Flight phenology and trap selection for monitoring potential viral vector Aphididae and Aleyrodidae (Hemiptera) in strawberry (Rosaceae) fields of ...
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378
Flight phenology and trap selection for monitoring
potential viral vector Aphididae and Aleyrodidae
(Hemiptera) in strawberry (Rosaceae) fields of
Québec, Canada
Phanie Bonneau1, Jean Denis Brisson, Stéphanie Tellier, and Valérie Fournier
Abstract—Strawberry decline disease, predominantly viral in origin, was a serious threat to the
strawberry (Fragaria x ananassa Duchesne ex Rozier; Rosaceae) fields of Québec, Canada, between
2012 and 2014. Our aim was to monitor the abundance and activity of the main insect vectors: the
strawberry aphid, Chaetosiphon fragaefolii (Cockerell) (Hemiptera: Aphididae) and the greenhouse
whitefly, Trialeurodes vaporariorum Westwood (Hemiptera: Aleyrodidae). First, we compared the
effectiveness of two trapping techniques, the yellow sticky trap and the yellow pan trap. Results
showed that the sticky traps are more effective in capturing alates in flight. Second, we determined the
peak flight period for each of the two vectors in several locations within the province of Québec.
Results suggest that the peak abundance of winged C. fragaefolii is during the first two weeks of
August, while the peak abundance of T. vaporariorum is in the last two weeks of September. Overall
trap captures also found 53 different species of winged aphids, and we documented a new distribution
record on commercial strawberry fields in Québec, Aleyrodes spiraeoides (Quaintance) (Hemiptera:
Aleyrodidae). Species composition and significant information of flight periods will be useful for the
management of virus-transmitting insects associated with strawberry decline disease in Québec.
Résumé—De 2012 à 2014, le dépérissement des fraisières, principalement d’origine virale, fut une
menace sérieuse pour les champs de fraises (Fragaria x ananassa Duchesne ex Rozier; Rosaceae) du
Québec, Canada. Notre objectif était de faire un suivi de l’abondance et l’activité des principaux
vecteurs: le puceron du fraisier, Chaetosiphon fragaefolii (Cockerell) (Hemiptera: Aphididae) et
l’aleurode des serres, Trialeurodes vaporariorum Westwood (Hemiptera: Aleyrodidae). Premièrement,
nous avons comparé l’efficacité de deux techniques de dépistage, le piège-collant et le piège-bol jaune.
Les résultats indiquent que les pièges-collants sont plus efficaces pour capturer les allates en vol.
Deuxièmement, nous avons déterminé les pics de vol pour chacun des vecteurs dans plusieurs régions
de la province. Les résultats suggèrent que le pic d’abondance de C. fragaefolii ailé se situe dans les
deux premières semaines d’août, celui de T. vaporariorum se situe dans les deux dernières semaines de
septembre. Les captures ont également permis d’identifier 53 espèces différentes de pucerons ailés et
une nouvelle mention de distribution dans les fraisières commerciales au Québec, soit l’aleurode de
l’iris Aleyrodes spiraeoides (Quaintance) (Hemiptera: Aleyrodidae). La composition des espèces et les
renseignements significatifs sur les périodes de vol seront utiles dans la gestion des insectes vecteurs de
virus associés au dépérissement des fraisières au Québec.
Introduction
ex Rozier; Rosaceae) in Canada, with 57% of the
The province of Québec is the largest producer production in the country on 1700 ha in 2016, and
of strawberries (Fragaria x ananassa Duchesne ranks third in North America, after California and
Received 20 July 2018. Accepted 17 December 2019. First published online 10 April 2019.
P. Bonneau,1 V. Fournier, Centre de recherche en innovation sur les végétaux, Département de Phytologie,
Université Laval, Ville de Québec, Québec, G1V 0A6, Canada
J.D. Brisson, Ministère des Forêts, de la Faune et des Parcs, Saint-Augustin-de-Desmaures, Ville de Québec,
Québec, G3A 2T3, Canada
S. Tellier, Ministère de l’Agriculture, des Pêcheries et de l’Alimentation (MAPAQ), Direction régionale de la
Capitale-Nationale, Ville de Québec, Québec, G1N 3Y7, Canada
1
Corresponding author (e-mail: phanie.bonneau.1@ulaval.ca)
Subject editor: John Wise
doi:10.4039/tce.2019.15
Can. Entomol. 151: 378–390 (2019) © Entomological Society of Canada 2019
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Florida, United States of America (Ministère de and Martin 2013). However, in the province of
l’Agriculture, des Pêcheries et de l’Alimentation Québec, there is limited published information on
et Institut de la statistique du Québec 2018). Most whiteflies. Officially, the only known database for
commercial strawberry growers in Québec Hemiptera insects in Canada, which currently
manage their crops using the conventional matted contains more than 3900 species (Maw et al.
