agronomy

Article Harvest Weed Seed Control: Seed Production and Retention of Fallopia convolvulus, arvensis, Spergula arvensis and Stellaria media at Spring Oat Maturity

Zahra Bitarafan and Christian Andreasen * Department of and Environmental Sciences, University of Copenhagen, Højbakkegaard Allé 13, DK-2630 Taastrup, ; [email protected] * Correspondence: [email protected]; Tel.: +45-35-333-453

 Received: 21 November 2019; Accepted: 22 December 2019; Published: 28 December 2019 

Abstract: If seeds retained on weeds at crop harvest could be collected and removed by the combine harvester, weed infestation could be reduced in the following years. We estimated the proportion of weed seeds that could be removed at oat harvest. The seed production and shedding pattern of Fallopia convolvulus, Sinapis arvensis, Spergula arvensis and Stellaria media, were assessed in two spring oat fields in Denmark during 2018 and 2019. Ten randomly chosen of each species were surrounded by a porous net before flowering. The start time of seed shedding was recorded, and the seeds were collected from the nets and counted weekly until oat harvest. Just before harvest, the retained seeds on the weed plants were counted. The ratio between harvestable seeds and shed 1 seeds during the growing season was determined. On average 260, 195, 411 and 316 seeds plant− were produced by F. convolvulus, Sinapis arvensis, Spergula arvensis and S. media, respectively, of which in average 44%, 67%, 45% and 56% of the seeds were retained on the plants at harvest. There was a strong, positive correlation between the weed biomass and the total seed production.

Keywords: HWSC; seed shedding; soil seed bank; spring cereals

1. Introduction Black bindweed (Fallopia convolvulus (L.) Á. Löve), wild (Sinapis arvensis L.), chickweed (Stellaria media (L.) Vill.) and corn spurrey (Spergula arvensis L.) are four common weed species in cereal fields in Scandinavia. Based on the Danish weed surveys in 1987–1989 and 2001–2004, F. convolvulus and S. media were among the dominant weed species with a frequency higher than 10% in all fields. Spergula arvensis and Sinapis arvensis became even more frequent in some crops from 1987–1988 to 2001–2004 [1]. Fallopia convolvulus is one of the most troublesome weeds in the world in cereal fields [2]. The climbing habit of the plant allows it to obtain sunlight while growing in stands of grain or other tall crops that may otherwise shade it [3]. The growth of F. convolvulus shoots is positively correlated with the daily temperature curve. However, as days become successively warmer, growth is successively less [4]. A single plant that emerges early in the growing season (April) may produce as many as 30,000 seeds, while individuals emerging two months later (June) may produce 15,000 seeds [2]. Fallopia convolvulus has an indeterminate flowering habit, which can result in flowers, immature seeds and mature seeds present on the same plant [3]. Sinapis arvensis is widely introduced and naturalized in temperate regions around the world. It has a persistent seed bank, a competitive annual growth habit and high fecundity; all characteristics contribute to its weedy nature, and ensure that it will remain a problem. During harvest operations,

Agronomy 2020, 10, 46; doi:10.3390/agronomy10010046 www.mdpi.com/journal/agronomy Agronomy 2020, 10, 46 2 of 10 pods shatter readily, and some seeds are harvested with the crop [5]. Sinapis arvensis flowers six weeks after emergence with the peak in June and July in northern latitudes, but it can continue flowering until 1 the frost starts [6]. The average number of seeds plant− reported for plants grown without competition varied from 2000 to 3500 [7], and in dense plant populations, from 10 to 590 [8]. Seed longevity of up to 75 years has been reported [7]. Stellaria media is native to Europe, and exists as one of the most distributed weeds in the world. It is one of the most common weeds in spring and winter cereals in northern Europe. It quickly colonizes 1 disturbed fields [9], but it is considered as a weak competitor [10]. The number of seeds plant− has been reported to be in the range of 500 [11] to 2500 [12]. It has numerous, small, easily dispersed seeds, and can flower and set seed throughout the year [13]. Spergula arvensis is a weed of cereals in almost all areas of the world. The plant flowers from June to November and will shatter mature seeds from July onward. Flowering and seeding continue until the plant dies. A large plant may have 500 capsules and releases 7500 seeds. Capsules produced early in the season may contain 25 seeds, but later capsules may only contain five [2]. Sinapis arvensis and Spergula arvensis can only reproduce by seeds, while F. convolvulus and S. media also can reproduce by creeping roots and creeping stems rooting at the nodes, respectively [14]. The soil seed bank is the primary source of weed infestations. Thus, information on their seed production and shedding pattern is necessary for applying proper weed management strategies. Weed seeds disperse when the seeds ripen, detach and fall to the ground [15]. Late season production of weed seeds has gained particular attention because of the development of herbicide-resistant weeds [16]. Most farmers adopt weed management programs that are efficient in controlling weeds and preventing weed seed production [17]. At harvest, weed seed control provides an opportunity to collect and destroy weed seeds before their return to the soil seed bank [18]. Chaff carts, narrow windrow burning, bale direct, chaff tramlining and use of the Harrington seed destructor are Harvest Weed Seed Control (HWSC) systems used to collect and/or kill weed seeds at harvest [19–21]. Seed shattering before harvest ensures that seeds escape control at crop harvest, and thereby persist within the field [15]. The amount of weed seeds shattered before harvest varies among weed species, and is influenced by environmental conditions and agronomic factors [22,23]. The effect of HWSC methods depends on the seed retention of the target species [23] and canopy height at which the weed seeds are retained relative to crop harvest height [24]. The objective of this study was to evaluate the seed production, shedding and retention of four of the most common weed species in conventional and organic oat fields in Denmark. We assessed the potential to harvest their seeds during grain harvest by a combine harvester as a weed seed control strategy to reduce the fresh seed input to the soil seed bank. We hypothesized that a significant fraction of their seeds potentially could be collected and removed from the field during crop harvesting.

