desroches et al. 2023). These studies show promise for the development of classical biological control given its potential to establish on the Canadian Prairies (Haye et al. 2018).

The majority of biological control research in North America has explored the potential of parasitoids to manage cabbage seedpod weevil, with studies suggesting more work needs to be conducted on predators (e.g., Gariepy et al. in press, Cárcamo and Brandt 2017). Larvae developing in pods are relatively protected from generalist predators, but upon exit they fall to the ground where both the mature larvae and pupae are prone to predation (Williams et al. 2010). In Europe, life table analysis conducted on cabbage seedpod weevil suggests generalist predators, and in particular ground beetles (Carabidae), can cause significant mortality (ca. 34–45%) of the mature larval and pupal stages (Haye et al. 2010). Both Harpalus affinis (Shrank) and Pseudophonus rufipes (De Geer) (Coleoptera: Carabidae) where found to consume Ceutorhynchus spp. from oilseed rape fields in Europe, but the exact Ceutorhynchus species could not be determined (Schlein et al. 2006). Harpalus affinis is also found throughout Canada in regions coinciding with cabbage seedpod weevil (Bousquet et al. 2013). In cabbage seedpod weevil life table studies in British Columbia and Ontario, Canada, both ground beetles and wolf spiders (Paradosa spp. C.L. Koch (Araneae: Lycosidae)) were estimated to cause 9–22% mortality of mature larvae and pupae (Gillespie et al. 2019). Studies on direct predation of cabbage seedpod weevil across the Canadian Prairies are lacking, although ground beetles are one of the best studied groups of insects in canola systems (see Gavloski et al. 2011) and thus warrant further investigations.

Conclusions and Future Directions

Despite decades of research on cabbage seedpod weevil, insecticide application remains the most prominent method of control. While considerable efforts have been made to move away from the use of chemical control methods to more sustainable and environmentally friendly methods, there are still many questions about weevil management that remain unanswered. Some of the questions involve developing host plant resistance, biological and cultural control, and an integration of these methods. Others include refining trap crops to reflect current farming systems (i.e., shatter-resistant and early-flowering canola cultivars); managing weevils concentrated in trap crops with insecticide alternatives such as entomopathogenic fungi or a strain of Bacillus thuringiensis or approaches that will integrate bee biovectoring (Kevan et al. 2020); identifying and establishing effective parasitoids in North America; developing and keeping a long-term data base repository of crop yield and weevil abundance/damage to refine thresholds; elaborating on population dynamics and migration, particularly between the United States and Canada, as well as other ecological factors that affect populations (e.g., predator communities in North America); and understanding the role of plant volatile compounds and weevil pheromones (Ulmer and Dosdall 2006b, Tansey et al. 2010d). In addition, further studies on fall-seeded canola (winter canola) in the southern Great Plains are needed as acreage continues to expand. Knowledge in these areas will improve the sustainability of cabbage seedpod weevil management, especially as climate change contributes to range expansion, and also variable weather patterns (i.e., temperature and moisture) which may influence population dynamics in established regions (Olfert and Weiss 2006, Cárcamo et al. 2009, Weiss et al. 2022).

Acknowledgments

We thank Shelley Barkley for providing photographs used in this paper and to Anthony Davies for preparation of the plate (Fig. 2). We would also like to thank 2 anonymous reviewers for their constructive comments. Financial support was provided by a NSERC Industrial Research Chair (545088) and partner organizations (Alberta Wheat Commission, Alberta Barley Commission, Alberta Canola Producers Commission, Alberta Pulse Growers Commission) as well as an NSERC Discovery Grant (2021-02479) to B.A.M. during the preparation of the manuscript.

Author Contributions

Altaf Hussain (Conceptualization [Equal], Investigation [Lead], Visualization [Supporting], Writing – original draft [Lead], Writing – review & editing [Supporting]), Priyanka Mittapelly (Conceptualization [Supporting], Investigation [Supporting], Writing – original draft [Supporting], Writing – review & editing [Supporting]), Adam Blake (Conceptualization [Supporting], Investigation [Supporting], Visualization [Supporting], Writing – original draft [Supporting], Writing – review & editing [Supporting]), Julian Dupuis (Conceptualization [Supporting], Investigation [Supporting], Visualization [Supporting], Writing – original draft [Supporting], Writing – review & editing [Supporting]), Patrice Bouchard (Investigation [Supporting], Resources [Supporting], Visualization [Supporting], Writing – review & editing [Supporting]), Tristan Skolrud (Investigation [Supporting], Writing – original draft [Supporting], Writing – review & editing [Supporting]), B. Keddie (Investigation [Supporting], Supervision [Supporting], Writing – original draft [Supporting], Writing – review & editing [Supporting]), Meghan Vankosky (Investigation [Supporting], Resources [Supporting], Visualization [Supporting], Writing – original draft [Supporting], Writing – review & editing [Supporting]), Hector Carcamo (Conceptualization [Supporting], Investigation [Supporting], Resources [Supporting], Visualization [Supporting], Writing – original draft [Supporting], Writing – review & editing [Supporting]), and Boyd Mori (Conceptualization [Equal], Funding acquisition [Lead], Investigation [Supporting], Project administration [Lead], Resources [Lead], Supervision [Lead], Writing – original draft [Equal], Writing – review & editing [Lead])

References