Introduction
The province of Québec is the largest producer of strawberries (Fragaria x ananassa Duchesne ex Rozier; Rosaceae) in Canada, with 57% of the production in the country on 1700 ha in 2016, and ranks third in North America, after California and Florida, United States of America (Ministère de l’Agriculture, des Pêcheries et de l’Alimentation et Institut de la statistique du Québec 2018). Most commercial strawberry growers in Québec manage their crops using the conventional matted row system, under which production lasts two or three years (Hancock et al. Reference Hancock, Goulart, Luby and Pritts1997). Every summer, plants are mowed immediately after harvest in order to eliminate the old leaves infested with diseases, stimulate the proliferation of runners (stolons) and fruit buds, and promote a bountiful yield the following year (Thireau and Lefebvre Reference Thireau and Lefebvre2014).
Strawberry decline disease has become a severe issue for growers worldwide (Tzanetakis and Martin Reference Tzanetakis, Martin, Zhang and Maas2014). Serious damage has been sustained by matted row strawberry fields of Québec between 2012 and 2014 (Lambert et al. Reference Lambert2014). Symptoms include a reduction of runners produced by the plant, a weakened root system, and failure to thrive after planting. One outcome is plant death, which represents an economic loss to the growers. The predominant causal factor of this worldwide disease is infection by two or more strawberry viruses (Martin and Tzanetakis Reference Martin and Tzanetakis2013).
As of now, the only known vector of Strawberry pallidosis virus (SPaV) (Crinivirus: Closteroviridae) is the greenhouse whitefly, Trialeurodes vaporariorum (Westwood) (Hemiptera: Aleyrodidae) (Tzanetakis et al. Reference Tzanetakis, Martin and Wintermantel2014). Only a few whitefly species have been documented as colonisers of commercial strawberry plants in the United States of America and Canada: Aleyrodes spiraeoides (Quaintance), Trialeurodes packardi (Morrill), Trialeurodes fernaldi (Morrill), and Trialeurodes ruborum (Cockerell) (Evans Reference Evans2008). Other sources have reported the presence of Trialeurodes abutiloneus (Haldeman) and the sweetpotato whitefly, Bemisia tabaci (Gennadius) biotype B (Tzanetakis et al. Reference Tzanetakis, Wintermantel, Cortez, Barnes, Barrett, Bolda and Martin2006) in strawberry fields. Surprisingly, the most recent strawberry crop profile does not identify T. vaporariorum as an insect pest in commercial strawberry fields in Canada (Agriculture and Agri-Food Canada 2015), similar to the local lists in Québec (Lambert et al. Reference Lambert, Laplante, Carisse and Vincent2007). Still, many studies have demonstrated that whiteflies do pose a risk to strawberry crop (e.g., Martin and Tzanetakis Reference Martin and Tzanetakis2006, Reference Martin and Tzanetakis2013; Tzanetakis et al. Reference Tzanetakis, Wintermantel, Cortez, Barnes, Barrett, Bolda and Martin2006; Tzanetakis and Martin Reference Tzanetakis and Martin2013). However, in the province of Québec, there is limited published information on whiteflies. Officially, the only known database for Hemiptera insects in Canada, which currently contains more than 3900 species (Maw et al. Reference Maw, Foottit, Hamilton and Scudder2000), reported three species for the province, Trialeurodes vaporariorum, Trialeurodes packardi, and an uncertain mention of Aleyrodes asumaris Shimer. There is no available information concerning the flight period of any whitefly species in Québec.
The main vector of Strawberry mild yellow edge virus (Potexvirus; Alphaflexiviridae), Strawberry mottle virus (Secoviridae), Strawberry crinkle virus (Cytorhabdovirus; Rhabdoviridae), and Strawberry vein banding virus (Caulimovirus; Caulimoviridae) is the strawberry aphid, Chaetosiphon fragaefolii (Cockerell) (Martin and Tzanetakis Reference Martin and Tzanetakis2006). However, many aphid species can be present in strawberry fields, either as colonisers or as errants (Stultz Reference Stultz1968). Among them, Rhodobium porosum (Sanderson), Myzus persicae (Sulzer), Aulacorthum solani (Kaltenbach), Amphorophora rubi (Kaltenbach), Aphis gossypii Glover, and Chaetosiphon Huber species (Hemiptera: Aphididae) may transmit strawberry viruses as well (Craig and Stultz Reference Craig and Stultz1964; Tzanetakis and Martin Reference Tzanetakis and Martin2013).
