Trialeurodes abutiloneus (Haldeman) (Hemiptera: Aleyrodidae) is a whitefly that has been recorded from South America, Iran, and the United States of America (including Hawaii) (Evans Reference Evans2008; Russell Reference Russell1963). Based on available literature, the northernmost limit of the distribution of this whitefly in North America is southern New York and Michigan, United States of America. It is also known to occur at latitudes >45° north in the northwestern United States of America where it is known to overwinter on potato (Solanum tuberosum Linnaeus; Solanaceae) (Landis and Getzendaner Reference Landis and Getzendaner1947). In that range, T. abutiloneus is a generalist, recorded to feed on plant species from 33 plant families (Russell Reference Russell1963; Slosser et al. Reference Slosser, Parajulee, Idol and Hendrix2005; Evans Reference Evans2008) including important crops such as Glycine max (Linnaeus) Merrill (Fabaceae) (soybean), Ipomoea batatas (Linnaeus) Lamarck (Convolvulaceae) (sweet potato), Gossypium Linnaeus (Malvaceae) (cotton), and Solanum Linnaeus (Solanaceae) (tomato) (Jones et al. Reference Jones, Clower, Milam, Caldwell and Melvill1975; Liu and Stansly Reference Liu and Stansly2000). In soybean crops, T. abutiloneus is usually found co-occurring with Bemisia tabaci (Gennadius) (Hemiptera: Aleyrodidae) (Lambert et al. Reference Lambert, McPherson and Herzog1997). In Canada, T. abutiloneus can potentially be found on host plants belonging to 22 families (Table 1).
Table 1 Potential host range of Trialeurodes abutiloneus in Canada based on host range from Evans (Reference Evans2008) superimposed onto the presence of the plant species in Canada (Vascan database: http://data.canadensys.net/vascan/search?lang=en).
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Trialeurodes abutiloneus has never been officially recorded in the literature as occurring in Canada, although archival specimens have been collected by R.J. McClanahan from Harrow, in southwestern Ontario, Canada dating back to September 1973. These insects were collected from velvet leaf, Abutilon theophrasti Medikus (Malvaceae), hosts. Recently, new specimens have been collected from the same region, again at the Harrow Research and Development Centre, in October to November 2016. This note therefore represents the first verifiable (morphological and molecular) published record of this species in Canada. A large population of T. abutiloneus was found on greenhouse soybean plants (Fig. 1). Seeing that individuals of this species have previously been recorded from southern Michigan and New York (Russell Reference Russell1963), this species can be assumed to be well adapted to climatic conditions in southwestern Ontario, which are on the same latitude as Michigan and New York.
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Fig. 1 Distribution of Trialeurodes abutiloneus nymphs and pupae on the underside of a soybean leaf. Circled individual is parasitised.
Adults are easily recognised morphologically due to a clear, black, zigzagging pattern on the wing (Fig. 2). Late instars and pupae of T. abutiloneus also closely resemble those of congeneric species including their typical top flattened oval shape as well as the production of a waxy peripheral fringe. They can be distinguished from other species by their cream colour and the presence of variably shaped dark dorsal blots along the midline of their body (Fig. 3). As with Trialeurodes vaporariorum Westwood that are parasitised by Encarsia formosa Gahan (Hymenoptera: Aphelinidae), we have noted the presence of entirely black pupal bodies of T. abutiloneus that hosted this parasitoid (Fig. 1: second instar from right side of image).
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Fig. 2 Adult Trialeurodes abutiloneus.
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Fig. 3 Nymphs and pupae of Trialeurodes abutiloneus.
We sequenced the cytochrome oxidase I barcode region of T. abutiloneus specimens in order to confirm its identity. Briefly, DNA was extracted from an adult whitefly using the Chelex extraction method (Walsh et al. Reference Walsh, Metzger and Higuchi1991). We amplified the barcode region using universal insect primers (LCO1490-F: 5'-GGTCAACAAATCATAAAGATATTGG-3'; HCO2198-R: 5'-TAAACTTCAGGGTGACCAAAAAATCA-3') (Folmer et al. Reference Folmer, Black, Hoeh, Lutz and Vrijenhoek1994) and the following thermal cycling condition: denaturation at 94 °C for one minute; followed by five cycles of 94 °C for 40 seconds, 45 °C for 40 seconds, and 72 °C for one minute; followed by 35 cycles of 94 °C for 40 seconds, 51 °C for 40 seconds, 72 °C for one minute, with a final extension at 72 °C for five minutes. Our resulting sequence (MG817067) nearly completely matched sequences available in GenBank (http://www.ncbi.nlm.nih.gov/genbank) and the Barcode of Life Datasystem (BOLD - http://www.boldsystems.org) listed as unidentified Aleyrodidae species. DNA barcoding of our collected specimens also allowed us to determine that this species has been collected from a cactus field in Point Pelee National Park, Ontario, Canada in 2012 (BOLD Sample ID: BIOUG03903-A02) suggesting that this species is mostly likely established in southwestern Ontario.