2. Materials and Methods We assessed the seed shattering and seed production of Fallopia convolvulus, Sinapis arvensis, Spergula arvensis and Stellaria media during the growing season of spring oat in two fields with sandy soil at the research station in Taastrup (55◦380 N, 12◦170 E), Denmark. The fields were ploughed in the spring and harrowed before sowing. One field was sown 19 April and harvested 2 August 2018 and the other field was sown 2 April and harvested 23 August 2019. The oat cultivar was Dominik and 1 Symphony in 2018 and 2019, respectively, with the sowing rate of 170 and 175 kg ha− . No pesticide or fertilizer was applied both years on the study. Ten plants of each species were selected randomly and surrounded by a trap comprised of a porous net (precision woven open mesh fabrics: SEFAR NITEX 06-475/56, Sefar, ; mesh opening: 475 µm—opening area: 56%) before flowering covering an area of approximate 710 cm2 (Figure1). Traps were checked each week to record the start time of seeds shedding. Hereafter, seeds were collected using a portable vacuum cleaner every 6 8 days, depending on weather conditions, − and stored in paper bags. The collected seeds were counted until oat harvest. Just before crop harvest, Agronomy 2020, 10, x FOR PEER REVIEW 3 of 11 Agronomy 2020, 10, 46 3 of 10 weedAgronomy plants 2020 were, 10, x cutFOR atPEER the REVIEW soil surface, and the number of seeds retained on the weed plants3 of 11was counted. The ratio of harvestable seeds to seeds produced by each weed species was determined. weedweed plants plants were were cut cut at at the the soilsoil surface,surface, and the number number of of seeds seeds retained retained on on the the weed weed plants plants was was counted. The ratio of harvestable seeds to seeds produced by each weed species was determined. counted. The ratio of harvestable seeds to seeds produced by each weed species was determined.

Figure 1. (a) Seed traps in the oat field in 2018. Maturing plants and shattered seeds of (b) Stellaria FigureFigure 1. 1.(a ()a Seed) Seed traps traps in in the the oat oat field field in 2018.in 2018. Maturing Maturing plants plants and and shattered shattered seeds seeds of (ofb) (Stellariab) Stellaria media media and (c) Fallopia convolvulus in traps in 2019. andmedia (c) Fallopiaand (c) Fallopia convolvulus convolvulusin traps in in traps 2019. in 2019. Weather data was provided from the research weather station in the area (55°67′ N, 12°30′ E) WeatherWeather data data was was provided provided fromfrom thethe research weather station station in in the the area area (55°67 (55◦67′ N,0 N, 12°30 12◦′ 30E)0 E) (Figure 2). Daily maximum and minimum temperature data were used to calculate the Growing (Figure(Figure2). 2). Daily Daily maximum maximum and and minimumminimum temperaturetemperature data data were were used used to to calculate calculate the the Growing Growing DegreeDegreeDegree Days Days Days (GDD) (GDD) (GDD) for for for the the the growing growing growing seasons: seasons:seasons: 𝐺𝐷𝐷XS2 𝑇𝑚 𝑏 (1) 𝐺𝐷𝐷 𝑇𝑚 𝑏 (1) GDD = (Tm b0) (1) − S1 wherewhere Tm Tm and and b0 brepresent0 represent the the mean mean daily daily temperature temperature andand thethe base base temperature temperature (0 (0 °C), °C), respectively. respectively. Swhere1 Sand1 and TmS2 S are2and are theb the0 timerepresent time of of crop crop the sowing meansowing daily and and harvesting, temperatureharvesting, respectively. and the base temperature (0 ◦C), respectively. S1 and S2 are the time of crop sowing and harvesting, respectively.