row system, under which production lasts two or 2000), reported three species for the province,
three years (Hancock et al. 1997). Every summer, Trialeurodes vaporariorum, Trialeurodes packardi,
plants are mowed immediately after harvest in and an uncertain mention of Aleyrodes asumaris
order to eliminate the old leaves infested with Shimer. There is no available information con-
diseases, stimulate the proliferation of runners cerning the flight period of any whitefly species
(stolons) and fruit buds, and promote a bountiful in Québec.
yield the following year (Thireau and Lefebvre The main vector of Strawberry mild yellow
2014). edge virus (Potexvirus; Alphaflexiviridae),
Strawberry decline disease has become a Strawberry mottle virus (Secoviridae), Strawberry
severe issue for growers worldwide (Tzanetakis crinkle virus (Cytorhabdovirus; Rhabdoviridae),
and Martin 2014). Serious damage has been and Strawberry vein banding virus (Caulimo-
sustained by matted row strawberry fields of virus; Caulimoviridae) is the strawberry aphid,
Québec between 2012 and 2014 (Lambert et al. Chaetosiphon fragaefolii (Cockerell) (Martin and
2014). Symptoms include a reduction of runners Tzanetakis 2006). However, many aphid species
produced by the plant, a weakened root system, can be present in strawberry fields, either as
and failure to thrive after planting. One outcome colonisers or as errants (Stultz 1968). Among
is plant death, which represents an economic loss them, Rhodobium porosum (Sanderson),
to the growers. The predominant causal factor of Myzus persicae (Sulzer), Aulacorthum solani
this worldwide disease is infection by two or (Kaltenbach), Amphorophora rubi (Kaltenbach),
more strawberry viruses (Martin and Tzanetakis Aphis gossypii Glover, and Chaetosiphon Huber
2013). species (Hemiptera: Aphididae) may transmit
As of now, the only known vector of strawberry viruses as well (Craig and Stultz
Strawberry pallidosis virus (SPaV) (Crinivirus: 1964; Tzanetakis and Martin 2013).
Closteroviridae) is the greenhouse whitefly, Among the viruses responsible for the straw-
Trialeurodes vaporariorum (Westwood) berry decline disease, there are two different
(Hemiptera: Aleyrodidae) (Tzanetakis et al. 2014). transmission modes: semi-persistent and persis-
Only a few whitefly species have been documen- tent (circulative and/or propagative) (Sylvester
ted as colonisers of commercial strawberry 1989). The semi-persistent viruses such as
plants in the United States of America and Strawberry mottle virus, Strawberry vein banding
Canada: Aleyrodes spiraeoides (Quaintance), virus, and Strawberry pallidosis virus are
Trialeurodes packardi (Morrill), Trialeurodes acquired quickly by the insects and located in
fernaldi (Morrill), and Trialeurodes ruborum their stylet for a few hours (Watson and Plumb
(Cockerell) (Evans 2008). Other sources 1972). Since the semi-persistent virus is only
have reported the presence of Trialeurodes present in the stylet of the vector, the vector-virus
abutiloneus (Haldeman) and the sweetpotato specificity is thereby moderate, which indicates
whitefly, Bemisia tabaci (Gennadius) biotype B that other aphid species could transmit these
(Tzanetakis et al. 2006) in strawberry fields. viruses as well (Andret-Link and Fuchs 2005;
Surprisingly, the most recent strawberry crop Pelletier et al. 2012). However, the circulative
profile does not identify T. vaporariorum as an persistent viruses such as Strawberry mild yellow
insect pest in commercial strawberry fields in edge virus are acquired during feeding, circulat-
Canada (Agriculture and Agri-Food Canada ing into the body for several days without
2015), similar to the local lists in Québec replicating inside the insect. The circulative prop-
(Lambert et al. 2007). Still, many studies have agative persistent viruses such as Strawberry
demonstrated that whiteflies do pose a risk to crinkle virus are also acquired during feeding,
strawberry crop (e.g., Martin and Tzanetakis circulating in the body and replicating inside the
2006, 2013; Tzanetakis et al. 2006; Tzanetakis insect for a few weeks or the lifetime of the aphid
© Entomological Society of Canada 2019
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(Gray and Banerjee 1999). Since sustained feed- seasonal variation in the abundance of winged
ing is necessary for the acquisition of persistent virus-vectors, yellow pan traps and yellow sticky
virus, the number of vector species is very limit- traps seem to be appropriate methods.
