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The Eurasian strawberry blossom weevil, Anthonomus rubi (Herbst, 1795), is established in North America

Published online by Cambridge University Press:  23 June 2021

Michelle T. Franklin*
Affiliation:
Agriculture and Agri-Food Canada, Agassiz Research and Development Centre, 6947 Highway 7, P.O. Box 1000, Agassiz, British Columbia, V0M 1A0, Canada
Tracy K. Hueppelsheuser
Affiliation:
British Columbia Ministry of Agriculture, Food and Fisheries, Plant and Animal Health Branch, 1767 Angus Campbell Road, Abbotsford, British Columbia, V3G 2M3, Canada
Paul K. Abram
Affiliation:
Agriculture and Agri-Food Canada, Agassiz Research and Development Centre, 6947 Highway 7, P.O. Box 1000, Agassiz, British Columbia, V0M 1A0, Canada
Patrice Bouchard
Affiliation:
Agriculture and Agri-Food Canada, Canadian National Collection of Insects, Arachnids, and Nematodes, Ottawa Research and Development Centre, 960 Carling Avenue, K.W. Neatby, Ottawa, Ontario, K1A 0C6, Canada
Robert S. Anderson
Affiliation:
Beaty Centre for Species Discovery, Canadian Museum of Nature, P.O. Box 3443, Station D, Ottawa, Ontario, K1P 6P4, Canada
Gary A.P. Gibson
Affiliation:
Agriculture and Agri-Food Canada, Canadian National Collection of Insects, Arachnids, and Nematodes, Ottawa Research and Development Centre, 960 Carling Avenue, K.W. Neatby, Ottawa, Ontario, K1A 0C6, Canada
*Corresponding
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Abstract

We report the strawberry blossom weevil, Anthonomus rubi (Herbst, 1795) (Coleoptera: Curculionidae), a species native to Europe, Asia, and North Africa, as established in British Columbia, Canada. This is the first report of A. rubi in North America. We provide a diagnosis of the species and compare it with other species of the genus Anthonomus Germar in Canada. This species is a pest of plants in Rosaceae Jussieu, including economically important berries such as strawberries (Fragaria Linnaeus) and raspberries (Rubus idaeus Linnaeus), and of native berries of importance to Indigenous peoples in Canada. Female weevils oviposit eggs inside developing flower buds and sever flower stalks, facilitating larval development inside damaged buds and thus reducing fruit yields. Surveys to confirm the presence of A. rubi conducted in 2020 found the weevil to be well established in cultivated and wild hosts throughout the Greater Vancouver area and Fraser Valley, British Columbia. At least one species of parasitoid wasp in the genus Pteromalus Swederus (Hymenoptera: Pteromalidae) has been found in association with A. rubi in the province. Future investigations are required to understand the biology of A. rubi in its new range, assess its impact on berries, and develop management strategies.

Type
Scientific Notes
Copyright
© The authors and Her Majesty, the Queen, in right of Canada, 2021. Published by Cambridge University Press on behalf of the Entomological Society of Canada

Accounts of new invasive species continue to rise, as increased global trade and transportation facilitate unintended movements of species around the world (Banks et al. Reference Banks, Paini, Bayliss and Hodda2015). Insects account for the greatest number of invasions of all animal taxa and pose a significant threat to agricultural production and food security worldwide (Liebhold et al. Reference Liebhold, Yamanaka, Roques, Augustin, Chown, Brockerhoff and Pyšek2016; Suckling et al. Reference Suckling, Stringer, Baird and Kean2019). Here, we report the first records of the economically significant agricultural pest, the strawberry blossom weevil, Anthonomus rubi (Herbst, 1795) (Coleoptera: Curculionidae), in North America. We found evidence that A. rubi is established in the Lower Mainland region of British Columbia, Canada. The previously known geographic range of A. rubi includes Europe, Asia, and parts of North Africa (Alonso-Zarazaga et al. Reference Alonso-Zarazaga, Barrios, Borovec, Bouchard, Caldara and Colonnelli2017).

The first five specimens of this weevil were collected by T. Hueppelsheuser in Abbotsford, British Columbia on raspberries (Rubus idaeus Linnaeus) (Rosaceae) during the summer of 2019 after a resident brought in dead flower buds from his backyard berry patch. The specimens were identified (by PB and RSA) using published information from a European source (Rheinheimer and Hassler Reference Rheinheimer and Hassler2013) and comparisons of external morphology and male genitalia with European specimens held in the Canadian National Collection of Insects, Arachnids, and Nematodes (Ottawa, Ontario, Canada) and the Canadian Museum of Nature (Ottawa). Species identification was confirmed using cytochrome c oxidase 1 DNA barcoding of two specimens (barcode index number BOLD: AAO1528; specimen database number BIOUG42770-H07, BIOUG42770-H08; www.boldsytem.org). Voucher specimens are deposited in the Canadian National Collection of Insects, Arachnids, and Nematodes and in the Canadian Museum of Nature.