Among the viruses responsible for the strawberry decline disease, there are two different transmission modes: semi-persistent and persistent (circulative and/or propagative) (Sylvester Reference Sylvester, Minks and Harrewijn1989). The semi-persistent viruses such as Strawberry mottle virus, Strawberry vein banding virus, and Strawberry pallidosis virus are acquired quickly by the insects and located in their stylet for a few hours (Watson and Plumb Reference Watson and Plumb1972). Since the semi-persistent virus is only present in the stylet of the vector, the vector-virus specificity is thereby moderate, which indicates that other aphid species could transmit these viruses as well (Andret-Link and Fuchs Reference Andret-Link and Fuchs2005; Pelletier et al. Reference Pelletier, Nie, Giguère, Nanayakkara, Maw and Foottit2012). However, the circulative persistent viruses such as Strawberry mild yellow edge virus are acquired during feeding, circulating into the body for several days without replicating inside the insect. The circulative propagative persistent viruses such as Strawberry crinkle virus are also acquired during feeding, circulating in the body and replicating inside the insect for a few weeks or the lifetime of the aphid (Gray and Banerjee Reference Gray and Banerjee1999). Since sustained feeding is necessary for the acquisition of persistent virus, the number of vector species is very limited. Due to its high virus-vector specificity, C. fragaefolii is believed to be the only known vector of Strawberry mild yellow edge virus and Strawberry crinkle virus (Sylvester Reference Sylvester1980; Andret-Link and Fuchs Reference Andret-Link and Fuchs2005).
Over the complex life cycle of aphids, the alate form occurs depending on the crowding conditions, the nutritional quality of the host plant (Wadley Reference Wadley1923), the temperature and photoperiod, or when conditions for growth are optimal (Kawada Reference Kawada, Minks and Harrewijn1987). It can also be induced by the presence of natural enemies and pathogens (Irwin et al. Reference Irwin, Kampmeier, Weisser, van Emden and Harrington2007). Throughout the strawberry growing season, most winged aphids emerge, including C. fragaefolii. The winged morph is adapted for dispersion over great distances, being carried by the wind to other strawberry fields (Dixon and Kindlmann Reference Dixon and Kindlmann1999). Moreover, the probing behaviour of alate aphids during host selection involves intensive probing activity with several plants in one feeding bout (Klingauf Reference Klingauf, Minks and Harrewijn1987; Boquel Reference Boquel2011). These features play a key role in the spread of viruses and the effectiveness of winged aphids as virus-vectors. The presence of C. fragaefolii in strawberry fields often coincides with high virus incidence in these same fields (Lavandero et al. Reference Lavandero, Rojas, Ramirez, Salazar and Caligari2012). There is currently no available information on the flight period of C. fragaefolii in Québec. However, a report published by Lewis (Reference Lewis2013) indicates that the flight period of C. fragaefolii in western Nova Scotia, Canada, is set from the beginning of June until the end of July.
The most common and relatively inexpensive trapping techniques to monitor the flight activity of insects are the combined interception and attraction traps: pan traps and sticky traps (Mukhopadhyay Reference Mukhopadhyay2011). As part of an effort to better understand the strawberry decline problem, yellow sticky traps were used in Nova Scotia to record flight periods of winged C. fragaefolii (Lewis Reference Lewis2013). Pelletier et al. (Reference Pelletier, Nie, Giguère, Nanayakkara, Maw and Foottit2012) used yellow pan traps filled with propylene glycol (40–60%) to conserve the RNA of the potato virus Y from the captured aphids. The success of these two types of trapping techniques comes from the yellow colour, which is very attractive to many insects, including aphids and whiteflies (Eastop Reference Eastop1955; Berlinger Reference Berlinger1980). In order to measure the seasonal variation in the abundance of winged virus-vectors, yellow pan traps and yellow sticky traps seem to be appropriate methods.