25 25 2018 2019 55 55 2018 2019 2018 2019 ) 2018 2019 2018 2019 ) 2018 2019 ͦ C) ͦ C) 2020 4 4 4 mm 4 mm ( ( 1515 33 33

10 2 itation 2

10 2 itation 2 p p Wind (m/s)

5 Wind (m/s) 1 1

Temperature ( Temperature 5 1 1 Preci Temperature ( Temperature

0 0 Preci 0 0 0 0 45678 45678 45678 (a) 45678 (b) 45678(c) 45678 (a) Month (b) Month (c) Month Month Month Month FigureFigure 2. 2.Weather Weather datadata duringduring thethe experiments: (a ()a )temperature, temperature, (b ()b wind) wind and and (c) (cprecipitation.) precipitation. Figure 2. Weather data during the experiments: (a) temperature, (b) wind and (c) precipitation. MeasurementMeasurement height: height: 2,2, 22 andand 1.5 m above ground ground level level for for temperature, temperature, wind wind and and precipitation, precipitation, Measurement height: 2, 2 and 1.5 m above ground level for temperature, wind and precipitation, respectively.respectively. respectively. ToTo test test whether whether the the total total seed seed production production and and dry weightdry weight of the of plants the plan variedts varied significantly significantly between thebetween years,To test analysisthe whether years, of analysisthe variance total of seed (ANOVA)variance production (ANOVA) followed and followed by dry Fisher’s weight by leastFisher’s of the significant leastplan significantts varied difference significantlydifference (LSD) for betweenmeans(LSD) separation forthe means years, separation was analysis done usingofwas variance done R version using (ANOVA) R 3.6.1 version [25 followed]. 3.6.1 Variance [25]. by Variance homogeneityFisher’s homogeneity least wassignificant assessed was assesseddifference by visual (LSD)inspectionby visual for means ofinspection residual separation of plots. residual was To done testplots. whether using To test R whether seedversion shed seed3.6.1 di ffshed [25].ered differedVariance between between homogeneity the weeks the weeks for was each for assessed species,each byrepeated species,visual inspection measurement repeated measurement of residual was used. plots. was The used. To analyses test The whether anal wereyses done seed were usingshed done differed the using extension the between extension packages the packages weekslme4 for[ 26lme4 ]each and species,multcomp[26] and repeated[ multcomp27]. Plants measurement [27]. were Plants considered werewas used. considered as The random anal as randomyses effect, were and effect, done the and number using the thenumber of extension shattered of shattered packages seeds overseeds lme4 the over the weeks considered as the response. The significance level was set to 0.05. The relationship [26]weeks and considered multcomp [27]. as the Plants response. were considered The significance as random level waseffect, set and to 0.05.the number The relationship of shattered between seeds between weed seed production and biomass was assessed using linear regression analysis. overweed the seed weeks production considered and biomassas the response. was assessed The significance using linear level regression was set analysis. to 0.05. The relationship between weed seed production and biomass was assessed using linear regression analysis.