Adults of A. rubi are small (2.5–3.0 mm), black, with an almost uniform dorsal covering of widely separated small, elongate, white scales. The scutellum has the scales condensed forming a bright white patch, and the rostrum is very long and slender. The front femoral tooth is small and sharp. Including A. rubi, there are 36 species of Anthonomus Germar in Canada. Of these, three are fully black; A. rubi, on the rose family (Rosaceae) (Fig. 1A, B); A. corvulus LeConte, on dogwood (Cornus Linnaeus) (Cornaceae) (Fig. 1C, D); and A. nigrinus Boheman, on horse nettle (Solanum carolinense Linnaeus) (Solanaceae) (Fig. 1E, F). The fourth species, Anthonomus signatus Say, on the rose family (Rosaceae), has a black colour morph in British Columbia (Fig. 1G, H) that appears to be conspecific with eastern reddish specimens. Anthonomus corvulus is widespread in Canada, from the Maritimes (New Brunswick, Nova Scotia, and Prince Edward Island) west to British Columbia, but is easily distinguished from A. rubi by its smaller body size – that is, 1.5–1.9 mm, compared to 2.5–3.0 mm for A. rubi – and association with dogwood. Anthonomus rubi could be confused with the similarly sized A. nigrinus (2.3–2.8 mm), but the latter is an eastern species recorded in Canada to date only from Québec (there is an old specimen in the Canadian National Collection labelled “N.W.T.”, with no further indication of locality), and it is associated with Solanaceae. In British Columbia, A. signatus is the most likely species to be confused with A. rubi. Specimens of A. signatus are also associated with Rosaceae, and the elytra vary in colour from black in British Columbia to reddish brown in eastern Canada. In British Columbia, the black specimens of A. signatus can be differentiated from A. rubi by their slightly smaller body size (1.5–1.9 mm) and presence of a crescentic fascia of scales on the elytra (Fig. 1G, H), which is lacking from A. rubi (Fig. 1A, B). Male genitalia also differs between these two species. The fifth species, Anthonomus eugenii Cano (the pepper weevil; Carpintera Reference Carpintera2002), is also fully black and of similar size to A. rubi, but it is a more southern species found in North America only in the southern United States of America as a pest of commercial peppers (Solanaceae) and sometimes found in Canadian pepper greenhouses, likely due to the import of peppers from the United States of America and Mexico (Fernández et al. Reference Fernández, VanLaerhoven, McCreary and Labbé2020).

Fig. 1. Habitus images of species of Anthonomus: A and B, A. rubi from Watson Glen Park, Chilliwack, British Columbia, Canada; C and D, A. corvulus from Spruce Woods National Park, Manitoba, Canada; E and F, A. nigrinus from La Porte County, Indiana, United States of America; and G and H, A. signatus from Dawson Creek, British Columbia.

In its native range, A. rubi is a serious pest of Rosaceae of agricultural importance, including strawberries (Fragaria Linnaeus), raspberries (Rubus idaeus Linnaeus), and roses (Rosa spp.; Milenković and Stanisavljević Reference Milenković, Stanisavljević, Gordon and Cross2003; Uggla and Martinsson Reference Uggla and Martinsson2005; Popov Reference Popov2017). Adult female weevils lay their eggs inside developing flower buds, severing the bud peduncle to prevent bud development and to facilitate larval development inside the aborted buds (Kovanci et al. Reference Kovanci, Kovanci and Gencer2005). Larvae feed on pollen inside the damaged buds and develop through three instars that can be differentiated based on head-capsule size (Popov Reference Popov2017). We observed the characteristic damage of severed buds on cultivated and wild hosts in the newly invaded range during the 2019 and 2020 growing seasons (Fig. 2). During her lifetime, a single female has been reported to damage between 20 and 30 buds (Krauß et al. Reference Krauß, Steen and Zebitz2014); however, bud damage could be considerably higher if the estimate of fecundity of 158 eggs per female by Easterbrook et al. (Reference Easterbrook, Fitzgerald, Pinch, Tooley and Xu2003) reflects A. rubi’s true damage potential. As a result, severe damage and yield losses can occur when A. rubi populations reach high numbers (Aasen et al. Reference Aasen, Ha˙gvar and Trandem2004; Baroffio et al. Reference Baroffio, Borg-Karlsson, Cross, Fountain, Guibert and Hall2015; Popov Reference Popov2017). Insecticides from the pyrethroid and organophosphate classes have been used to target adult weevils; however, these insecticides have had limited success in their native range (15%–30% less bud damage), and resistance of A. rubi to pyrethroids has been reported (Aasen and Trandem Reference Aasen and Trandem2006).