Our overall goals undertaking this study were to mitigate the very limited information available on virus-vectors present in strawberry fields, as well as helping agronomists and strawberry growers in Québec. Specifically, objectives were to (1) compare the effectiveness of sticky traps and pan traps in monitoring C. fragaefolii and T. vaporariorum in strawberry fields; (2) determine the flight peak of these two vectors; and (3) document aphid and whitefly population and species diversity in commercial strawberry fields.
Materials and methods
Trapping technique comparison
Two monitoring techniques for capturing aphids and whiteflies as vectors of strawberry viruses were evaluated: yellow sticky traps and yellow pan traps. The yellow sticky traps were recycled polyvinyl chloride and sticky on both faces (Bug-Scan Dry; Biobest, Ilse Velden, Belgium). The glue was non-toxic, waterproof, and did not dry out (Bug-Scan Dry, Biobest 2016). The trap measured 25 cm × 10 cm, for a total surface of 250 cm2. The sticky traps were hooked on two metal stakes to remain stable in the fields. Yellow pan traps were set up following the collecting protocol used to monitor aphid flight in Nova Scotia (D. Moreau, Agriculture and Agri-Food Canada, Kentville, Nova Scotia, Canada, personal communication). Stainless steel bowls were painted matte yellow, using Rust-Oleum (Painter’s Touch 2X Ultra Spray Paint number 253712; Vernon Hills, Illinois, United States of America). Bowls were 19.7 cm in diameter and 6 cm deep for a surface of 305 cm2. Pan traps were filled twice a week with propylene glycol solution (55–70% propylene glycol mixed with water) using the protocol described in Pelletier et al. (Reference Pelletier, Nie, Giguère, Nanayakkara, Maw and Foottit2012). Propylene glycol concentration was higher because of evaporation in the fields. An individual bowl was hooked on to a modified tomato cage to remain stable in the fields.
Experimental setting
Strawberry fields were selected in the following localities: Portneuf (46.77541°N, 71.64213°W), Côte-de-Beaupré (46.91502°N, 71.10600°W), Ⓘle d’Orléans (46.86277°N, 71.04923°W), St-Nicolas (46.68881°N, 71.45499°W), Beauce (46.41925°N, 70.97209°W), and Bellechasse (46.74127°N 70.92041°W), for a total of six fields. In both years (2014 and 2015), each field measured 1 ha and was in the first year of production using a conventional matted row system. Ten sticky traps and 10 pan traps were placed in a single corner in each field, with a 1 m distance between traps. The corner was chosen according to the prevailing wind direction. From 23 June to 25 August 2014 and 22 June to 24 August 2015, sticky traps were collected once a week and pan traps were collected twice a week. When collected, sticky traps were wrapped in plastic wrap. For pan traps, a strainer was used to empty the specimens in Whirl-pack Nasco bags (Fort Atkinson, Wisconsin, United States of America) and 95% ethanol was added for preservation. Samples were carried to the laboratory on ice packs and then placed in a refrigerator until processing. Abundance counts and identification of C. fragaefolii aphid and whitefly specimens were performed using a stereomicroscope and based on morphological characteristics described in Foottit and Richards (Reference Foottit and Richards1993) and Brisson (Reference Brisson2015). For the purpose of this objective, alate aphids were sorted as C. fragaefolii or “other species,” and all the whiteflies species were combined.
Statistical analysis
Counts of winged aphids across time were analysed using a generalised randomised block analysis of variance model with repeated measures. In order to deal with the overdispersed count outcome variables, the negative binomial distribution was chosen with a log link function. The experimental unit at each site was a group of 4–10 traps, depending on the number of traps recovered. There were 12 experimental units for each type of traps, as there were six strawberry fields for two years. Since the number of traps was not constant, this variable was used as an offset in the model in the log scale. The fixed effects were the type of traps (pan traps versus sticky traps) and the dates, while the random effects were the sites. The total catch of winged aphids for the season was also analysed using a similar approach, but this time without repeated measurements. Analyses were done using the Glimmix procedure of SAS (release 9.4; SAS Institute, Cary, North Carolina, United States of America). Following significant effects in the analysis of variance table, protected least significant difference multiple comparisons were done to evaluate the differences between the average counts. All analyses were made at the α = 0.05 level of significance.
