Crop Protection 55 (2014) 21e27

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Crop Protection
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Impact of quarantine procedures on weed biodiversity and

abundance: Implications for the management of the golden potato
cyst nematode, Globodera rostochiensis
Benjamin Mimee a, *, Roxane Andersen b, c, Guy Bélair a, Anne Vanasse b, Mike Rott d
a
Agriculture and Agri-Food Canada, Horticulture Research and Development Centre, 430 Boul. Gouin, St-Jean-sur-Richelieu, Québec, QC J3B 3E6, Canada
b
Université Laval, Faculté des Sciences de l’Agriculture et de l’Alimentation, Département de Phytologie, 2425 rue de l’Agriculture, Québec,
QC G1V 0A6, Canada
c
University of the Highlands and Islands, North Highland College, Ormlie Road, Thurso, Caithness KW14 7EE, UK
d
Canadian Food Inspection Agency, Sidney Laboratory, 8801 East Saanich Road, Sidney, BC V8L 1H3, Canada

a r t i c l e i n f o a b s t r a c t

Article history: In 2006, the golden nematode, Globodera rostochiensis, a regulated pest causing heavy losses in potato
Received 13 June 2013 fields was discovered in Quebec, Canada. The rapid application of quarantine measures by the Canadian
Received in revised form Food Inspection Agency significantly changed the use and management of infested fields. The objectives
26 September 2013
of this study were to assess the evolution of weed populations following these measures and assess their
Accepted 2 October 2013
impact on the management of G. rostochiensis. A comparison of weed inventories conducted in 2008 and
2011 on the edges of the affected fields has shown that the composition of the flora had changed
Keywords:
considerably. Alarmingly, the presence of Solanaceae that could potentially serve as host plants for the
Biodiversity
Globodera rostochiensis
potato cyst nematode increased significantly. The biodiversity index was also significantly affected by
Nightshade this change and decreased by more than 50% between the two years. Interestingly, the lowest biodi-
Potato cyst nematode versity was observed in one of the few fields where potatoes were grown in 2011 and where an explosion
Quarantine of Solanum sarrachoides was observed. Meanwhile, eight species of nightshade were evaluated for their
Solanum ability to support the growth of G. rostochiensis. Solanum villosum allowed the greatest rates of repro-
duction while only a few cysts were produced on Solanum nigrum and Solanum dulcamara. This study has
shown that the modifications in weed control regimes associated with the implementation of quarantine
procedures could hamper its success by favouring the multiplication of potential pest refuges.
Crown Copyright Ó 2013 Published by Elsevier Ltd. All rights reserved.

1. Introduction Newfoundland (Olsenand and Mulvey, 1962) and since 1965 in

British Columbia (Orchard, 1965). More recently, G. rostochiensis was
Potato cyst nematodes (PCN), Globodera pallida Stone and Glo- detected in several fields in Quebec (Sun and Miller, 2007). These
bodera rostochiensis (Wollenweber) Skarbilovich, are serious quar- areas have been subject to strict quarantine regulations and a recent
antine pests of potato that cause severe damage. Once established in survey on Vancouver Island, British Columbia showed that fields
a new area, they are very difficult to eradicate because of their ability with no known quarantine infractions were found to be free of
to survive for extended periods without a suitable host (Turner, viable cysts (Rott et al., 2010). Quarantine measures have also proven
1996). Both species have co-evolved with their host in the Andean to be effective in New York State where United States Department of
regions of Peru and Bolivia, in South America (Grenier et al., 2010). Agriculture (USDA) Animal and Plant Health Inspection Service
G. rostochiensis is now found in 75 countries around the world (Yu (APHIS) announced on December 2010 that two counties had been
et al., 2010). In Canada, it has been present since 1962 in removed from the quarantine area after being tested free of PCN
(USDA APHIS PPQ, 2011). This was the first deregulation since the
establishment of G. rostochiensis quarantine area in 1944.
Since it is imperative to react promptly following the discovery
Abbreviations: PCN, Potato cyst nematode. of a regulated pest, changes in field usage and management prac-
* Corresponding author. Tel.: þ1 450 515 2136.
E-mail addresses: [email protected] (B. Mimee), Roxane.Andersen@
tices can be abrupt. Producers often turn to alternative crops that
uhi.ac.uk (R. Andersen), [email protected] (G. Bélair), Anne.Vanasse@ they are less familiar with and work is frequently contracted out.
fsaa.ulaval.ca (A. Vanasse), [email protected] (M. Rott). The combination of rapid change, new crops and cultivation

0261-2194/$ e see front matter Crown Copyright Ó 2013 Published by Elsevier Ltd. All rights reserved.
http://dx.doi.org/10.1016/j.cropro.2013.10.003
22 B. Mimee et al. / Crop Protection 55 (2014) 21e27