ed. Due to its high virus-vector specificity, Our overall goals undertaking this study were
C. fragaefolii is believed to be the only known to mitigate the very limited information available
vector of Strawberry mild yellow edge virus on virus-vectors present in strawberry fields, as
and Strawberry crinkle virus (Sylvester 1980; well as helping agronomists and strawberry
Andret-Link and Fuchs 2005). growers in Québec. Specifically, objectives were
Over the complex life cycle of aphids, the alate to (1) compare the effectiveness of sticky traps
form occurs depending on the crowding condi- and pan traps in monitoring C. fragaefolii and
tions, the nutritional quality of the host plant T. vaporariorum in strawberry fields; (2) deter-
(Wadley 1923), the temperature and photoperiod, mine the flight peak of these two vectors; and
or when conditions for growth are optimal (3) document aphid and whitefly population and
(Kawada 1987). It can also be induced by the species diversity in commercial strawberry fields.
presence of natural enemies and pathogens (Irwin
et al. 2007). Throughout the strawberry growing Materials and methods
season, most winged aphids emerge, including
C. fragaefolii. The winged morph is adapted for Trapping technique comparison
dispersion over great distances, being carried by Two monitoring techniques for capturing
the wind to other strawberry fields (Dixon and aphids and whiteflies as vectors of strawberry
Kindlmann 1999). Moreover, the probing behav- viruses were evaluated: yellow sticky traps and
iour of alate aphids during host selection involves yellow pan traps. The yellow sticky traps were
intensive probing activity with several plants in recycled polyvinyl chloride and sticky on both
one feeding bout (Klingauf 1987; Boquel 2011). faces (Bug-Scan Dry; Biobest, Ilse Velden,
These features play a key role in the spread of Belgium). The glue was non-toxic, waterproof,
viruses and the effectiveness of winged aphids as and did not dry out (Bug-Scan Dry, Biobest
virus-vectors. The presence of C. fragaefolii in 2016). The trap measured 25 cm × 10 cm, for
strawberry fields often coincides with high virus a total surface of 250 cm2. The sticky traps were
incidence in these same fields (Lavandero et al. hooked on two metal stakes to remain stable in the
2012). There is currently no available information fields. Yellow pan traps were set up following the
on the flight period of C. fragaefolii in Québec. collecting protocol used to monitor aphid flight in
However, a report published by Lewis (2013) Nova Scotia (D. Moreau, Agriculture and Agri-
indicates that the flight period of C. fragaefolii Food Canada, Kentville, Nova Scotia, Canada,
in western Nova Scotia, Canada, is set from the personal communication). Stainless steel bowls
beginning of June until the end of July. were painted matte yellow, using Rust-Oleum
The most common and relatively inexpensive (Painter’s Touch 2X Ultra Spray Paint number
trapping techniques to monitor the flight acti- 253712; Vernon Hills, Illinois, United States of
vity of insects are the combined interception America). Bowls were 19.7 cm in diameter and 6
and attraction traps: pan traps and sticky traps cm deep for a surface of 305 cm2. Pan traps were
(Mukhopadhyay 2011). As part of an effort to filled twice a week with propylene glycol solution
better understand the strawberry decline problem, (55–70% propylene glycol mixed with water)
yellow sticky traps were used in Nova Scotia to using the protocol described in Pelletier et al.
record flight periods of winged C. fragaefolii (2012). Propylene glycol concentration was
(Lewis 2013). Pelletier et al. (2012) used yellow higher because of evaporation in the fields. An
pan traps filled with propylene glycol (40–60%) individual bowl was hooked on to a modified
to conserve the RNA of the potato virus Y from tomato cage to remain stable in the fields.
the captured aphids. The success of these two
types of trapping techniques comes from the Experimental setting
yellow colour, which is very attractive to many Strawberry fields were selected in the following
insects, including aphids and whiteflies (Eastop localities: Portneuf (46.77541°N, 71.64213°W),
1955; Berlinger 1980). In order to measure the Côte-de-Beaupré (46.91502°N, 71.10600°W),
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Île d’Orléans (46.86277°N, 71.04923°W), measurements. Analyses were done using the
St-Nicolas (46.68881°N, 71.45499°W), Beauce Glimmix procedure of SAS (release 9.4; SAS
(46.41925°N, 70.97209°W), and Bellechasse Institute, Cary, North Carolina, United States of
(46.74127°N 70.92041°W), for a total of six America). Following significant effects in the
fields. In both years (2014 and 2015), each field analysis of variance table, protected least signifi-
measured 1 ha and was in the first year of cant difference multiple comparisons were done
production using a conventional matted row sys- to evaluate the differences between the average
tem. Ten sticky traps and 10 pan traps were placed counts. All analyses were made at the α = 0.05
in a single corner in each field, with a 1 m distance level of significance.