Flight activity of vectors in Québec
Seventeen sites throughout the province of Québec were selected for the vector flight activity measurements for both C. fragaefolii and whitefly species using yellow sticky traps as described above. These sites included one strawberry field in each site: Gaspésie (48.07317°N, 65.58967°W), Bas-Saint-Laurent (47.90776°N, 69.43342°W), Lac Saint-Jean (48.48722°N, 72.30742°W), Portneuf (46.77541°N, 71.64213°W), Côte-de-Beaupré (46.91502°N, 71.10600°W), Ⓘle d’Orléans (46.86277°N, 71.04923°W), St-Nicolas (46.68881°N, 71.45499°W), Beauce (46.41925°N, 70.97209°W), Bellechasse (46.74127°N 70.92041°W), Laurentides (45.59260°N, 73.92252°W), Lanaudière (45.90888°N, 73.35410°W), Mauricie (46.55323°N, 72.21815°W), Outaouais (45.56983°N, 75.45687°W), Montérégie Est (45.70113°N, 72.95870°W), Montérégie Ouest (45.21296°N, 73.64083°W), Estrie (45.44158°N, 72.00257°W), and Centre-du-Québec (46.08587°N, 72.83665°W). For 2014 and 2015, each field had a surface area of 1 ha, and was in the first or second year of production using a conventional matted row system. Five sticky traps were placed in one corner of each field, with a distance of 1 m between traps. The corner was chosen according to the prevailing wind direction. From 26 May to 27 October 2014 and 25 May to 26 October 2015, sticky traps were collected once a week and wrapped in plastic wrap. Traps were promptly shipped to V.F.’s laboratory at Laval University and placed in a refrigerator at 4 °C upon arrival. Abundance counts and identification of C. fragaefolii aphid and whitefly specimens were performed using a stereomicroscope and based on the morphological characteristics described in Foottit and Richards (Reference Foottit and Richards1993) and Brisson (Reference Brisson2015). Again, for the purpose of this part of the study, alate aphids were sorted as either C. fragaefolii or “other species” and all whitefly species were combined.
Abundance and diversity of whiteflies and aphids in selected strawberry fields
Data on the abundance and diversity of whiteflies were obtained by counting the specimens caught from 25 May to 26 October 2015 on the yellow sticky traps used at the 17 sites described previously. Specimens were identified under stereomicroscope based on morphological characteristics (Brisson Reference Brisson2015) and identification was validated by J.D.B.
The abundance of aphid species and genera reported in this paper was measured by collecting the aphids caught in yellow pan traps as described above. Three sites, located in St-Nicolas (46.68881°N, 71.45499°W), Portneuf (46.77541°N, 71.64213°W), and Ⓘle d’Orléans (46.86277°N, 71.04923°W), were selected for the survey of aphid species and genera. We selected these fields due to the reduced number of overall pesticide applications that prevailed in them. Trap setup and collection methods were as previously outlined under Experimental setting for Trapping technique comparison sections. Once collected from the field, aphids were sorted and then mounted on microscope slides in Canada balsam, according to an established protocol (Maw Reference Maw1999). A total of 203 mounted specimens were identified under the stereomicroscope based on morphological characteristics (MacGillivray Reference MacGillivray1979; Quednau Reference Quednau1985; Foottit and Richards Reference Foottit and Richards1993; Gualtieri and McLeod Reference Gualtieri and McLeod1994). Identifications were validated by taxonomist Eric Maw (Canadian National Collection of Insects, Arachnids, and Nematodes, Ottawa, Ontario, Canada). Voucher specimens from our study are stored in the Fournier Laboratory in the Phytology Department at the Université Laval (Ville de Québec, Québec, Canada).