practices that may not be optimized could impact the weed Agriculture and Agri-Food Canada (AAFC) (n ¼ 1) located in the
composition at the field margins. It is of interest to understand how quarantine area of the locality of St-Amable, QC. In each field, the
these changes may affect the dynamics of disease and efficacy of percent cover of weeds was evaluated in 0.5 m by 1 m (0.5 m2)
quarantine procedures. We chose to focus on the impact of quadrats. One quadrat was placed every 50 m along all sides of the
G. rostochiensis quarantine procedures on weed biodiversity in field or closer in smaller fields (less than 150 m/side) in order to
quarantined fields as weeds are generally good hosts for plant- obtain a minimum of three observations per side. The composition
parasitic nematodes (Bélair and Benoit, 1996). of the immediate environment (river, forest, grass, road, etc.) and
In soybean, it is well known that various weeds may enable the adjacent crop (corn, potato, etc.) were also noted for each
soybean cyst nematode reproduction in infested fields during the quadrat. In addition, the edges of the fields were walked and every
early or late growing season, even when soybean plants are absent weed belonging to the Solanaceae family was identified to the
(Venkatesh et al., 2000). There are also reports in the literature that species level and its geographical position determined using a GPS
PCN can reproduce on weeds belonging to the same family as po- device. The inventories were repeated in the same fields during the
tato (Solanaceae) (Bates, 1945; Boydston et al., 2010; Rott et al., summer of 2008 and 2011.
2011; Sullivan et al., 2007). In this case, even if a good rotation
system with non-host crops is implemented, the nematode could 2.1.2. Biodiversity
still survive and multiply if such weeds were present in and around All statistical analyses were performed using the R software
the fields. Nightshades are Solanum species that have a widespread environment (R Development Core Team, Vienna, Austria). Average
distribution. They are already known to substantially reduce yield weed richness and diversity (functions specnumber and diversity in
in several major crops and to interfere with harvest, causing the vegan package, Oksanen et al., 2008) were estimated for the
reduction in crop quality (Crotser and Witt, 2000; Majek, 1981). whole dataset (n ¼ 1470 points, 22 fields) and compared between
Sullivan et al. (2007) listed over 30 nightshade species as potential years using the t-test (t.test function in stats package in R). To
hosts for PCN. In the province of Quebec, four species of nightshade characterize the weed composition, a truncated and pre-
have been recorded in the past: Solanum nigrum L., Solanum dul- transformed matrix of weed-species cover was used: species
camara L., Solanum sarrachoides Sendtner (Doyon et al., 1987) and which occurred in less than 10% of the points were eliminated and
Solanum pseudocapsicum L. (Lemieux, 1988). S. sarrachoides has the percentage cover of the weed species was subjected to a Hel-
previously been reported in 11% of the surveyed potato fields of the linger’s transformation (function decostand, vegan package in R),
region of Lanaudière (Doyon et al., 1987). A recent study on which is well suited for community analyses of such data. The
G. pallida host range has indicated that S. sarrachoides and Solanum Hellinger’s transformation gives less weight to abundant species
physalifolium Rusby were good host plants, while the other species and avoids problems arising from Euclidean distance where the
tested (S. dulcamara, Solanum triflorum Nutt. and S. nigrum) were distance between two sites sharing no species can be smaller than
unable to support G. pallida reproduction (Boydston et al., 2010). that between two sites sharing species (Legendre and Gallagher,
For G. rostochiensis, Doncaster (1953) showed that S. nigrum is 2001). The influence of year, cultivation type and adjacent envi-
resistant but conflicting results are found in the literature and the ronment on weed composition in the field margins was evaluated
same species is often rated both resistant and susceptible by using a redundancy analysis (RDA).
different authors (Prummel, 1958; Sullivan et al., 2007).
Recently, Rott et al. (2011) showed that most of the nightshades 2.1.3. Changes in occurrence and cover of Solanaceae spp. in field
were resistant to G. rostochiensis populations from Newfoundland margins
and British Columbia, Canada. No reproduction was observed on To estimate the spread of Solanaceae spp. in the field margins,
Solanum americanum Mill., S. physalifolium, Solanum carolinense L., we compared the frequency, cover, distribution and aggregation of
Solanum ptycanthum Dunal, Solanum rostratum Dunal., Solanum S. sarrachoides and Solalum tuberosum in 2008 and 2011. For each
sisymbriifolium Lam., S. sarrachoides and S. triflorum Nutt. Most of field, the frequencies of occurrence were estimated as the ratio of
the S. nigrum tested were also fully resistant to G. rostochiensis. the number of quadrats in which either species was present over
Conversely two accessions (probably hybrids between Solanum the total number of quadrats visited, and the average percentage
villosum Mill. and S. nigrum) were found to be susceptible to cover when the species were present. The values between the two
G. rostochiensis from Newfoundland but resistant to the British years were compared using a paired t-test.
Columbia isolate. The most problematic weeds were S. dulcamara
and S. villosum for which susceptible plants to G. rostochiensis have 2.1.4. Changes in patch size and aggregation
been found. The distribution and aggregation of Solanaceae spp. were esti-
In 2006, a unique opportunity arose in Canada with the detection mated by calculating patch number and average patch size and
of G. rostochiensis in several fields in Quebec (Mahran et al., 2010; changes between years for each field and for the entire dataset.
Sun and Miller, 2007; Yu et al., 2010) and the subsequent imple- Patch sizes were calculated using the GPS coordinates of points
mentation of quarantine measures in these fields. This situation with Solanaceae as the number of consecutive points where the
allowed for the assessment of weed populations over time following presence of either S. sarrachoides or S. tuberosum had been regis-
PCN quarantine measures. More specifically, the occurrence, cover tered within a maximum of 15 m of each other (to account for GPS
and distribution of Solanum spp. were considered in these fields and error). A relative size was used based on the number of points,
the host status of Solanum spp. to the Quebec population of where a single point would have a value of one. Re-occurrence of
G. rostochiensis was determined in controlled experiments. single points and patches between years was also estimated to
determine if the patches were likely to persist over time once
2. Material and methods established.