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,
Flight activity of vectors in Québec
Seventeen sites throughout the province of
sticky traps were collected once a week and pan
Québec were selected for the vector flight activ-
traps were collected twice a week. When col-
ity measurements for both C. fragaefolii and
lected, sticky traps were wrapped in plastic
whitefly species using yellow sticky traps as
wrap. For pan traps, a strainer was used to empty
described above. These sites included one
the specimens in Whirl-pack Nasco bags (Fort
strawberry field in each site: Gaspésie
Atkinson, Wisconsin, United States of America)
(48.07317°N, 65.58967°W), Bas-Saint-Laurent
and 95% ethanol was added for preservation.
(47.90776°N, 69.43342°W), Lac Saint-Jean
Samples were carried to the laboratory on ice
(48.48722°N, 72.30742°W), Portneuf
packs and then placed in a refrigerator until
(46.77541°N, 71.64213°W), Côte-de-Beaupré
processing. Abundance counts and identifica-
(46.91502°N, 71.10600°W), Île d’Orléans
tion of C. fragaefolii aphid and whitefly speci-
(46.86277°N, 71.04923°W), St-Nicolas
mens were performed using a stereomicroscope
(46.68881°N, 71.45499°W), Beauce (46.41925°
and based on morphological characteristics
N, 70.97209°W), Bellechasse (46.74127°N
described in Foottit and Richards (1993) and
70.92041°W), Laurentides (45.59260°N,
Brisson (2015). For the purpose of this objec-
73.92252°W), Lanaudière (45.90888°N,
tive, alate aphids were sorted as C. fragaefolii or
73.35410°W), Mauricie (46.55323°N, 72.21815°
“other species,” and all the whiteflies species
W), Outaouais (45.56983°N, 75.45687°W), Mon-
were combined.
térégie Est (45.70113°N, 72.95870°W), Montéré-
gie Ouest (45.21296°N, 73.64083°W), Estrie
Statistical analysis (45.44158°N, 72.00257°W), and Centre-du-Québec
Counts of winged aphids across time were (46.08587°N, 72.83665°W). For 2014 and 2015,
analysed using a generalised randomised block each field had a surface area of 1 ha, and was in
analysis of variance model with repeated mea- the first or second year of production using a con-
sures. In order to deal with the overdispersed ventional matted row system. Five sticky traps were
count outcome variables, the negative binomial placed in one corner of each field, with a distance of
distribution was chosen with a log link function. 1 m between traps.Thecornerwaschosenaccording
The experimental unit at each site was a group of to the prevailing wind direction. From 26 May to 27
4–10 traps, depending on the number of traps October 2014 and 25 May to 26 October 2015,
recovered. There were 12 experimental units for stickytrapswerecollectedonce a week and wrapped
each type of traps, as there were six strawberry in plastic wrap. Traps were promptly shipped to
fields for two years. Since the number of traps V.F.’s laboratory at Laval University and placed in a
was not constant, this variable was used as an refrigerator at 4 °C upon arrival. Abundance counts
offset in the model in the log scale. The fixed and identification of C. fragaefolii aphid and
effects were the type of traps (pan traps versus whitefly specimens were performed using a stereo-
sticky traps) and the dates, while the random microscope and based on the morphological char-
effects were the sites. The total catch of winged acteristics described in Foottit and Richards (1993)
aphids for the season was also analysed using a and Brisson (2015). Again, for the purpose of this
similar approach, but this time without repeated part of the study, alate aphids were sorted as either
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C. fragaefolii or “other species” and all whitefly McLeod 1994). Identifications were validated by
species were combined. taxonomist Eric Maw (Canadian National Collec-
tion of Insects, Arachnids, and Nematodes, Otta-
Abundance and diversity of whiteflies and wa, Ontario, Canada). Voucher specimens from
aphids in selected strawberry fields our study are stored in the Fournier Laboratory in
Data on the abundance and diversity of white- the Phytology Department at the Université Laval
flies were obtained by counting the specimens (Ville de Québec, Québec, Canada).
caught from 25 May to 26 October 2015 on the
yellow sticky traps used at the 17 sites described Results
previously. Specimens were identified under
stereomicroscope based on morphological char- Trapping technique comparison
acteristics (Brisson 2015) and identification was Yellow sticky traps were more effective in
validated by J.D.B. capturing alate aphids compared to yellow pan
The abundance of aphid species and genera traps (F = 173.29; df = 1, 11; P < 0.0001)
reported in this paper was measured by collecting (Fig. 1A). The mean of the total captures, all sites
the aphids caught in yellow pan traps as described combined, was 24.0 ± 5.8 aphids (mean ± stan-
above. Three sites, located in St-Nicolas dard error) per pan trap, while it was 133.2 ± 32.4
(46.68881°N, 71.45499°W), Portneuf (46.77541° aphids per sticky trap. Yellow sticky traps were
N, 71.64213°W), and Île d’Orléans (46.86277°N, more effective in capturing C. fragaefolii speci-
71.04923°W), were selected for the survey of mens than pan traps (F = 21.04; df = 1, 11;
aphid species and genera. We selected these P = 0.0008), even though the numbers were very
fields due to the reduced number of overall pesti- low (Fig. 1B). The mean of the total catch, all sites
cide applications that prevailed in them. Trap combined, was 0.9 ± 0.2 C. fragaefolii per pan
setup and collection methods were as previously trap, while it was 1.8 ± 0.4 C. fragaefolii per
outlined under Experimental setting for Trapping sticky trap. No whitefly was captured in pan traps
technique comparison sections. Once collected in 2014 or 2015. Therefore, no comparison was
from the field, aphids were sorted and then made between the two types of traps for this
mounted on microscope slides in Canada balsam, taxon.