Results
Trapping technique comparison
Yellow sticky traps were more effective in capturing alate aphids compared to yellow pan traps (F = 173.29; df = 1, 11; P < 0.0001) (Fig. 1A). The mean of the total captures, all sites combined, was 24.0 ± 5.8 aphids (mean ± standard error) per pan trap, while it was 133.2 ± 32.4 aphids per sticky trap. Yellow sticky traps were more effective in capturing C. fragaefolii specimens than pan traps (F = 21.04; df = 1, 11; P = 0.0008), even though the numbers were very low (Fig. 1B). The mean of the total catch, all sites combined, was 0.9 ± 0.2 C. fragaefolii per pan trap, while it was 1.8 ± 0.4 C. fragaefolii per sticky trap. No whitefly was captured in pan traps in 2014 or 2015. Therefore, no comparison was made between the two types of traps for this taxon.
Fig. 1. Mean (± standard error) total captures in pan traps and sticky traps, for both years and for all six sites combined. * indicates significant (P < 0.05) difference between the two traps. A, Alate aphids; B, alate Chaetosiphon fragaefolii.
Fig. 2. Mean (± standard error) total captures of insect vectors per year in yellow sticky traps from 26 May to 27 October 2014 and from 25 May to 26 October 2015 at 17 sites. A, Whitefly flight peak by year; B, Chaetosiphon fragaefolii flight peak by year.
Flight activity of vectors across Québec
In 2014, the highest count per trap was 4.2 ± 2.2 whiteflies, captured in mid-September, while there was a peak of 56.6 ± 36.9 whiteflies per trap at the end of September in 2015 (Fig. 2A). Based on this, the highest abundance of whiteflies was observed near the end of the growing season, although whiteflies were usually present throughout the entire season, from the end of May until the end of October in both years. As for C. fragaefolii, there was a peak of 0.5 ± 0.1 per trap in mid-August 2014, and 0.7 ± 0.3 per trap around the same time in 2015 (Fig. 2B). They were mostly present from early June to the end of September, with a recurrence in mid-October in both years.
Abundance and diversity of whiteflies and aphids in selected strawberry fields
Two different species of whiteflies were identified: Trialeurodes vaporariorum and Aleyrodes spiraeoides (Table 1). The highest number of T. vaporariorum was found in the Lanaudière region, with 1398 individuals. Aleyrodes spiraeoides was the most abundant in St-Nicolas, with 88 individuals. Trialeurodes vaporariorum represents 96% of all the catches; and Aleyrodes spiraeoides, 4%.
Table 1. Total seasonal counts of whitefly species per site, captured in yellow sticky traps from 25 May to 26 October 2015 at 17 sites.
A total of 1595 specimens were captured, representing 35 different genera and over 53 species (Table 2). The 10 most abundant species were: Aphis Linnaeus species (764); Hayhurstia atriplicis (Linnaeus) (239); pea aphid, Acyrthosiphon pisum Harris (123); Aphis glycines Matsumura (98); green peach aphid, Myzus persicae (Sulzer) (54); mustard aphid, Lipaphis pseudobrassicae (Davis) (43); yellow clover aphid, Therioaphis trifolii (Monell) (39); strawberry aphid, Chaetosiphon fragaefolii (Cockerell) (24); Macrosiphum Passerini species (21); and Amphorophora agathonica (Hottes) (20).
Table 2. Total seasonal counts of aphid species or genera captured in yellow pan traps from 23 June to 27 October 2014 at three sites combined.
Discussion
In the context of the strawberry decline disease, the management of viruses begins with managing the winged form of the virus-carrying insects. Our aim was, therefore, to gather new and crucial information on the population dynamics by identifying the flight activity of C. fragaefolii and T. vaporariorum, throughout the province of Québec, using an efficient monitoring technique. Consequently, the main goal of this study was to compare commonly used methodologies: (1) yellow sticky traps, as used in Nova Scotia to monitor the flight activity of C. fragaefolii (Lewis Reference Lewis2013); and (2) yellow pan traps, as used in New Brunswick, Canada, to monitor aphid vectors of potato virus Y in potato fields (Pelletier et al. Reference Pelletier, Nie, Giguère, Nanayakkara, Maw and Foottit2012). Results presented above contribute additional knowledge of species composition and peaks in flight period, as well as the relative effectiveness of the yellow sticky trap technique.