2.1. Weed survey 2.2. Host range study

2.1.1. Inventories 2.2.1. Solanum weeds accessions

All the fields tested were sandy soils either in commercial pro- Seeds of Solanum weeds were obtained from the United
duction (n ¼ 21), in meadow (n ¼ 2) or an experimental site for States Department of Agriculture (USDA) Germplasm Resources
 B. Mimee et al. / Crop Protection 55 (2014) 21e27 23

Information Network (GRIN) and from the Botanical and Experi- 2.5  5 cm nylon bag with a mesh size of 50 mm, in pots with
mental Garden from Radboub University, Nijmegen, Netherlands. approximately 1 L of pasteurized soil composed of three parts of
Two isolates were also collected from the fields: S. dulcamara from sand for one part of black earth. Six plants of both ‘Desirée’ and
Ottawa, ON and S. nigrum from St-Hyacinthe, QC. The complete list ‘Snowden’ potato cultivars were grown and inoculated as suscep-
of the different species and accession numbers can be found in the tible indicators while the cultivar ‘Andover’ was used as a resistant
results section. control. All the pots were inoculated with cysts once the plant had
reached approximately 10 cm in size. Plants were grown in a
2.2.2. Host susceptibility to G. rostochiensis greenhouse for 120 days with daily temperature regimes between
A population of G. rostochiensis from St-Amable, QC was 19 and 22  C and 16 h of light. At the end of the experiment, the soil
increased in a greenhouse on susceptible potatoes (cv. ‘Chieftain’) was dried and the cysts recovered using a modified Fenwick can
and used in this study. The susceptibility of the different weeds to extraction procedure (Fenwick, 1940), and counted. Multiplication
G. rostochiensis was conducted following the standard EPPO pro- rates (pf/pi) were determined by dividing the number of cysts at the
tocol (EPPO, 2006). Six plants from each Solanum accession num- end of the experiment (pf) by the number of cysts used for inocu-
ber, grown from seed, were inoculated with 10 cysts contained in a lation (pi). Relative susceptibility was expressed as a percentage of

Table 1
Percent occurrence of each weed species in 2008 and 2011.

Species Occurrencea Species (cont.) Occurrence

2008 2011 2008 2011

Field horsetail 45.53 43.00 Wire-stemmed muhly 1.20 0.00

Tufted vetch 38.83 14.90 Purslane 1.20 8.70
Quack grass 31.79 7.99 Broad-leaved Cat-tail 1.20 0.20
Common ragweed 27.66 20.81 Drummond’s Arabis 1.03 0.15
Common reed 25.95 14.00 Cut-leaved Bugle-weed 1.03 0.00
Yellow nut sedge 21.82 34.00 Wild Parsnip 1.03 0.00
Perennial sow-thistle 17.53 6.20 Sheep sorrel 1.03 0.20
Common milkweed 16.67 9.05 Reed Phalaris 1.03 0.00
Canada goldenrod 16.67 2.41 Silver-weed 1.03 0.00
Purple Loosestrife 15.46 10.00 Smooth brome 0.86 0.20
Yellow foxtail 15.12 16.00 Filicophyte 0.86 0.60
Large crab grass 14.43 30.20 Mugwort 0.86 0.00
Dandelion 13.92 6.50 Salix spp. 0.86 0.00
Lamb’s-quarters 12.37 18.30 Giant foxtail 0.86 1.10
Yellow evening-primrose 7.22 5.00 Green pigweed 0.69 0.75
Wild buckwheat 6.53 8.60 Low cudweed 0.69 0.80
Cape Touch-me-not 6.36 3.60 Rough cinquefoil 0.69 1.50
Narrow-leaved goldenrod 6.36 3.02 Yarrow 0.52 0.30
Kentucky blue grass 6.01 2.00 Nodding beggarticks 0.52 0.50
Redtop 5.50 0.15 Canada thistle 0.52 0.30
Hedge bindweed 5.50 1.10 Chicory 0.52 0.00
Alleghenny Blackberry 5.15 2.60 Common Flax 0.52 0.00
Colt’s-foot 4.98 0.80 Common St. John’s-wort 0.52 0.50
Raspberry 4.81 1.20 Grass-leaved stitchwort 0.52 1.51
Witch grass 4.81 11.00 Sedge sp. 0.34 0.00
Canada fleabane 4.81 1.40 Wild cucumber 0.34 0.60
Barnyard-grass 4.47 5.70 Hairy galinsoga 0.34 0.80
European wood-sorrel 4.30 2.10 Prickly lettuce 0.34 0.00
Timothy 3.95 1.70 Great Mullein 0.34 0.50
Lady’s-thumb 3.78 1.70 Marshpepper smartweed 0.34 2.90
Redroot pigweed 3.61 5.28 Spreading Dogbane 0.17 0.00
Wild carrot 3.61 2.40 Spreading atriplex 0.17 0.00
Green smartweed 3.61 1.80 Shepherd’s-purse 0.17 0.60
Alsike clover 3.61 0.30 Marsh Hedge-Nettle 0.17 0.00
Red fescue 2.75 1.70 Glandular Willow-herb 0.17 0.00
American Strawberry 2.75 1.50 Sun spurge 0.17 0.00
Wild mustard 2.75 3.60 Great burdock 0.17 0.20
Smooth crab grass 2.58 5.40 Ground Ivy 0.17 0.00
Hemp-nettle 2.58 2.70 Squirrel-tail Grass 0.17 0.00
Red clover 2.58 2.60 Fall panicum 0.17 0.00
Bird’s-foot trefoil 2.41 0.20 Curled dock 0.17 0.00
Rubus spp. 2.41 1.70 Aspen 0.17 0.30
Broad-leaved plantain 2.23 2.40 Potatob 0.17 0.50
Hairy nightshadeb 2.06 9.00 Three-toothed Cinquefoil 0.17 0.00
Arrow-leaved Tear-thumb 1.72 0.20 Prostate knotweed 0.17 0.00
Chickweed 1.72 0.50 Black-eyed Susan 0.17 0.20
Meadow goat’s-beard 1.55 0.30 Night-flowering catchfly 0.17 0.30
White clover 1.55 0.80 Corn spurry 0.17 0.20
Umbellate Aster 1.37 0.30 Common valerian 0.17 0.00
Alfalfa 1.37 0.20 Wormseed mustard 0.17 0.20
Ox-eye daisy 1.37 0.90 Grapevine 0.17 0.20
Green foxtail 1.37 0.60
a
Percentage of quadrat in which the plant was found.
b
Solanaceae.
24 B. Mimee et al. / Crop Protection 55 (2014) 21e27