according to an established protocol (Maw 1999).
A total of 203 mounted specimens were identified Flight activity of vectors across Québec
under the stereomicroscope based on morpholog- In 2014, the highest count per trap was
ical characteristics (MacGillivray 1979; Quednau 4.2 ± 2.2 whiteflies, captured in mid-September,
1985; Foottit and Richards 1993; Gualtieri and while there was a peak of 56.6 ± 36.9 whiteflies
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.
A B
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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.
A
B
per trap at the end of September in 2015 end of September, with a recurrence in mid-
(Fig. 2A). Based on this, the highest abundance October in both years.
of whiteflies was observed near the end of the
growing season, although whiteflies were usually Abundance and diversity of whiteflies and
present throughout the entire season, from the aphids in selected strawberry fields
end of May until the end of October in both years. Two different species of whiteflies were identi-
As for C. fragaefolii, there was a peak of 0.5 ± fied: Trialeurodes vaporariorum and Aleyrodes
0.1 per trap in mid-August 2014, and 0.7 ± 0.3 spiraeoides (Table 1). The highest number of
per trap around the same time in 2015 (Fig. 2B). T. vaporariorum was found in the Lanaudière
They were mostly present from early June to the region, with 1398 individuals. Aleyrodes
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Table 1. Total seasonal counts of whitefly species per Table 2. Total seasonal counts of aphid species or
site, captured in yellow sticky traps from 25 May to genera captured in yellow pan traps from 23 June to
26 October 2015 at 17 sites. 27 October 2014 at three sites combined.
Trialeurodes Aleyrodes Number of
Sites vaporariorum spiraeoides Species specimens caught
Bas-Saint-Laurent 1 1 Acyrthosiphon pisum 123
Beauce 13 0 Harris
Bellechasse 13 0 Acyrthosiphon Mordvilko 2
Centre-du- 468 6 species
Québec Amphorophora agathonica 20
Côte-de-Beaupré 31 1 (Hottes)
Estrie 35 0 Amphorophora Buckton 5
Gaspésie 0 0 species
Île d’Orléans 103 1 Anoecia Koch species 7
Lac Saint-Jean 16 0 Aphis fabae Scopoli 2
Lanaudière 1398 2 Aphis glycines Matsumura 98
Laurentides 228 11 Aphis gossypii Glover 8
Mauricie 22 0 Aphis Linnaeus species 764
Montérégie Est 4 0 Aphis spiraecola Patch 1
Montérégie Ouest 212 6 Capitophorus elaeagni 3
Outaouais 172 1 (Del Guercio)
Portneuf 11 0 Capitophorus hippophaes 3
St-Nicolas 407 88 (Walker)
Total 3134 117 Capitophorus Van Der 1
Goot species
Carolinaia Wilson species 3
Cavariella aegopodii 2
spiraeoides was the most abundant in St-Nicolas, (Scopoli)
with 88 individuals. Trialeurodes vaporariorum Chaetosiphon fragaefolii 24
represents 96% of all the catches; and Aleyrodes (Cockerell)
spiraeoides, 4%. Chaetosiphon Huber 5
A total of 1595 specimens were captured, species
representing 35 different genera and over 53 Chaitophorus populicola 14
(Thomas)
species (Table 2). The 10 most abundant species
Chaitophorus populifolii 2
were: Aphis Linnaeus species (764); Hayhurstia (Essig)
atriplicis (Linnaeus) (239); pea aphid, Cinara Curtis species 1
Acyrthosiphon pisum Harris (123); Aphis glycines Euceraphis Walker species 1
Matsumura (98); green peach aphid, Myzus Forda formicaria von 1
persicae (Sulzer) (54); mustard aphid, Lipaphis Heyden
pseudobrassicae (Davis) (43); yellow clover aphid, Hayhurstia atriplicis 239
Therioaphis trifolii (Monell) (39); strawberry (Linnaeus)
aphid, Chaetosiphon fragaefolii (Cockerell) Hyalopterus pruni 1
(24); Macrosiphum Passerini species (21); and (Geoffroy)
Amphorophora agathonica (Hottes) (20). Hyperomyzus lactucae 2
(Linnaeus)
Hyperomyzus pallidus 12
Discussion Hille Ris Lambers
Hyperomyzus Börner 1
In the context of the strawberry decline dis- species
ease, the management of viruses begins with Unknown 2
managing the winged form of the virus-carrying Lipaphis pseudobrassicae 43
insects. Our aim was, therefore, to gather new (Davis)
and crucial information on the population
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Table 2. Continued methodologies: (1) yellow sticky traps, as used
in Nova Scotia to monitor the flight activity of
Number of
C. fragaefolii (Lewis 2013); and (2) yellow pan
Species specimens caught
traps, as used in New Brunswick, Canada, to
Macrosiphoniella Del 2 monitor aphid vectors of potato virus Y in potato
Guercio species fields (Pelletier et al. 2012). Results presented
Macrosiphum euphorbiae 1 above contribute additional knowledge of species
(Thomas)
composition and peaks in flight period, as well as
Macrosiphum Passerini 21
the relative effectiveness of the yellow sticky trap
species
Metopolophium dirhodum 5 technique.