Trapping technique comparison
The analysis of variance results demonstrate that the yellow sticky traps are by far the most efficient trapping technique for all species of aphids found in strawberry fields combined, as they collected the highest number of insects (Fig. 1). This further confirms previous findings that sticky traps are very effective in measuring the relative abundance of aphids (A’Brook Reference A’Brook1973; Harrington et al. Reference Harrington, Hullé, Plantegenest, van Emden and Harrington2007). Sticky traps are also very easy to use, as they require less equipment and manipulation compared to pan traps. In contrast, one of the disadvantages of using sticky traps is that the identification of aphid species can be difficult because the specimens are stuck to the trap and sometimes in poor condition, as key taxonomic characteristics can often be obscured and damaged.
With regard to the monitoring of C. fragaefolii, statistical analysis indicated a significant difference between the trap type, with the yellow sticky traps being the most effective. However, although statistically significant, the actual difference between capture numbers of C. fragaefolii was 0.9. The overall low captures of C. frageafolii likely impacted the analyses. Our results pointed out that the numbers of the winged form of C. fragaefolii were much lower than winged form of other aphids (Fig. 1), similar to what was found in yellow sticky traps in Nova Scotia (Lewis Reference Lewis2013). It appears typical to encounter fewer populations of winged C. fragaefolii compared with other winged aphid species. However, the numbers of wingless C. fragaefolii are probably much higher than winged C. fragaefolii inside the fields, on the plants, as Lewis (Reference Lewis2013) demonstrated by sampling leaves.
Several studies using yellow pan traps have shown their effectiveness in capturing high numbers of aphids in general (Labonne et al. Reference Labonne, Lauriaut and Quiot1989; Avinent et al. Reference Avinent, De Mendoza and Llácer1991) as well as C. fragaefolii (O’Loughlin Reference O’Loughlin1963). Aphids are easier to identify when captured with pan traps, as their morphological characteristics would remain intact in liquid. This allowed us to mount the captured specimens on Canada balsam microscope slides for easier identification (Maw Reference Maw1999). One inconvenience observed in the field was that bowls sometimes dried out in the hot summer weather, a problem also reported by Harrington et al. (Reference Harrington, Hullé, Plantegenest, van Emden and Harrington2007).
Little research has been conducted to compare these two methods directly in the field. The first documented user of pan traps for catching aphids, Moericke (Reference Moericke1951), experimented with different coloured traps to identify which was attracting the highest number of insects. Other studies compared cylindrical and flat sticky traps (Broadbent Reference Broadbent1948, Reference Broadbent1957). Both trap types are considered effective in capturing winged C. fragaefolii and other aphid species that visit strawberry plants, as both are the most frequently used methods worldwide (Mukhopadhyay Reference Mukhopadhyay2011). Nonetheless, when we compared both techniques, our results were quite different from studies that compared yellow Moericke-style pan traps and Broadbent-style yellow flat sticky traps (Heathcote Reference Heathcote1957; O’Loughlin Reference O’Loughlin1963), in which the number of aphids caught in yellow pan traps was much higher than the number of aphids caught on sticky traps.
Based on our fieldwork, sticky traps would seem to be the most efficient trapping technique to capture whiteflies, since no whitefly has been caught in pan traps during the two growing seasons of this study. This result is similar to conclusions drawn in other studies: sticky traps are very effective in detecting whitefly populations and measuring population dynamics (Ohnesorge and Rapp Reference Ohnesorge and Rapp1986; Gillespie and Quiring Reference Gillespie and Quiring1987).
Since the presence of C. fragaefolii coincides with the presence of strawberry viruses (Lavandero et al. Reference Lavandero, Rojas, Ramirez, Salazar and Caligari2012) and the presence of T. vaporariorum coincides with the presence of Strawberry pallidosis virus (Tzanetakis et al. Reference Tzanetakis, Wintermantel, Cortez, Barnes, Barrett, Bolda and Martin2006), trapping using sticky traps in order to monitor flight activity of the winged vectors will continue to provide important knowledge for agronomists and strawberry growers across the province of Québec.
Flight activity of vectors across Québec
The winged forms of virus-carrying insects navigate using their olfactory sense (Pickett et al. Reference Pickett, Wadhams, Woodcock and Hardie1992). Thus, thousands of winged aphids can land on a random strawberry field (Perring et al. Reference Perring, Gruenhagen and Farrar1999). Knowledge of the flight activity of known vectors in Québec strawberry fields is essential to control the spread of viruses, as flight peaks correspond to virus transmission peaks.