multiplication on weeds compared to multiplication on ‘Desirée’. A

score was also attributed to each species based on their relative
susceptibility with a score of 1 indicating very high level of sus-
ceptibility and 9 a very high level of resistance (multiplication rate
less than 1% of control) (EPPO, 2006). Relative standard deviation (%
RSD), was calculated by dividing the standard deviation by the
average cyst count and multiplying by 100.

3. Results

3.1. Weed survey

3.1.1. Inventories
Due to quarantine measures, producers in the St-Amable region
were restricted from growing potatoes in 2008. Of the 21 fields in
cultivation, 19 were planted with maize and two with soybean. Two
meadows and the AAFC experimental site (planted with susceptible Fig. 1. Reduction in weed species richness and diversity between 2008 and 2011 in the
potato) were also included in the survey. Weed inventory for all the field margins (n ¼ 512). An asterisk indicates a significant difference between years
fields is listed in Table 1. The most common species were field according to the t-test (p ¼ 0.001).

horsetail (Equisetum arvense L.); tufted vetch (Vicia cracca L); quack
grass [Elymus repens (L.) Gould subsp. repens (synonym: Agropyron
out of 23 fields. In the remaining fields, the frequency of occurence
repens (L.) P. Beauv.)]; common ragweed (Ambrosia artemisiifolia L.);
didn’t change, and in one case, the Solanaceae were less frequent in
common reed (Phragmites australis (Cav.) Trin. ex Streud.); and
2011 than in 2008. While the presence of S. sarrachoides increased
yellow nut sedge (Cyperus esculentus L.).
over time in a number of points, the average percent cover value
In 2011, growers in the quarantine area were allowed to grow
when the species was detected was not significantly different be-
potato for the first time since the discovery of PCN but had to use
tween 2008 and 2011 (p ¼ 0.31). It was not possible to statistically
resistant cultivars. Of the 21 fields in commercial production, four
evaluate the change in S. tuberosum, because of the small number of
were planted with potatoes, one producer decided to grow hemp
occurrences: the plant was only detected three times in 2011,
while the remaining fields were in maize. The most common spe-
covering on average 32% of the quadrats where it was found.
cies for 2011 were field horsetail; yellow nut sedge, large crab grass
(Digitaria sanguinalis (L.) Scop.); common ragweed; lamb’s-quar-
3.1.4. Changes in patch size and aggregation
ters (Chenopodium album L.); yellow foxtail (Setaria pumila (Poiret)
There was a total of 264 points where Solanaceae were found in
Roemer & Schultes subsp. pumila) tufted vetch; and common reed.
the field margins in 2008, compared to 390 in 2011, 85 of which
Approximately two thirds of the weed species found in field
were the same. In other words, a third (32%) of the points contained
margins occurred less often in 2011 than in 2008, with the greatest
Solanaceae in both 2008 and 2011. Overall, the average patch size
diminution observed for the tufted vetch (24%), quack grass
was similar in 2008 and 2011, for all patches (t-test, p ¼ 0.23), and
(24%), Canada goldenrod (Solidago canadensis L.) (14%), common
for the patches greater than one unit (t-test, p ¼ 0.08). Similarly, the
reed (12%) and perennial sow-thistle (Sonchus arvensis L.) (11%).
average number of patches per field was similar between the two
The large crab grass (þ16%) and the yellow nuts edge (þ12%)
years (t-test, p ¼ 0.16) (Table 2). This is mainly due to a split be-
showed the greatest increase between 2008 and 2011.
tween the number of fields which experienced an augmentation in
patch size (8) and/or number (10) between 2008 and 2011, and
3.1.2. Biodiversity
fields where there was a reduction in the average patch size (10)
Not surprisingly, weed species richness and diversity were also
and/or number (6) (Fig. 3) over the same period.
significantly greater (p < 0.001) in 2008 than in 2011 in the field
margins (Fig. 1), the greatest number of species being found in one
of the two meadows (8.60  0.64) in 2008, and the smallest
number in field 4, one of the fields planted with potatoes in 2011
(0.81  0.14). The survey year, surrounding and immediate envi-
ronment as well as type of culture in field margin only explained a
small (axis 1: 3.07%, p ¼ 0.005; axis 2: 1.52%, p ¼ 0.005) proportion
of the variation in the weed community composition. The statistical
significance is likely a consequence of the high number of points
recorded rather than an ecologically meaningful pattern, thus we
refrained to interpreting it further.