Fig. 2. A, Damage caused by adult female Anthonomus rubi to Himalayan blackberry (Rubus armeniacus), including severing of the pedicel and oviposition hole; B, adult A. rubi inside an open strawberry (Fragaria sp. Linnaeus) blossom. Photos by Warren Wong, University of British Columbia, Vancouver, British Columbia, Canada.

Bud losses associated with A. rubi in Europe typically range from 5% to 90% and can result in yield losses over 60% (Simpson et al. Reference Simpson, Easterbrook, Bell and Greenway1997; Aasen et al. Reference Aasen, Ha˙gvar and Trandem2004; Baroffio et al. Reference Baroffio, Borg-Karlsson, Cross, Fountain, Guibert and Hall2015; Popov Reference Popov2017). In our 2020 survey in British Columbia, adult weevils and larvae were found to be present in cultivated strawberries, raspberries, and blackberries (Rubus fruticosus Linnaeus; Fig. 3). If fruit losses are consistent with those reported in the native range of A. rubi, this weevil poses a significant risk to British Columbia’s raspberry and strawberry industries. British Columbia is the largest raspberry producer of all Canadian provinces, with over 75% of Canada’s production; the province also contributes 5% to Canada’s strawberry production (Statistics Canada 2019). Any further spread of this pest across Canada is of even greater concern because the combined farm gate value of these industries to Canada is more than $150 million annually (Statistics Canada 2019). Anthonomus rubi may also pose a substantial threat to berry production in adjacent areas in the United States of America if it spreads and establishes southwards. In our surveys, A. rubi was also found on non-crop native berries such as salmonberries (Rubus spectabilis Pursh) and thimbleberry (Rubus parviflorus Nuttall) and thus also presents a risk to berry crops that are important to Indigenous peoples in Canada (Kuhnlein Reference Kuhnlein1989). In addition, these non-crop hosts could serve as reservoirs that could make management of A. rubi in cropping systems more challenging.

Fig. 3. Map of locations where Anthonomus rubi was found associated with various host plants in British Columbia, Canada in 2020, indicated with coloured points. Some points are displaced slightly for clarity. The red box within the inset (upper right) shows the surveyed region within North America. Map tiles by Stamen Design, CC BY 3.0; data by OpenStreetMap, open database licence.

In its native range, A. rubi is known to complete a single generation in a year, with the oviposition period typically beginning in May and lasting one to two months (Jary and Dip Reference Jary and Dip1931). Adult weevils overwinter in the litter within crop fields or surrounding forest habitats (Parikka and Tuovinen Reference Parikka and Tuovinen2014). At 20 °C, the total development time from egg to adult is approximately 23 days; at lower temperatures, development time can exceed 90 days (Easterbrook et al. Reference Easterbrook, Fitzgerald, Pinch, Tooley and Xu2003). In British Columbia, we observed adult weevils on buds and flowers from May until the end of September in 2020. We suspect that Himalayan blackberry (Rubus armeniacus Focke) may be an important late-season host in British Columbia because we observed eggs, all larval stages, and pupae in dissected blackberry buds until the end of September. The phenology of A. rubi has been observed to be closely linked with that of its host plants in its native range, and larval diapause has been observed in the laboratory (Popov Reference Popov2017). Based on our observations of late-season presence of A. rubi larvae in Himalayan blackberry, we hypothesise that, in addition to adult diapause, A. rubi can also undergo larval diapause, allowing larvae to successfully overwinter and complete development during the following spring in British Columbia. Further studies are required to test this hypothesis.

From the end of July to mid-September 2020, we collected branches containing fully closed (pre-bloom) severed and intact green buds from Himalayan blackberry at the Agassiz Research and Development Centre, Agriculture and Agri-Food Canada (Agassiz, British Columbia) and dissected a random sample of 6–32 buds weekly (total N = 116). On average, the percentage of buds containing A. rubi eggs and larvae ranged from 33% to 54% over the course of the sampling period. Adult females typically oviposit a single egg in each bud; however, previous studies have observed a small fraction of strawberry buds that contain two or three eggs (Popov Reference Popov2017). We observed two larvae in 6% of the Himalayan blackberry buds examined.