Agronomy 2020, 10, 46 4 of 10

Agronomy 2020, 10, x FOR PEER REVIEW 4 of 11 Agronomy 2020, 10, x FOR PEER REVIEW 4 of 11 3. Results 3. Results 3. Results 3.1. Seed Production and Shedding in 2018 3.1. Seed Production and Shedding in 2018 3.1. Seed Production and Shedding in 2018 F. convolvulus Sinapis arvensis Spergula arvensis FiguresFigures3–5 show 3–5 show the seed the sheddingseed shedding pattern pattern of of F. convolvulus, , Sinapis arvensisand and Spergula , Figures 3–5 show the seed shedding pattern of F. convolvulus, Sinapis arvensis and Spergula respectively.arvensis, respectively All three species. All three started species seed started shedding seed shedding more than more one than week one week before before oat harvestoat harvest in 2018. arvensis, respectively. All three species started seed shedding more than one week before oat harvest Fallopiain 2018. convolvulus Fallopia convolvulusstarted to started shed seeds to shed between seeds between 12–19 12–19 July, andJuly, theandlargest the largest number number of of shed shed seeds in 2018. Fallopia convolvulus started to shed seeds between 12–19 July, and the largest number of shed took placeseeds took in the place week in the before week harvest before (26harvest July–1 (26 August)July–1 August) (Figure (Figure3a). Seed 3a). sheddingSeed shedding of Sinapis of Sinapis arvensis seeds took place in the week before harvest (26 July–1 August) (Figure 3a). Seed shedding of Sinapis startedarvensis between started 20–27 between July. 20–27 The largest July. The number largest of number seeds wasof seeds shed was between shed between 27 July–2 27 July–2 August, August, one week arvensis started between 20–27 July. The largest number of seeds was shed between 27 July–2 August, beforeone harvest week before (Figure harvest4a). (FigureSpergula 4a). arvensis Spergulastarted arvensis seed started shedding seed shedding between between 26 June–3 26 June–3 July, July, and the one week before harvest (Figure 4a). Spergula arvensis started seed shedding between 26 June–3 July, and the greatest number of shed seeds took place between 9–16 July (Figure 5a). On average 200, 109 greatestand numberthe greatest of number shed seeds of shed took seeds place took between place betw 9–16een July9–16 July (Figure (Figure5a). 5a). On On average average 200, 200, 109109 and and 697 seeds1 plant−1 were produced by F. convolvulus, Sinapis arvensis and Spergula arvensis, 697 seedsand 697 plant seeds− were plant produced−1 were produced by F. convolvulus by F. convolvulus, Sinapis, arvensisSinapis andarvensisSpergula and Spergula arvensis ,arvensis respectively,, respectively, of which 57.5%, 27.7% and 39.0% of the seeds were shed before harvest. The difference of whichrespectively, 57.5%, 27.7%of which and 57.5%, 39.0% 27.7 of% the and seeds 39.0% were of the shed seeds before were shed harvest. before The harvest. difference The difference between the between the weekly numbers of shed seeds for these three species was statistically significant (p = between the weekly numbers of shed seeds for these three species was statistically significant (p = weekly0.001). numbers of shed seeds for these three species was statistically significant (p = 0.001). 0.001). Fallopia convolvulus 2019 Fallopia convolvulus 2018 Fallopia convolvulus 2019 Fallopia convolvulus 2018 200 Weekly shattered seeds 200 WeeklyTotal shattered shattered seeds seeds 200 Weekly shattered seeds Total shattered seeds 200 Weekly shattered seeds Total shattered seeds 150 Total shattered seeds 150 150 150 100 100 100 a 100 bc a a a 50 bc bc a seeds of Number 50 bc d 50 a b e Number of seeds of Number d Number of seeds of Number 50 b f e Number of seeds of Number 0 f 0 0

0 19-Jul 26-Jul

(b) 3-Aug 9-Aug 16-Aug 23-Aug 19-Jul 26-Jul

(b) 3-Aug 9-Aug 19-Jul 26-Jul

(a) 1-Aug

GDD 1418 1555 1708 1816 193716-Aug 205623-Aug

19-Jul 26-Jul (a) 1-Aug GDD 1418 1555 1708 1816 1937 2056 GDD 1406 1559 1698 GDD 1406 1559 1698 Figure 3. Average weekly and cumulative seed shedding per plant of Fallopia convolvulus in (a) 2018 FigureFigure 3. Average 3. Average weekly weekly and and cumulative cumulative seed seed shedding shedding per per plant plant of ofFallopia Fallopia convolvulusconvolvulus inin ( (aa)) 2018 2018 and and (b) 2019 during the growing season of spring oat. GDD = Growth Degree Days = sum of daily (b) 2019and during(b) 2019 the during growing the growing season season of spring of spring oat. GDD oat. GDD= Growth = Growth Degree Degree Days Days= sum= sum of of daily daily mean mean temperatures above 0 from the date the oat was sown. Columns with different letters are temperaturesmean temperatures above 0 from above the 0 datefrom thethe oatdate was the sownoat was. Columns sown. Columns with di ffwitherent different letters areletters statistically are statistically different at the 0.05 probability level. differentstatistically at the 0.05different probability at the 0.05 level. probability level. Sinapis arvensis 2019 Sinapis arvensis 2018 Sinapis arvensis 2019 Sinapis arvensis 2018 150 Weekly shattered seeds 150 150 WeeklyTotal shattered shattered seeds seeds Weekly shattered seeds 150 Total shattered seeds WeeklyTotal shattered shattered seeds seeds Total shattered seeds a 100 a 100 100 100

50 50 b 50 a seeds of Number b 50 c a seeds of Number c Number of seeds of Number b 0 Number of seeds of Number b 0 0 0 (b) 9-Aug 16-Aug 23-Aug 9-Aug