3.1.3. Changes in occurrence and cover of Solanaceae in field

margins
Species of Solanum were only found in a few quadrats in 2008.
The two species encountered were S. sarrachoides in 2.06% of the
quadrats and volunteer S. tuberosum in 0.17% of the observations. In
2011, the presence of S. sarrachoides had increased to 9% while Fig. 2. Change in frequency of Solanaceae recorded in the quadrats during weed
S. tuberosum were observed in 0.5% of the quadrats (Table 1). survey in the different field margins, for all fields, and for the two species (black bars:
Sol_sar ¼ Solanum sarrachoides; Sol_tub ¼ Solalum tuberosum) between 2008 and 2011.
The frequency of occurrence of Solanaceae in the field margins Negative value indicates a decrease in the frequency, positive values indicate an in-
increased significantly between 2008 and 2011 (p ¼ 0.0003) crease in frequency. Fields with potatoes as the crop in the 2011 rotations are identified
(Fig. 2). More specifically, the Solanaceae were more frequent in 17 in grey.
 B. Mimee et al. / Crop Protection 55 (2014) 21e27 25

Table 2
Number (N) and size of patches of Solanaceae in the field margins. The size represents the number of consecutive points (within 15 m) with a record of Solanaceae. The mean
size was calculated both including (all) and excluding (>1) the isolated points. SE ¼ Standard Error, NA ¼ Not Available (e.g.  1 point or patch).

Field 2008 2011

N Mean size (all) SE Mean size (>1) SE N Mean size (all) SE Mean size (>1) SE

1 Maize 0 0.00 NA 0.00 NA Maize 0 0.00 NA 0.00 NA

2 Maize 7 5.00 1.50 5.00 1.50 Maize 11 3.36 1.52 6.20 3.01
3 Maize 1 1.00 NA 0.00 NA Maize 9 1.67 0.33 3.00 0.00
4 Soybean 0 0.00 NA 0.00 NA Potato 20 6.30 1.09 6.58 1.11
5 Maize 0 0.00 NA 0.00 NA Maize 0 0.00 NA 0.00 NA
6 Maize 1 1.00 NA 0.00 NA Maize 1 1.00 NA 0.00 NA
7 Maize 4 5.25 1.97 5.25 1.97 Maize 0 0.00 NA 0.00 NA
8 Maize 3 7.00 3.06 10.00 1.00 Maize 6 6.00 3.83 8.50 5.52
9 Maize 0 0.00 NA 0.00 NA Potato 13 3.15 0.60 4.50 0.57
10 Maize 10 3.40 0.99 5.00 1.29 Maize 4 2.50 0.50 3.00 0.00
11 Maize 1 1.00 NA 0.00 NA Potato 8 1.75 0.75 7.00 NA
12 Maize 1 1.00 NA 0.00 NA Potato 0 0.00 NA 0.00 NA
13 Maize 7 3.00 1.21 4.50 1.85 Maize 12 4.17 1.25 5.22 1.52
14 Soybean 0 0.00 NA 0.00 NA Maize 1 1.00 NA 0.00 NA
15 Maize 9 3.11 1.15 5.75 1.93 Maize 9 1.11 0.11 2.00 NA
16 Maize 0 0.00 NA 0.00 NA Maize 1 1.00 NA 0.00 NA
17 Maize 6 1.50 0.50 4.00 NA Hemp 2 2.50 1.50 4.00 NA
18 Maize 13 4.08 1.47 6.00 2.15 Maize 10 1.70 0.21 2.17 0.17
19 Maize 2 1.00 0.00 0.00 NA Maize 2 1.00 0.00 0.00 NA
20 Potato 6 4.17 1.40 4.80 1.53 Potato 2 1.00 0.00 0.00 NA
21 Maize 2 3.00 2.00 5.00 NA Maize 2 3.00 1.00 3.00 1.00
22 Maize 3 2.00 0.58 2.50 0.50 Maize 9 1.56 0.34 2.67 0.67
23 Meadow 0 0.00 NA 0.00 NA Meadow 0 0.00 NA 0.00 NA
24 Meadow 0 0.00 NA 0.00 NA Meadow 0 0.00 NA 0.00 NA
Total 76 3.48 0.42 5.30 2.25 122 3.25 0.37 5.09 2.67

3.2. Host susceptibility to G. rostochiensis 3 (score 7). Among the S. nigrum accessions, only PI304600 allowed
the production of a few cysts (pf/pi ¼ 0.5, score 8) while the local
Among the weeds tested, four species were fully resistant (EPPO strain from St-Amable was fully resistant. Only a few cysts were
score ¼ 9) to the Quebec population of G. rostochiensis: produced on S. sarrachoides. Among the species tested, S. villosum
S. carolinense, S. ptycanthum, S. rostratum, and S. sisymbriifolium allowed the greatest rates of reproduction (pf/pi up to 1.2, score 7),
(Table 3, and Table 4 for comparison with other Canadian pop- although very limited compared with S. tuberosum (pf/pi > 20,
ulations of G. rostochiensis). The three strains of S. dulcamara were score 2). However, the results were very variable among the rep-
resistant except for one plant of PI 643457 that showed a pf/pi over licates (% RSD of 231 for S. villosum 914750047) and some individual
plants supported much higher G. rostochiensis development.

Table 3
Susceptibility of different Solanum species to Globodera rostochiensis.