The flight peak of whiteflies in the province of Québec occurs around the last two weeks of September, though it slightly differs across geographic regions (Fig. 2A). A significantly higher number of whiteflies (over 14 times higher) was documented in 2015 compared to the same period in 2014. There are various possible reasons why whiteflies have a flight peak. Trialeurodes vaporariorum are likely to exit greenhouse structures at the end of the summer after the crops have been harvested (Lambert et al. Reference Lambert2014). It is also possible that nearby fields were being or had just been harvested, as tillage or mowing can provoke insect flights in large numbers (Gencsoylu and Yalcin Reference Gencsoylu and Yalcin2004).
Our results showed that the main flight peak of C. fragaefolii in Québec was around the first two weeks of August, though this slightly varied from one region to another. In 2015, the flight period seemed to have lasted longer than in 2014. This could be explained by temperatures during the 2015 growing season, which were warmer early and later in the season as compared to 2014 (The Weather Network 2015). In addition, spring of 2014 was quite cold with recorded precipitations above normal across the province (The Weather Network 2014). A second, smaller flight peak at the end of the season could be explained by winged male production in autumn for sexual reproduction (Williams and Dixon Reference Williams, Dixon, van Emden and Harrington2007), and also the senescence of the host plants and shorter day lengths, leading to aphids developing wings and leaving the fields (Wadley Reference Wadley1923; Kawada Reference Kawada, Minks and Harrewijn1987).
The flight peaks of C. fragaefolii occurred earlier in western Nova Scotia (Lewis Reference Lewis2013) than was identified in Québec. This could be due, in part, to the warming influence of the marine climate and slightly higher mean maximum temperatures, measured in Kentville, Nova Scotia, for the same years.
Abundance and diversity of whiteflies and aphids in selected strawberry fields
Regarding the whitefly survey, two species were captured: the greenhouse whitefly, Trialeurodes vaporarorium, and a new distribution record for the province of Québec, the iris whitefly, Aleyrodes spiraeoides. Interestingly, the distribution of these two species of whiteflies in commercial strawberry fields of various regions of Québec was not initially suspected. According to Brisson (Reference Brisson2014), A. spiraeoides was observed in Québec in 2001, though it has since gone unnoticed until now and even confused with T. vaporariorum, which is better known. Both species are active at temperatures as low as 8 °C (Landis et al. Reference Landis, Gibson and Schopp1958; van Roermund and van Lenteren Reference van Roermund and van Lenteren1992). They therefore appear very early in the season, feeding and breeding on a very large number of plants, including wild strawberry plants – Fragaria chiloensis Linnaeus and Fragaria virginiana Miller (Landis et al. Reference Landis, Gibson and Schopp1958; McClanahan Reference McClanahan1979; Tzanetakis et al. Reference Tzanetakis, Wintermantel, Cortez, Barnes, Barrett, Bolda and Martin2006). Although A. spiraeoides represents only 4% of all catches in Québec strawberry fields, it is considered an emerging pest in strawberry fields in California, United States of America (Zalom et al. Reference Zalom, Phillips, Toscano and Bolda2005). Curiously, Trialeurodes packardi reported in the database for Hemiptera insects in Canada (Maw et al. Reference Maw, Foottit, Hamilton and Scudder2000) was not captured.
The number of described genera and species of whiteflies worldwide has increased dramatically in the recent years and is undoubtedly underestimated (Martin and Mound Reference Martin and Mound2007; Evans Reference Evans2008). The whiteflies of Québec are no exception. An unofficial list from various sources was recently initiated by Entomofaune du Québec (2018), including some observed species such as Trialeurodes abutiloneus (Lambert Reference Lambert1999), Aleurochiton forbesii (Ashmead) (Claude Pilon, Repentigny, Québec, Canada, unpublished data, personal communication), and Aleyrodes proletella (Linnaeus) (Brisson Reference Brisson2015). A more exhaustive research with field sampling should be considered to obtain a precision of the number of all the whitefly species present and established in Québec.