(Walker)
Myzocallis punctata 8 Trapping technique comparison
(Monell) The analysis of variance results demonstrate
Myzus persicae (Sulzer) 54 that the yellow sticky traps are by far the most
Nasonovia ribisnigri 3 efficient trapping technique for all species of
(Mosley)
aphids found in strawberry fields combined, as
Nearctaphis crataegifoliae 2
they collected the highest number of insects
(Fitch)
Nearctaphis Shaposhnikov 1
(Fig. 1). This further confirms previous findings
species that sticky traps are very effective in measuring
Pemphigus 6 the relative abundance of aphids (A’Brook 1973;
populitransversus Riley Harrington et al. 2007). Sticky traps are also very
Pemphigus Hartig species 3 easy to use, as they require less equipment and
Pleotrichophorus Börner 3 manipulation compared to pan traps. In contrast,
species one of the disadvantages of using sticky traps is
Prociphilus Koch species 1 that the identification of aphid species can be
Protaphis middletonii 7 difficult because the specimens are stuck to the
Thomas trap and sometimes in poor condition, as key
Rhopalomyzus Mordvilko 4
taxonomic characteristics can often be obscured
species
Rhopalosiphum padi 2
and damaged.
(Linnaeus) With regard to the monitoring of C. fragaefolii,
Rhopalosiphum Koch 5 statistical analysis indicated a significant differ-
species ence between the trap type, with the yellow sticky
Sitobion avenae (Fabricius) 10 traps being the most effective. However, although
Tetraneura Hartig species 1 statistically significant, the actual difference
Thecabius gravicornis 2 between capture numbers of C. fragaefolii was
(Patch) 0.9. The overall low captures of C. frageafolii
Therioaphis trifolii 39 likely impacted the analyses. Our results pointed
(Monell) out that the numbers of the winged form of
Uroleucon sonchi 4
C. fragaefolii were much lower than winged form
(Linnaeus)
Uroleucon Mordvilko 19 of other aphids (Fig. 1), similar to what was found
species in yellow sticky traps in Nova Scotia (Lewis
Uroleucon taraxaci 2 2013). It appears typical to encounter fewer
(Kaltenbach) populations of winged C. fragaefolii compared
with other winged aphid species. However, the
numbers of wingless C. fragaefolii are probably
dynamics by identifying the flight activity of much higher than winged C. fragaefolii inside the
C. fragaefolii and T. vaporariorum, throughout fields, on the plants, as Lewis (2013) demonstrat-
the province of Québec, using an efficient moni- ed by sampling leaves.
toring technique. Consequently, the main goal of Several studies using yellow pan traps have
this study was to compare commonly used shown their effectiveness in capturing high
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numbers of aphids in general (Labonne et al. Flight activity of vectors across Québec
1989; Avinent et al. 1991) as well as C. fragaefolii The winged forms of virus-carrying insects
(O’Loughlin 1963). Aphids are easier to navigate using their olfactory sense (Pickett
identify when captured with pan traps, as their et al. 1992). Thus, thousands of winged aphids
morphological characteristics would remain in- can land on a random strawberry field (Perring
tact in liquid. This allowed us to mount the et al. 1999). Knowledge of the flight activity of
captured specimens on Canada balsam micro- known vectors in Québec strawberry fields is
scope slides for easier identification (Maw essential to control the spread of viruses, as
1999). One inconvenience observed in the field flight peaks correspond to virus transmission
was that bowls sometimes dried out in the hot peaks.