Solanum species Accession Pf/Pia Rel suc %b Scorec %RSDd

S. carolinense 894750095 0 <1 9 0

S. dulcamara Ottawa, ON 0e <1 9 245
S. dulcamara PI 643457 0.5 1.8 8 235
S. dulcamara PI 645684 0.2 <1 9 200
S. nigrum St-Hyacinthe, QC 0 <1 9 0
S. nigrum PI304600 0.5 1.8 8 93
S. nigrum PI381290 0 <1 9 0
S. ptycanthum A64750068 0 <1 9 0
S. rostratum PI 420997 0 <1 9 0
S. sarrachoides 954750073 0e <1 9 224
S. sisymbriifolium 894750017 0 <1 9 0
S. tuberosum cv. Snowden 23.1 86.0 2 39
S. tuberosum cv. Désirée 26.9 100 2 48
S. tuberosum cv. Andover 0e <1 9 245
S. villosum 884750018 0e <1 9 245
S. villosum 914750047 0.4 1.3 8 231
S. villosum 804750186 0.2 <1 9 100
S. villosum 814750090 1.2 4.3 7 116
a
Pf/Pi is the multiplication rate expressed as the ratio between final population
(Pf) divided by initial population (Pi) both expressed as number of cysts.
b
Rel Suc % is the relative susceptibility of each Solanum compared to the sus-
ceptible potato cv. ‘Desirée’.
c
Score is attributed based on Rel Suc % with a score of 1 indicating very high level
of susceptibility and 9 full resistance.
d
%RSD is the relative standard deviation calculated by dividing the standard
Fig. 3. Evolution of patch size and number between 2008 and 2011 in the field deviation by the average cyst count and multiplying by 100.
e
margins. Some cysts were found on individual plant; not a full resistance.
26 B. Mimee et al. / Crop Protection 55 (2014) 21e27

Table 4 recommendations are not fully followed. Thus, the utilization of a

Level of susceptibility (EPPO scorea) of different Solanum species to three different single application of glyphosate to control weeds in the regulated
Canadian populations of Globodera rostochiensis.
area could have promoted the growth and proliferation of these
Solanum species Accession Populationsb annual species.
NFLDc BCc QC On the other hand, the utilization of glyphosate has reduced the
occurrence of the majority of the other species, thus reducing the
S. carolinense 894750095 9 9 9
S. dulcamara Ottawa, ON 7 4 9 number of points with weeds and the number of weeds at each
S. dulcamara PI643457 9 6 8 point. Consequently, the weed species richness and diversity was
S. dulcamara PI645684 9 5 9 significantly reduced in the second inventory. It is interesting to
S. nigrum PI304600 3 9 8
note that the lowest weed species richness (0.81  0.14) was found
S. nigrum PI381290 8 9 9
S. ptycanthum A64750068 9 9 9 in a field where there has been a sudden rise in S. sarrachoides and
S. rostratum PI 420997 9 9 9 where potatoes were grown in 2011. If nightshade abundance was
S. sarrachoides 954750073 9 9 9 promoted during the years when glyphosate was used because of
S. sisymbriifolium 894750017 9 9 9 its late emergence, it is not surprising to see the population of
S. villosum 884750018 4 9 9
S. sarrachoides increase even more when potatoes are grown and
S. villosum 914750047 4 9 8
S. villosum 804750186 2 9 9 herbicides are not targeting Solanum at all.
S. villosum 814750090 3 9 7 While the number of points with S. sarrachoides increased over
a
Scores indicate the level of susceptibility, 1 being susceptible and 9 fully time, the average percent cover value was not significantly different
resistant. between 2008 and 2011, suggesting an increase in the number of
b
NFLC ¼ Newfoundland, Canada; BC ¼ British Columbia, Canada; QC ¼ Quebec, similarly sized plants, rather than an increase in the size of the
Canada. plants between the two years. Experimental site (20) is the only
c
Results from Rott et al. (2011).
field where potatoes were grown in 2011 that showed a diminution
in the number and size of patches with Solanaceae. This site was
4. Discussion never used to grow RR corn and always received appropriate weed
control treatments, which further supports the possible connection
Enforcement of quarantine procedures following the discovery of glyphosate with the proliferation of S. sarrachoides.
of G. rostochiensis in the province of Quebec, Canada in 2006 has A paradoxical effect of the introduction of plant quarantine
considerably modified the way growers use their fields. While measures is the increase of machinery movement and hence the
numerous reports support the efficacy of these procedures for the spread of weeds and other inoculum. Indeed, the producers who
limitation of PCN inoculum and spread (Rott et al., 2010; USDA cultivated potato for decades have had to turn to alternative crops