A comprehensive survey of all aphids present in strawberry fields in Québec has never been conducted. Since virus-vector specificity is not as strong for semi-persistent viruses as for persistent viruses, many different and, as yet, unknown species could certainly transmit semi-persistent strawberry viruses (Andret-Link and Fuchs Reference Andret-Link and Fuchs2005; Pelletier et al. Reference Pelletier, Nie, Giguère, Nanayakkara, Maw and Foottit2012). Thus, our aim was to identify which aphid species may be pests in strawberry crop in the province of Québec.
The aphid survey we conducted in strawberry fields using yellow pan traps was done on three different sites located in the region of the greater area of Ville de Québec. It documented the presence of at least 53 different species of winged aphids (Table 2). Among them, Aphis was the most abundant genus. Some species found in our pan traps are potential vectors of strawberry viruses, such as Myzus persicae, Aphis gossypii, and different species of Chaetosiphon (Craig and Stultz Reference Craig and Stultz1964; Tzanetakis and Martin Reference Tzanetakis and Martin2013).
Moreover, we did find 20 specimens of Amphorophora agathonica, which is an important vector of the red raspberry and black raspberry (Rubus Linnaeus; Rosaceae) viruses (Lightle et al. Reference Lightle, Quito-Avila, Martin and Lee2014). Interestingly enough, this aphid species is noted to be monoecious, and Rubus is its only known host (Blackman and Eastop Reference Blackman and Eastop2006). Its presence in strawberry fields corroborates the Stultz (Reference Stultz1968) findings in Nova Scotia.
Rhodobium porosum and Macrosiphum euphorbiae (Thomas), which were the most abundant aphids found in the strawberry fields in Nova Scotia in the 1960s (Stultz Reference Stultz1968), were practically not observed during our inventory (n = 0 R. porosum; n = 1 M. euphorbiae). MacGillivray (Reference MacGillivray1963) reports that Rhodobium porosum is a coloniser of strawberry plants in New Brunswick and Nova Scotia. However, as these surveys were done over 50 years ago, much has changed, and new surveys confirmed that R. porosum is no longer a predominant species in 2015 (D. Moreau, personal communication). The landscape and vegetation surrounding the crop fields can certainly be involved and influence the patterns of aphids found in agricultural fields (Parry et al. Reference Parry, Evans and Morgan2006).
Conclusion
The main concern of Québec strawberry stakeholders and growers facing the phenomenon of strawberry decline is the lack of information on virus-carrying insects in the province. Indeed, there are very little published studies to date on C. fragaefolii and whitefly vectors in Québec. All new information gathered in this research project, such as the evaluation of an effective trapping technique, aphid and whitefly survey conducted in strawberry fields, and determination of flight peaks of the main vectors and population dynamics, should be very useful and transferable to those involved in strawberry production.
Acknowledgements
We would like to thank all 17 strawberry growers for their crucial participation in this project, as well as Liette Lambert and all the agronomists involved in the study for their valuable contribution to sampling. We are indebted to all the field and laboratory assistants who worked with us: Manon Bellanger, Noémie Brisson, Sophie LeBoulanger, Vivien Michel, Frédéric McCune, Étienne Nadeau, Sandra Savard, and Stéphane Thibault. We are also grateful to all the researchers who contributed to the project: Pam Fisher, Robert Foottit, John Lewis, and Robert R. Martin; as well as Conrad Cloutier and Debra Moreau for their constructive comments on a previous version of the manuscript. We are thankful to Eric Maw and the Laboratoire de diagnostic du Ministère de l’Agriculture, des Pêcheries et de l’ Alimentation du Québec for their help with aphid identifications, as well as to Gaétan Daigle for his assistance with statistical analyses. This study was funded by (1) the Programme Innov’Action Volet 2 of the Ministère de l’Agriculture, des Pêcheries et de l’Alimentation du Québec, (2) the Programme d’Appui au Développement de l’Agriculture et de l’Agroalimentaire en Région of the Ministère de l’Agriculture, des Pêcheries et de l’Alimentation du Québec and the Programme Cultivons l’Avenir Volet 2, and (3) the Association des Producteurs de Fraises et Framboises du Québec.