27-Jul (b) 2-Aug (a) GDD 1816 193716-Aug 205623-Aug

27-Jul (a) 2-Aug GDD 1583 1719 GDD 1816 1937 2056 GDD 1583 1719 Figure 4. Average weekly and cumulative seed shedding per plant of Sinapis arvensis in (a) 2018 and Figure 4. Average weekly and cumulative seed shedding per plant of Sinapis arvensis in (a) 2018 and Figure(b) 4. 2019Average during weekly the growing and cumulativeseason of spring seed oat. shedding GDD = Growth per plant Degree of Sinapis Days = arvensis sum of dailyin (a )mean 2018 and (b) 2019 during the growing season of spring oat. GDD = Growth Degree Days = sum of daily mean (b) 2019 during the growing season of spring oat. GDD = Growth Degree Days = sum of daily mean temperatures above 0 from the date the oat was sown. Columns with different letters are statistically

di fferent at the 0.05 probability level. Agronomy 2020, 10, 46 5 of 10

Agronomy 2020, 10, x FOR PEER REVIEW 6 of 11 Agronomy 2020, 10, x FOR PEER REVIEW 6 of 11 Spergula arvensis 2019 Spergula arvensis 2018 Spergula arvensis 2019 300 Spergula arvensis 2018 Weekly shattered seeds 300 Weekly shattered seeds Total shattered seeds 250300 Weekly shattered seeds Total shattered seeds 300 Weekly shattered seeds Total shattered seeds 250 250 Total shattered seeds 200 200250 150200 150200 100150 150 100 a a a 100 Number of seeds of Number 50 d d bb a b d 100 a a abc bc ab Number of seeds of Number 50 a Number of seeds of Number 500 d d b bb abc a d bc ab Number of seeds of Number 500

0 1-Jul 9-Jul

(b) 16-Jul 24-Jul 31-Jul 6-Aug 14-Aug 22-Aug

0 3-Jul 9-Jul

GDD 11361-Jul 12499-Jul 1365 1512 1658 1763 1904 2037 (a) 16-Jul 23-Jul 31-Jul

(b) 16-Jul 24-Jul 31-Jul 6-Aug GDD 1097 1207 1344 1486 1676 14-Aug 22-Aug 3-Jul 9-Jul GDD 1136 1249 1365 1512 1658 1763 1904 2037 (a) 16-Jul 23-Jul 31-Jul GDD 1097 1207 1344 1486 1676 Figure 5. Average weekly and cumulative seed shedding per plant of Spergula arvensis in (a) 2018 and Figure 5. Average weekly and cumulative seed shedding per plant of Spergula arvensis in (a) 2018 and (b) 2019 during the growing season of spring oat. GDD = Growth Degree Days = sum of daily mean (b) 2019Figure during 5. Average the growing weekly and season cumulative of spring seed oat. shedding GDD =perGrowth plant of Degree Spergula Days arvensis= sumin (a) of2018 daily and mean temperatures(b) 2019 during above the growing0 from the season date theof spring oat was oat. sown GDD. Columns = Growth with Degree different Days letters = sum are of statisticallydaily mean temperatures above 0 from the date the oat was sown. Columns with different letters are statistically differenttemperatures at the above 0.05 probability 0 from the datelevel. the oat was sown. Columns with different letters are statistically different at the 0.05 probability level. different at the 0.05 probability level. Seeds of S. media started to shatter one week before harvest (26 July–2 August) (Figure 6a). Seeds of S. media started to shatter one week−1 before harvest (26 July–2 August) (Figure6a). StellariaSeeds media of producedS. media started on average to shatter 52 seeds one plant week, beof forewhich harvest 16.2% (26were July–2 shattered August) before (Figure harvest. 6a). 1 StellariaStellaria media mediaproduced produced on on average average 52 52 seeds seeds plantplant−1, ,of of which which 16.2% 16.2% were were shattered shattered before before harvest. harvest.

Stellaria media 2018 Stellaria media 2019 500 Stellaria media 2018 StellariaWeekly media shattered 2019 seeds Total shattered seeds 500 500 Weekly shattered seeds 400 Weekly shattered seeds 500 Total shattered seeds 400 Weekly shattered seeds 400 300 400 300 300 200 c 300 200 200 b d 100 c

Number of seeds of Number e

Number of seeds of Number a 200 b d a a 100 100 Number of seeds of Number 0 e Number of seeds of Number a a a 100 0 2-Aug 0

(b) 12-Jul 19-Jul 26-Jul 3-Aug 9-Aug 0 16-Aug 23-Aug (a) 2-Aug GDD 1300 1418 1555 1708 1816 1937 2056