APHIS PPQ, 2011), it is of interest to examine the indirect effects for which they were not equipped. As a result, most have chosen to
of a rapid change in field usage and management practices. In the cultivate their fields under contract by farmers from outside the
case of PCN, weed control is probably the most important factor to area where the soils are more suitable for growing corn and soy-
consider as certain species have been reported as potential hosts bean. Weeds such as nightshade have an increased presence in
and could serve as a reservoir for nematodes, thus limiting quar- these crops than was found in the areas of potato production before
antine outcomes (Bates, 1945; Boydston et al., 2010; Rott et al., quarantine restrictions were implemented. The law requires pro-
2011; Sullivan et al., 2007). ducers to clean their machinery before leaving the quarantine area
Between 2008 and 2011, the occurrence of several weed species but there is no obligation upon entry. Therefore, it is easy to
has considerably changed. These changes could be explained by the speculate that the multiplication of Solanum has been caused or at
method of weed control associated with crops planted during the least facilitated by the supply of seed from outside the area.
quarantine which consisted primarily of Roundup Ready (RR) corn Our results with the Solanum host range of the Quebec strain of
(Personal communication from producers and agronomists). These G. rostochiensis are consistent with those obtained by Rott et al.
crops allow the application of glyphosate in a single pass and (2011). S. dulcamara allowed a slight multiplication of the Quebec
suppress annual and perennial species at lower cost compared with strain of G. rostochiensis, similar to the multiplication rate of the
more focused herbicides involving a mixture of several active in- Newfoundland population but was less susceptible to these nem-
gredients (Gianessi, 2005). It is recognized that glyphosate effec- atodes in comparison with the British Columbia population tested
tively suppresses quack grass, the perennial sow-thistle, common by Rott et al. (2011) (see Table 4 for comparison). For S. nigrum, we
milkweed and dandelion, but has no effect on the field horsetail observed a low reproduction (score 8) on PI304600, the same
and only a limited action on the yellow nut sedge (CPVQ, 2000; accession that is highly susceptible (score 3) to the Newfoundland
MAAARO, 2012). This could explain the changes observed for population but does not support the reproduction of the British
these species. However, the effect of glyphosate is not as well Columbia isolate (score 9). S. villosum was found to be slightly
documented for other species (tufted vetch, common reed, Canada susceptible to G. rostochiensis from Quebec (score 8) while the
goldenrod). Glyphosate very effectively suppresses annual grasses Newfoundland isolate reproduces well on S. villosum (4) and
and broadleaf weeds when they are present at application, but as S. villosum is totally resistant to G. rostochiensis from British
this herbicide has no residual activity, it cannot inhibit late Columbia. Overall, the host range of the PCN population from
germinating weeds such as nightshade or annuals (large crab grass, Quebec was found to be more similar to the population from
yellow foxtail, witch grass, lamb’s-quarters) that germinate after Newfoundland although multiplication rates were less significant.
application. For example, the optimum germination for hairy This result is in agreement with the recent finding by Boucher et al.
nightshade occurs between 27 and 33  C (Zhou et al., 2005). Rec- (2013) that PCN found in Quebec are genetically distinct from
ommendations expound the use of a residual herbicide combined populations in British Columbia.
with glyphosate to control late germinating weeds such as black Four species of nightshade have been recorded in the past in the
nightshade (Roundup label, Monsanto Canada Inc, 2012). However, province of Quebec: S. nigrum, S. dulcamara, S. sarrachoides and
in the context of quarantine procedures, especially during the first Solanum pseudo-capsicum (Doyon et al., 1987; Lemieux, 1988).
years when producers are compensated monetarily by the Among these species, S. dulcamara could function as a host for local
government, investment in time and money is reduced and PCN in our greenhouse assay but the multiplication rate was low.
 B. Mimee et al. / Crop Protection 55 (2014) 21e27 27