Trialeurodes abutiloneus is recognised as a pest and can vector for many plant viruses. In the United States of America, T. abutiloneus has also been recorded to occur on cotton (Clower et al. Reference Clower, Watve, Melville and Graves1971). It has also been recorded to transmit Crinivirus (Closteroviridae) (sweet potato chlorotic stunt virus) to sweet potatoes (Valverde et al. Reference Valverde, Sim and Lotrakul2004) and Abutilon yellows virus (Crinivirus; Closteroviridae) to other crops (Liu et al. Reference Liu, Li, Wisler and Duffus1997). In the case of Abutilon yellows, T. abutiloneus is known to retain the virus for up to three days suggesting that an infected individual can have a lasting impact on a crop (Wisler and Duffus Reference Wisler and Duffus2001). It is also known to vector Crinivirus such as blackberry yellow vein associated virus, diodia vein chlorosis virus, and tomato chlorosis virus (Tzanetakis et al. Reference Tzanetakis, Martin and Wintermantel2013). Records also show this species vectoring multiple viruses of the genus Torradovirus (Secoviridae) including the tomato marchitez virus, the tomato torrado virus, and the tomato chocolàte virus that are restricted to Mexico (Verbeek et al. Reference Verbeek, van Bekkum, Dullemans and van der Vlugt2014). Each of these viruses are known to infect Solanum plant species and have the potential to cause significant crop losses attributed to leaf necrosis and patches on fruits (Verbeek et al. Reference Verbeek, van Bekkum, Dullemans and van der Vlugt2014). Together, the viruses transmitted by T. abutiloneus can negatively impact multiple crop types and therefore we suggest the development of a monitoring programme for this whitefly species.
Little is known about the biological control of T. abutiloneus however some Aphelinidae (Hymenoptera) parasitoid species (Encarsia Förster and Eretmocerus Haldeman) have been shown to successfully parasitise T. abutiloneus (Dysart Reference Dysart1966; Watve and Clower Reference Watve and Clower1976; Polaszek et al. Reference Polaszek, Manzari and Quicke2004; Evans Reference Evans2008; Greenberg et al. Reference Greenberg, Jones and Liu2009; Pickett et al. Reference Pickett, Keaveny and Rose2013) (Table 2). Encarsia lutea (Masi) and Encarsia pergandiella Howard are listed among these species (Gerling Reference Gerling1967; Rivnay and Gerling Reference Rivnay and Gerling1987). In the context of our observations, we have also extracted DNA from a parasitised T. abutiloneus whitefly and amplified its COI barcode gene using the same protocol as described for the whitefly. This parasitoid shared 99% identity with E. formosa as molecularly identified in GenBank and BOLD (MG817066). There is also an entomopathogenic fungus, Orthomyces aleyrodis Steinkraus, Humber, and Oliver (Entomophthoraceae) that has been shown to control this species (Steinkraus et al. Reference Steinkraus, Oliver, Humber and Gaylor1998), and it would be likely that entomopathogens such as Beauveria bassiana (Balsamo-Crivelli) (Clavicipitaceae) commonly used to control T. vaporariorum, would also infect this species. Finally, generalist predators such as Coccinellidae (Coleoptera), Hemiptera, Neuroptera, and Arachnida are also known to prey readily on this species (Watve and Clower Reference Watve and Clower1976; Evans Reference Evans2008). These include the adults of Spanagonicus albofasciatus (Reuter) (Hemiptera: Miridae), which was shown to lower per cent survival of eggs and adults of T. abutiloneus to 3–5% after two to three days in cages with the predator (Butler Reference Butler1961) (Table 2).
Trialeurodes abutiloneus is a species that has not officially been recorded from Canada although it has surely been established for at least 40 years based on collections from McLanahan at the Harrow Research and Development Centre (Agriculture and Agri-Food Canada), the Barcode of Life collection in Pointe Pelee National Park, and our own in 2016. It has been a nuisance in the United States of America in cotton and sweet potato crops but we cannot consider it an important pest in Canada. A few potential reasons why T. abutiloneus has not caused any noticeable damage may be that it is a generalist that does not need to survive on specific crops, that the population size is controlled because of a number of natural enemy species, and that it is outcompeted by closely related species. However, the distribution of this species in Canada still remains unclear and we urge that time be taken for the identification of whiteflies from historical and collection of new ecological and agricultural samples so that we can gain a better understanding of this species in North America.
Table 2 Records of the natural enemies of Trialeurodes abutiloneus.
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Acknowledgements
The authors thank George Driedger and Dr. Owen Wally for bringing the specimens to our attention and Dana Gagnier for photographing the adult. The sequencing was performed by R.M.L.