(b) 12-Jul 19-Jul 26-Jul 3-Aug 9-Aug (a)GDD 1719 16-Aug 23-Aug GDD 1300 1418 1555 1708 1816 1937 2056 GDD 1719 Figure 6. Average weekly and cumulative seed shedding per plant of Stellaria media in (a) 2018 and (b) 2019 during the growing season of spring oat. GDD = Growth Degree Days = sum of daily mean FigureFigure 6. Average 6. Average weekly weekly and and cumulative cumulative seedseed shedding per per plant plant of ofStellariaStellaria media media in (ain) 2018 (a) 2018and and temperatures above 0 from the date the oat was sown. Columns with different letters are statistically (b) 2019(b) 2019 during during the the growing growing season season of of spring spring oat.oat. GDDGDD == GrowthGrowth Degree Degree Days Days = sum= sum of daily of daily mean mean differenttemperatures at the above 0.05 probability 0 from the datelevel. the oat was sown. Columns with different letters are statistically temperatures above 0 from the date the oat was sown. Columns with different letters are statistically different at the 0.05 probability level. 3.2.diff erentSeed Production at the 0.05 and probability Shedding level. in 2019 3.2. Seed3.2. Seed ProductionAll fourProduction species and and Sheddingstarted Shedding seed in in 2019shedding 2019 more than one week before oat harvest in 2019. Fallopia convolvulusAll four started species to startedshed seeds seed between shedding 12–19 more July, than and one the week largest before number oat ofharvest shed seedsin 2019. took Fallopia place All four species started seed shedding more than one week before oat harvest in 2019. theconvolvulus week before started harvest to shed (16–23 seeds August) between (Figure 12–19 3b).July, Seed and sheddingthe largest of number Sinapis arvensisof shed seedsstarted took between place Fallopia2–9the convolvulus weekAugust. before Thestarted harvest greatest to(16–23 number shed August) seeds of seeds between (Figure was 3b). 12–19shed Seed between July, shedding and 16 the− of23 Sinapis largestAugust, arvensis number also one started of week shed between before seeds took placeharvest2–9 the August. week (Figure beforeThe 4b). greatest harvestSpergula number (16–23arvensis ofAugust) startedseeds was seed (Figure shed shedding between3b). Seedbetween 16− shedding23 24August, June–1 of also July,Sinapis one and week arvensisthe largestbeforestarted betweennumberharvest 2–9 (Figureof August. shed 4b).seeds The Spergula took greatest place arvensis numberbetween started of31 seed seedsJuly–6 shedding was August shed between (Figure between 245b). June–1 16Seed23 sheddingJuly, August, and ofthe also S .largest media one week − beforestartednumber harvest between of shed (Figure 5–12seeds4b). July. tookSpergula The place largest between arvensis number 31started July–6of seeds seedAugust was shedding shed (Figure between 5b). between Seed19–26 shedding 24July June–1 (Figure of July,S 6b).. media On and the largestaveragestarted number between 321, of282, shed 5–12 125 seedsandJuly. 580 The took seeds largest place plant number between−1 were of produced se 31eds July–6 was by shed F. August convolvulus between (Figure 19–26, Sinapis5b). July arvensis, Seed (Figure shedding Spergula 6b). On of S. mediaarvensisaveragestarted and321, between S282,. media 125 5–12, andrespectively, July. 580 seeds The largest ofplant which−1 were number 53.2%, produced 38.1%, of seeds by 69 F..5% was convolvulus and shed 70.7% between, Sinapis of the 19–26 arvensis,seedsJuly were Spergula (Figure shed 6b). arvensis and S. media, respectively, of which 53.2%,1 38.1%, 69.5% and 70.7% of the seeds were shed On average 321, 282, 125 and 580 seeds plant− were produced by F. convolvulus, Sinapis arvensis,

Spergula arvensis and S. media, respectively, of which 53.2%, 38.1%, 69.5% and 70.7% of the seeds were

Agronomy 2020, 10, 46 6 of 10 shedAgronomy before harvest.2020, 10, x FOR The PEER diff erenceREVIEW between the weekly numbers of shed seeds for all four species7 of 11 was statisticallybefore harvest. significant The (differencep = 0.001). between the weekly numbers of shed seeds for all four species was Seedstatistically production significant was (p significantly = 0.001). different between the years for Spergula arvensis (p = 0.0056), Sinapis arvensisSeed production(p = 0.03) was and significantlyS. media (p =different0.0016), between but not the for yearsF. convolvulus for Spergula(p arvensis= 0.25). (p = 0.0056), Sinapis arvensis (p = 0.03) and S. media (p = 0.0016), but not for F. convolvulus (p = 0.25). 3.3. Plant Dry Weight 3.3. Plant Dry Weight The average plant dry weight at crop harvest was only different between the years for Spergula arvensis (1.03The average g in 2018; plant 0.28 dry g weight in 2019; at cropp 0.002).harvest Thewas only average different plant between dry weight the years at cropfor Spergula harvest for ≤ F. convolvulusarvensis (1.03, Sinapis g in 2018; arvensis 0.28and g in S.2019; media p ≤ was0.002). 1.6, The 0.8 average and 4.8 plant g, respectively. dry weight at crop harvest for F. convolvulus, Sinapis arvensis and S. media was 1.6, 0.8 and 4.8 g, respectively. For all species, there was a positive correlation between weed plant dry weight and total seed For all species, there was a positive correlation between weed plant dry weight and total seed production (Figure7). production (Figure 7).