However, other studies have reported high susceptibility of Boydston, R.A., Mojtahedi, H., Bates, C., Zemetra, R., Brown, C.R., 2010. Weed hosts of
Globodera pallida from Idaho. Plant Dis. 94, 918.
S. dulcamara and this species should be surveyed as the PCN
CPVQ, 2000. Traitements Herbicides. Grandes cultures 2000. Conseil des pro-
multiplication rate could be very different on native specimens. ductions végétales du Québec, p. 358.
Similarly, S. sarrachoides was a poor host for G. rostochiensis in our Crotser, M.P., Witt, W.W., 2000. Effect of Glycine max canopy characteristics, G. max
study but has already been reported as a good host for PCN (Bates, interference, and weed-free period on Solanum ptycanthum growth. Weed Sci.
48, 20e26.
1945) and should be monitored carefully. This is particularly Doncaster, C.C., 1953. A study of host-parasite relationships. The potato root
important since our study suggests that S. sarrachoides may become eelworm (Heterodera rostochiensis) in black nightshade (Solanum nigrum) and
a dominant weed species in the field margins. S. nigrum is known to tomato. J. Helminthol. 27, 1e8.
Doyon, D., Néron, R., Bouchard, C.J., 1987. Inventaire des mauvaises herbes dans les
be resistant to PCN (Boydston et al., 2010). However, Rott et al. cultures du Québec (1980e1984).
(2011) have identified two strains (PI304600 and PI381290) with European Plant Protection Organization, 2006. Testing of potato varieties to assess
unusual phenotype that were susceptible to the Newfoundland resistance to Globodera rostochiensis and Globodera pallida. EPPO Bull. 36, 419e
420.
population. This highlights the importance of testing the potential Fenwick, D.M., 1940. Methods for the recovery and counting of cysts of Heterodera
of a given weed to be a good host with local plant strains as schachtii from soil. J. Helminthol. 18, 155e172.
reference accessions may not be representative of what may be Gianessi, L.P., 2005. Economic and herbicide use impacts of glyphosate-resistant
crops. Pest Manag. Sci. 61, 241e245.
happening in the field. Grenier, E., Fournet, S., Petit, E., Anthoine, G., 2010. A cyst nematode ‘species factory’
The highest reproduction rate of the Quebec PCN population called the Andes. Nematology 12, 163e169.
was observed on S. villosum. While this species has not been found Legendre, P., Gallagher, E.D., 2001. Ecologically meaningful transformations for
ordination of species data. Oecologia 129, 271e280.
in our inventory or anywhere else in Canada, it is present in several
Lemieux, C., 1988. Inventaires des mauvaises herbes au Québec: cultures céréal-
American states, including northeastern ones (NRCS, 2013), and ières. Station de recherches. Direction générale de la recherche. Agriculture
could probably survive in some parts of Canada especially with the Canada.
expected rise of temperature related to climate change. MAAARO, 2012. Guide de lutte contre les mauvaises herbes 2012e2013. Publication
75F. Ministère de l’agriculture, de l’alimentation et des affaires rurales de
This study has shown the importance of monitoring the di- l’Ontario, p. 464.
versity and occurrence of weed species at the margin of fields when Mahran, A., Turner, S., Martin, T., Yu, Q., Miller, S., Sun, F., 2010. The golden potato
implementing quarantine procedures. Modification in weed control cyst nematode Globodera rostochiensis pathotype Ro1 in the Saint-Amable
regulated area in Quebec, Canada. Plant Dis. 94, 1510.
regimes in the field associated with drastic change in field usage Majek, B.A., 1981. Nightshade identification and controls. Weeds Today 12, 5.
could have a major impact on the composition of this ecosystem. Monsanto Canada Inc, 2012. Roundup WeatherMAX Transorb 2 Technology Label.
The multiplication of pest refuges could hamper the success of any National Resources Conservation Services, 2013. United States Department of
Agriculture, National Resources Conservation Service, Plants Database. http://
regulatory procedures. The recent appearance of G. rostochiensis in plants.usda.gov/.
the province of Quebec and the installation of a quarantine area Oksanen, J., Kindt, R., Legendre, P., O’Hara, B., Simpson, G.L., Solymos, P.,
offers the unique opportunity to monitor these changes and should Stevens, M.H.H., Wagner, H., 2008. Vegan: Community Ecology Package. R
Package Version 1.15-0. Available at: http://cran.r-project.org/.
be continued over several years. Olsenand, O.A., Mulvey, R.H., 1962. The discovery of golden nematode in
Newfoundland. Can. Plant Dis. Surv. 42, 253.
Acknowledgements Orchard, W.R., 1965. Occurence of the golden nematode on Vancouver Island,
British Columbia. Can. Plant Dis. Surv. 45, 89e91.
Prummel, W., 1958. Solanum nigrum L. as a host of the potato root eelworm, Het-
The authors would like to thank Michelle Breton and Élise erodera rostochiensis Wollenweber. Tijdschr. Plantenziekten 64, 142e143.
Tremblay from Groupe ProConseil and Marie-Édith Cuerrier from Rott, M., Lawrence, T., Belton, M., Sun, F., Kyle, D., 2010. Occurrence and detection of
CÉROM for their meticulous work in weed identification; Eveline Globodera rostochiensis on Vancouver Island, British Columbia: an update. Plant
Dis. 94, 1367e1371.
Mousseau from Groupe ProConseil for giving a significance to all Rott, M., Lawrence, T., Belton, M., 2011. Nightshade hosts for Canadian isolates of
those GPS points; Diane-Lyse Benoit from Agriculture and Agri- Globodera rostochiensis pathotype Ro1. Can. J. Plant Pathol. 33, 410e415.
Food Canada (AAFC) for her invaluable knowledge of weeds; and Sullivan, M.J.I., Franco, J., Moreno-Leheude, I., Greco, N., 2007. Potato cyst nem-
atodes: plant host status and their regulatory impact. Nematropica 37, 193e
Annie Christine Boucher for technical assistance during the prep- 201.
aration of this manuscript. This project was funded by a grant from Sun, F., Miller, S., 2007. Occurrence of potato cyst nematode, Globodera rostochiensis,
the Canadian Food Inspection Agency’s Research Partnership on potato in the Saint-Amable region, Quebec, Canada. Plant Dis. 91, 908.
Turner, S.J., 1996. Population decline of potato cyst nematodes (Globodera ros-
Strategy (RPS) program to Guy Bélair. tochiensis, G. pallida) in field soils in Northern Ireland. Ann. Appl. Biol. 129, 315e
322.
References USDA APHIS PPQ, 2011. Golden Nematode Program 2011, USDA APHIS PPQ.
DEregulation of Quarantined Areas.
Venkatesh, R., Harrison, S.K., Riedel, R.M., 2000. Weed hosts of soybean cyst
Bates, G.H., 1945. An alien weed host of Heterodera rostochiensis in England.
nematode (Heterodera glycines) in Ohio. Weed Technol. 14, 156e160.
J. Helminthol. 21, 104.
Yu, Q., Ye, W., Sun, F., Miller, S., 2010. Characterization of Globodera rostochiensis
Bélair, G., Benoit, D.L., 1996. Host suitability of 32 common weeds to Meloidogyne
(Tylenchida: Heteroderidae) associated with potato in Quebec, Canada. Can. J.
hapla in organic soils of southwestern Quebec. J. Nematol. 28 (Suppl.), 643e647.
Plant Pathol. 32, 264e271.
Boucher, A.C., Mimee, B., Montarry, J., Bardou-Valette, S., Bélair, G., Moffett, P.,
Zhou, J., Deckard, E.L., Ahrens, W.H., 2005. Factors affecting germination of hairy
Grenier, E., 2013. The golden nematode Globodera rostochiensis: inferring the
nightshade (Solanum sarrachoides) seeds. Weed Sci. 53, 41e45.
origin of populations introduced in Quebec, Canada through its worldwide
genetic structure. Mol. Phylo. Evol. 69, 75e82.