summer weather, a problem also reported by The flight peak of whiteflies in the province of
Harrington et al. (2007). Québec occurs around the last two weeks of
Little research has been conducted to compare September, though it slightly differs across geo-
these two methods directly in the field. The first graphic regions (Fig. 2A). A significantly higher
documented user of pan traps for catching aphids, number of whiteflies (over 14 times higher) was
Moericke (1951), experimented with different documented in 2015 compared to the same period
coloured traps to identify which was attracting in 2014. There are various possible reasons
the highest number of insects. Other studies why whiteflies have a flight peak. Trialeurodes
compared cylindrical and flat sticky traps vaporariorum are likely to exit greenhouse struc-
(Broadbent 1948, 1957). Both trap types are tures at the end of the summer after the crops have
considered effective in capturing winged been harvested (Lambert et al. 2014). It is also
C. fragaefolii and other aphid species that visit possible that nearby fields were being or had just
strawberry plants, as both are the most frequently been harvested, as tillage or mowing can provoke
used methods worldwide (Mukhopadhyay 2011). insect flights in large numbers (Gencsoylu and
Nonetheless, when we compared both techni- Yalcin 2004).
ques, our results were quite different from studies Our results showed that the main flight peak of
that compared yellow Moericke-style pan traps C. fragaefolii in Québec was around the first two
and Broadbent-style yellow flat sticky traps weeks of August, though this slightly varied from
(Heathcote 1957; O’Loughlin 1963), in which one region to another. In 2015, the flight period
the number of aphids caught in yellow pan traps seemed to have lasted longer than in 2014. This
was much higher than the number of aphids could be explained by temperatures during the
caught on sticky traps. 2015 growing season, which were warmer early
Based on our fieldwork, sticky traps would and later in the season as compared to 2014 (The
seem to be the most efficient trapping technique Weather Network 2015). In addition, spring of
to capture whiteflies, since no whitefly has been 2014 was quite cold with recorded precipitations
caught in pan traps during the two growing above normal across the province (The Weather
seasons of this study. This result is similar to Network 2014). A second, smaller flight peak at
conclusions drawn in other studies: sticky traps the end of the season could be explained by
are very effective in detecting whitefly populations winged male production in autumn for sexual
and measuring population dynamics (Ohnesorge reproduction (Williams and Dixon 2007), and
and Rapp 1986; Gillespie and Quiring 1987). also the senescence of the host plants and shorter
Since the presence of C. fragaefolii coincides day lengths, leading to aphids developing wings
with the presence of strawberry viruses and leaving the fields (Wadley 1923; Kawada
(Lavandero et al. 2012) and the presence of 1987).
T. vaporariorum coincides with the presence of The flight peaks of C. fragaefolii occurred
Strawberry pallidosis virus (Tzanetakis et al. earlier in western Nova Scotia (Lewis 2013) than
2006), trapping using sticky traps in order to was identified in Québec. This could be due, in
monitor flight activity of the winged vectors will part, to the warming influence of the marine
continue to provide important knowledge for climate and slightly higher mean maximum tem-
agronomists and strawberry growers across the peratures, measured in Kentville, Nova Scotia, for
province of Québec. the same years.
© Entomological Society of Canada 2019
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https://www.cambridge.org/core/terms. https://doi.org/10.4039/tce.2019.15Bonneau et al. 387
Abundance and diversity of whiteflies and species could certainly transmit semi-persistent
aphids in selected strawberry fields strawberry viruses (Andret-Link and Fuchs 2005;
Regarding the whitefly survey, two species were Pelletier et al. 2012). Thus, our aim was to
captured: the greenhouse whitefly, Trialeurodes identify which aphid species may be pests in
vaporarorium, and a new distribution record strawberry crop in the province of Québec.
for the province of Québec, the iris whitefly, The aphid survey we conducted in strawberry
Aleyrodes spiraeoides. Interestingly, the dis- fields using yellow pan traps was done on three
tribution of these two species of whiteflies in different sites located in the region of the greater
commercial strawberry fields of various regions area of Ville de Québec. It documented the
of Québec was not initially suspected. According presence of at least 53 different species of winged
to Brisson (2014), A. spiraeoides was observed in aphids (Table 2). Among them, Aphis was the
Québec in 2001, though it has since gone most abundant genus. Some species found in our
unnoticed until now and even confused with pan traps are potential vectors of strawberry
T. vaporariorum, which is better known. Both viruses, such as Myzus persicae, Aphis gossypii,
species are active at temperatures as low as 8 °C and different species of Chaetosiphon (Craig and
(Landis et al. 1958; van Roermund and van Stultz 1964; Tzanetakis and Martin 2013).