In Europe, parasitoid wasps from the families Braconidae (Ichneumonoidea) and Pteromalidae (Chalcidoidea) have been recorded as parasitoids of the larval stages of A. rubi and have some potential as biocontrol agents (Cross et al. Reference Cross, Easterbrook, Crook, Crook, Fitzgerald and Innocenzi2001). To determine whether natural enemies of A. rubi were present in its newly invaded range, damaged blackberry and raspberry buds were collected from the Agassiz Research and Development Centre as well as from roadsides and disturbed sites in Chilliwack and Maple Ridge, British Columbia from July to October 2020. These buds were then stored in plastic containers (temperatures range 14–25 °C) and monitored three times weekly for parasitoid emergence. More than 150 specimens of Pteromalidae emerged from these samples, representing at least one species of Pteromalus Swederus (Pteromalidae) to be associated with A. rubi, based on these bud collections. Strengthening the case that these parasitoids were in fact attacking A. rubi, we observed parasitoid larvae inside aborted buds with dead, shrivelled A. rubi larvae from samples that later yielded emerging Pteromalus. The parasitoid specimens were identified to genus by G. Gibson using available keys and morphological comparison with specimens in the Canadian National Collection, where voucher specimens are deposited. However, about 45 valid species of Pteromalus are currently recognised from North America (Noyes Reference Noyes2019), including species recorded only from North America and those recorded also from Europe. There is no modern revision of the species from North America, and additional research is required to identify the specimens to species, determine their origin, and assess their potential as biocontrol agents. Natural enemies, including these parasitoids, could serve as an important component of integrated pest management programmes for A. rubi in North America.

Examination of records from the United States Department of Agriculture, Agriculture Quarantine Activity System database from 1984 to 2014 indicates that A. rubi has been previously intercepted at a United States of America port of entry on a shipment of flowers of a species of Astilbe Arends (Saxifragaceae) from the Netherlands (Smith-Pardo Reference Smith-Pardo2015). Although no known specimens have been recorded to date from the United States of America, we suspect that A. rubi is likely already in Washington state because weevils were detected at several sites in British Columbia, including three within 20 metres of the Canada–United States of America border (Fig. 3). We encourage future collaborative studies by Canadian and American agencies to monitor the pest’s distribution and to develop effective, low environmental risk mitigation strategies to limit its spread and protect cultivated and native berry production in North America.

Acknowledgements

The authors thank Emily Grove, Paula Eraso, Jade Sherwood, and Jason Thiessen for their assistance in the field and Warren Wong for providing images. They also thank Jen McFarlane, Allyson Mittelstaedt, and Arlan Benn from ES Cropconsult, Dave Holden from the Canadian Food Inspection Agency for assisting with field monitoring and collections, Eric Gerbrandt, Research Director of the BC Strawberry and Raspberry Associations for their help with organising access to field sites, and Andrew Smith of the Canadian Museum of Nature for taking the specimen photos and preparing the plate. Last, the authors thank Hannes Baur from the Natural History Museum of Bern for his assistance with the morphological identification of Pteromalus specimens. This research was supported by funding from Agriculture and Agri-Food Canada (MTF, PKA, PB), the Lower Mainland Horticulture Improvement Association, and the Canadian Agricultural Partnership, a federal–provincial–territorial initiative (MTF, PKA, TH).

Footnotes

Subject editor: Roselyne Labbé

References

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Figure 0

Fig. 1. Habitus images of species of Anthonomus: A and B, A. rubi from Watson Glen Park, Chilliwack, British Columbia, Canada; C and D, A. corvulus from Spruce Woods National Park, Manitoba, Canada; E and F, A. nigrinus from La Porte County, Indiana, United States of America; and G and H, A. signatus from Dawson Creek, British Columbia.

Figure 1

Fig. 2. A, Damage caused by adult female Anthonomus rubi to Himalayan blackberry (Rubus armeniacus), including severing of the pedicel and oviposition hole; B, adult A. rubi inside an open strawberry (Fragaria sp. Linnaeus) blossom. Photos by Warren Wong, University of British Columbia, Vancouver, British Columbia, Canada.

Figure 2

Fig. 3. Map of locations where Anthonomus rubi was found associated with various host plants in British Columbia, Canada in 2020, indicated with coloured points. Some points are displaced slightly for clarity. The red box within the inset (upper right) shows the surveyed region within North America. Map tiles by Stamen Design, CC BY 3.0; data by OpenStreetMap, open database licence.

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