Fallopia convolvulus Sinapis arvensis 800 800 700

700 600 y = 34.688x + 30.406 R² = 0.8038 600 y = 195.73x - 63.966 500 R² = 0.8781 500 400 400 300 300 200 200 100 Total seed production per plant 100 0 Total seed production per plant 0 0 5 10 15 20 (b) Dry weight plant-1 (g) 012345 (a) -1 Dry weight plant (g)

Spergula arvensis Stellaria media 1800 1800 1600 1600 y = 272.56x + 99.36 1400 1400 y = 798.47x - 113.54 R² = 0.4019 1200 1200 R² = 0.9421 1000 1000 800 800 600 600 400 400 200 200 Total seedper plantTotal production Total seed production per plant 0 0 012345 012345 -1 (c) -1 (d) Dry weight plant (g) Dry weight plant (g)

FigureFigure 7. Total 7. Total seed seed production production per per plant plant ofof ((aa)) Fallopia convolvulus convolvulus, (b,() bSinapis) Sinapis arvensis arvensis, (c) ,(Spergulac) Spergula arvensisarvensisand and (d) Stellaria(d) Stellaria media mediaas as a functiona function of of thethe plant dry dry weight weight in in 2018 2018 and and 2019. 2019.

4. Discussion4. Discussion A highA high fraction fraction of weedof weed seed seed retained retained onon thethe w weedeed plants plants at at harvest harvest increases increases the potential the potential for for HWSC methods. We determined both the amounts of shed seeds and the retained seeds on the weeds HWSC methods. We determined both the amounts of shed seeds and the retained seeds on the weeds to find the potentially harvestable ratio. The weed species showed different patterns in seed to find the potentially harvestable ratio. The weed species showed different patterns in seed production production and shedding, which also varied between the years. Different weather conditions and shedding,characterized which the two also growing varied seasons. between In the 2018, years. the summer Different was weather unusually conditions dry, warm characterized and sunny, the two growingwith many seasons. days having In 2018,temperat theures summer greater was than unusually 30 °C. It was dry, the warmwarmest and summer sunny, since with 1874 many [28]. days havingThe temperatures oat plants became greater drought-stressed, than 30 ◦C. It resulting was the in warmest less growth summer and a since thinner 1874 oat [ 28stand,]. The creating oat plants becamemore drought-stressed, space and light for resulting the weeds. in In less the growth dry and and warm a thinner weather oat in stand,2018, weeds creating and morecrop plants space and lightmatured for the weeds. earlier Inthan the in dry 2019, and resulting warm weatherin a three in weeks 2018, earlier weeds harvest. and crop In plantsthe dry matured season, the earlier dry than in 2019, resulting in a three weeks earlier harvest. In the dry season, the dry weight of F. convolvulus, Agronomy 2020, 10, 46 7 of 10