Lenteren 1992). They therefore appear very early Moreover, we did find 20 specimens of
in the season, feeding and breeding on a very Amphorophora agathonica, which is an important
large number of plants, including wild strawberry vector of the red raspberry and black raspberry
plants – Fragaria chiloensis Linnaeus and (Rubus Linnaeus; Rosaceae) viruses (Lightle
Fragaria virginiana Miller (Landis et al. 1958; et al. 2014). Interestingly enough, this aphid
McClanahan 1979; Tzanetakis et al. 2006). species is noted to be monoecious, and Rubus is
Although A. spiraeoides represents only 4% of its only known host (Blackman and Eastop 2006).
all catches in Québec strawberry fields, it is Its presence in strawberry fields corroborates the
considered an emerging pest in strawberry fields Stultz (1968) findings in Nova Scotia.
in California, United States of America (Zalom Rhodobium porosum and Macrosiphum
et al. 2005). Curiously, Trialeurodes packardi euphorbiae (Thomas), which were the most
reported in the database for Hemiptera insects in abundant aphids found in the strawberry fields
Canada (Maw et al. 2000) was not captured. in Nova Scotia in the 1960s (Stultz 1968),
The number of described genera and species of were practically not observed during our inventory
whiteflies worldwide has increased dramatically (n = 0 R. porosum; n = 1 M. euphorbiae).
in the recent years and is undoubtedly under- MacGillivray (1963) reports that Rhodobium
estimated (Martin and Mound 2007; Evans porosum is a coloniser of strawberry plants in
2008). The whiteflies of Québec are no excep- New Brunswick and Nova Scotia. However, as
tion. An unofficial list from various sources was these surveys were done over 50 years ago, much
recently initiated by Entomofaune du Québec has changed, and new surveys confirmed that
(2018), including some observed species such R. porosum is no longer a predominant species
as Trialeurodes abutiloneus (Lambert 1999), in 2015 (D. Moreau, personal communication).
Aleurochiton forbesii (Ashmead) (Claude Pilon, The landscape and vegetation surrounding the
Repentigny, Québec, Canada, unpublished data, crop fields can certainly be involved and influence
personal communication), and Aleyrodes proletella the patterns of aphids found in agricultural fields
(Linnaeus) (Brisson 2015). A more exhaustive (Parry et al. 2006).
research with field sampling should be considered
to obtain a precision of the number of all the
Conclusion
whitefly species present and established in Québec.
A comprehensive survey of all aphids present The main concern of Québec strawberry sta-
in strawberry fields in Québec has never been keholders and growers facing the phenomenon of
conducted. Since virus-vector specificity is not as strawberry decline is the lack of information on
strong for semi-persistent viruses as for persistent virus-carrying insects in the province. Indeed,
viruses, many different and, as yet, unknown there are very little published studies to date on
© Entomological Society of Canada 2019
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https://www.cambridge.org/core/terms. https://doi.org/10.4039/tce.2019.15388 Can. Entomol. Vol. 151, 2019
C. fragaefolii and whitefly vectors in Québec. All Andret-Link, P. and Fuchs, M. 2005. Transmission
new information gathered in this research project, specificity of plant viruses by vectors. Journal of
such as the evaluation of an effective trapping Plant Pathology, 87: 153–165.
Avinent, L., De Mendoza, A.H., and Llácer, G. 1991.
technique, aphid and whitefly survey conducted Comparison of traps for capture of alate aphids
in strawberry fields, and determination of flight (Homoptera, Aphidinea) in apricot tree orchards.
peaks of the main vectors and population dynam- Agronomie, 11: 613–618.
ics, should be very useful and transferable to Berlinger, M.J. 1980. A yellow sticky trap for
those involved in strawberry production. whiteflies: Trialeurodes vaporariorum and Bemisia
tabaci (Aleurodidae). Entomologia Experimentalis
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Acknowledgements Biobest. 2016. Website of Bug-Scan Dry product.
Available from www.biobestgroup.com/en/biobest/
We would like to thank all 17 strawberry products/monitoring-and-scouting-4464/sticky-traps-
growers for their crucial participation in this and-rolls-4486/bug-scan-dry-4670 [accessed 29 Jan-
project, as well as Liette Lambert and all the uary 2019].
agronomists involved in the study for their valu- Blackman, R.L. and Eastop, V.F. 2006. Aphids on the
able contribution to sampling. We are indebted to world’s herbaceous plants and shrubs. Volume 2, the
aphids. John Wiley & Sons, Chichester, United
all the field and laboratory assistants who worked Kingdom.
with us: Manon Bellanger, Noémie Brisson, Boquel, S. 2011. Propension vectorielle des
Sophie LeBoulanger, Vivien Michel, Frédéric pucerons dans l’épidémiologie du virus Y (PVY)
McCune, Étienne Nadeau, Sandra Savard, and en culture de pommes de terre. Thèse de doctorat.
Stéphane Thibault. We are also grateful to all the Université de Picardie Jules Verne, Amiens,
France.
researchers who contributed to the project: Pam
Brisson, J.D. 2014. Les aleurodes d’importance agri-
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