Sinapis arvensis and S. media decreased by 68.3%, 40.8% and 11.3%, and the total seed production decreased by 90.9%, 61.3% and 37.5%, respectively. In field trials in the , Wright et al. [29] evaluated the influence of two different soil moisture regimes on the competitive ability of Sinapis arvensis in spring wheat. Under dry conditions, the competitiveness of Sinapis arvensis measured as plant dry weight and seed production was significantly reduced. The dry weight and total seed production of Spergula arvensis increased by 72.9% and 81.9% in 2018 compared to the rainy season in 2019, as it was a rather weak competitor to oat [10]. On average, 195 seeds were produced by each plant of Sinapis arvensis in the two years. Forcella et al. [30] estimated the total viable seed production of Sinapis arvensis to be 2475 seeds 2 m− in corn fields in two years. Seeds were completely dispersed before corn harvest in the warmest year, whereas in the cold year, one-third of seeds were retained on the plant and dispersed via combines during harvest [30]. Matured pods of Sinapis arvensis usually remain intact until the crop is harvested. During harvesting operations, seeds fall in the vicinity of the parent plants, or are most likely gathered with the crop seeds and afterwards spread with the chaff within the field during the harvesting operation [5,7]. We recorded that seeds started to shatter at 1583 GDD in the first year and 1816 GDD in the second year. Before harvest, 27.7% and 38.1% of the seeds were shed, while Burton et al. [31] reported that seed shatter of Sinapis arvensis began at 1110 GDD in spring wheat in 2015 in Saskatchewan, Canada. Only 10.6% of the total seed production of Sinapis arvensis shattered before harvest. During the growing seasons, F. convolvulus climbs upwards, twining around the crop plants and in the case of cereals, it can cause lodging and make combine harvesting difficult [2]. Seeds started to shatter almost at the same period both years (1406 and 1418 GDD in 2018 and 2019, respectively) and almost with the same amount of seed shatter. Before harvest, 57.5% and 53.2% of seed shed. Burton et al. [31] reported from Saskatchewan, Canada, that seed shatter of F. convolvulus began at 1120 GDD in spring wheat in 2014 and 1060 GDD in 2015. They have observed a considerable variation in the seed shatter of F. convolvulus between the two years (31% of seed shattered before harvest in 2014 and 4.7% in 2015). They found that the high percentage of seed shattering in 2014 was caused by the dry conditions with periods of wind gusts close to the harvest time. However, we only observe a small variation in the seed shattering patterns. In both years, about 50% of the seed shed happened before harvest, but the total seed production was significantly reduced in the dry season. Dosland and Arnold [32] found that the supply of soil moisture was an essential factor for the competition between F. convolvulus and cereals. In a year with low precipitation, the weed germinated earlier and developed area and dry weight, rapidly contributing to the early depletion of water in the field. The growth of the crop proceeded slowly, and there was an early loss of leaf area at heading time, resulting in a reduced yield [32]. There is limited information on seed retention and the possibility of harvesting Spergula arvensis and S. media seeds by a combine harvester. On average, 411 and 316 seeds were produced by Spergula arvensis and S. media in the two years, respectively, of which 45% and 56% was retained on the plants at harvest. In the dry season (2018), S. media started to shed seeds at 1559 GDD, while in the rainy year (2019), shattering started at 1300 GDD with 16.2% and 70.7% of seeds shed before harvest, respectively. Spergula arvensis started to shed seeds at 1097 and 1136 GDD in 2018 and 2019, respectively, with 39.0% and 69.5% of seeds shed before harvest. Tidemann et al. [33] reported that seed retention decreased as GDD increased. Seed retention over time varies by species, site, year and treatment. Many factors may contribute to the variation in seed retention of a plant species such as soil condition, drought, thunderstorm, wind, rainfall and competition between plants, and variation between biotypes [33]. The efficiency of HWSC relies on the proportion of the weed seed production that is retained at crop maturity [34]. Seed retention higher than 80% at crop maturity happens for many agronomically important weed species creating a unique opportunity to target these weed seeds and prevent them from becoming a part of the weed seed bank in the soil [34]. Delays in crop harvest can result in fewer weed seeds being captured because of a higher rate of seed shatter [35,36]. Agronomy 2020, 10, 46 8 of 10

Fifteen cm reflects the practical harvest height for many growers. This height does not ensure that a large fraction of retained seeds on the weeds can be harvested for all the weed species. Sinapis arvensis is a tall plant (30–60 cm) with erect branching stems [14], making it possible to harvest the retained seeds by a combine harvester. This is also possible for Spergula arvensis (15–40 cm), which also has ascending or erect stems [14]. The stem of F. convolvulus (height: up to 2 m) is prostrate, but climbs the stems of other plants [14], which also make it possible to harvest retained seeds. However, S. media, which may become 20–60 cm tall, has decumbent to erect stems [14], which may make it difficult to collect a large proportion of the retained seeds at crop harvest. It is also likely that some seeds spread and fall to the soil surface during the harvesting process. We observed a strong positive correlation between the weed biomass and the total seed production. The larger the plant, the more seeds were produced [37]. Schwartz et al. [37] also reported a strong correlation between the weed biomass and total seed production of Amaranthus tuberculatus and A. palmeri in soybean fields. A strong correlation between biomass production and seed production has been documented for many weed species [38–41]. Regardless of the species, the majority of smaller plants had low seed production, indicating that these plants were late-emerging cohorts [42]. We have now shown that a large proportion of seeds produced during the growing season of common weed species potentially can be collected and removed or destroyed [43–45] by a combine harvester at crop harvest. The next step will be to test how large a fraction of this potential a combine harvest actually collects, as it depends on several factors such as harvest height and the number of seeds dropping to the soil surface under the harvesting process.

Author Contributions: C.A. was responsible for funding acquisition and the design of the experiment. Z.B. conducted the practical work, data processing and wrote the first draft of the manuscript. Both authors reviewed, edited and accepted the final manuscript. All authors have read and agreed to the published version of the manuscript. Funding: This work was a part of the project: 105 SWEEDHART-Separation of weeds during harvesting and hygienisation to enhance crop productivity in the long term. The activity was conducted under the “Joint European research projects in the field of Sustainable and Resilient Agriculture” under ERA-NET Cofund FACCE SURPLUS 2015. We thank Innovation Fund Denmark for financial support. Conflicts of Interest: The authors declare no conflict of interest. The funders had no role in the design of the study, the collection, analyses, interpretation of data, the writing of the manuscript or in the decision to publish the results.

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