The Biology of Canadian Weeds. 159. Capsella bursa - BioOne

The Biology of Canadian Weeds 159 Capsella bursa-pastoris (L) Medik

Authors Ahmed Hafsa T Francis Ardath Clements David R DyckElyse Ross Natalie et al

Source Canadian Journal of Plant Science 102(3) 529-552

Published By Canadian Science Publishing

URL httpsdoiorg101139CJPS-2021-0059

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ARTICLE

The Biology of Canadian Weeds 159 Capsella bursa-pastoris (L)MedikHafsa T Ahmed Ardath Francis David R Clements Elyse Dyck Natalie RossMahesh K Upadhyaya Linda M Hall and Sara L Martin

Abstract Capsella bursa-pastoris (L) Medik shepherdrsquos purse is a cosmopolitan summer or winter annual weedspecies distributed throughout temperate and subtropical regions of the world and is considered one of the mostcommon plants on earth It is an opportunistic annual that colonizes newly disturbed open or dry environmentsand is ubiquitous in cultivated lands in Canada In annual crops in western Canada C bursa-pastoris has beenamong the 20 most abundant weeds since the first weed surveys in 1970 It is most easily distinguished by its smallwhite four-petalled flowers and its heart-shaped seed-pods but exhibits considerable variation in leaf shape andflowering time It has been used for food and medicine by numerous cultures Its golden-brown seeds areproduced in large numbers predominantly through self-pollination and can form a substantial seed bank withreported values ranging to several hundred thousand seeds mminus2 While seeds usually disperse near the motherplant long-distance dispersal by attaching to vehicles people and other vectors may be facilitated by its mucilagi-nous coat Capsella bursa-pastoris does not produce fertile hybrids with other species of economic or ecologicalsignificance It is generally well controlled by soil-applied and foliar (post-emergence) herbicides although itspresence in agricultural fields may result in substantial yield loss as documented in cole crops in North Americaand grain crops in Europe The species can host a wide range of insect nematode fungal viral and bacterial peststhat may damage crop species

Key words Capsella bursa-pastoris shepherdrsquos purse cole crops weed dispersal

Reacutesumeacute La bourse-agrave-pasteur [Capsella bursa-pastoris (L) Medik] est une adventice annuelle cosmopolite qursquoon ren-contre lrsquoeacuteteacute ou lrsquohiver dans toutes les reacutegions agrave climat tempeacutereacute ou subtropical du globe On estime qursquoil srsquoagit drsquounedes plantes les plus courantes sur la Terre Opportuniste lrsquoannuelle colonise les endroits deacutegageacutes ou aridesreacutecemment perturbeacutes et on la recense sur toutes les terres cultiveacutees au Canada C bursa-pastoris figure parmi lesvingt adventices les plus abondantes dans les cultures annuelles canadiennes depuis qursquoon a commenceacute agravereacutepertorier les mauvaises herbes en 1970 La plante se reconnaicirct aiseacutement en raison de ses petites fleurs agrave quatrepeacutetales et de ses gousses en cœur mais la forme des feuilles et la peacuteriode de floraison varient consideacuterablementBeaucoup drsquoethnies lrsquoutilisent comme plante vivriegravere ou meacutedicinale Les graines brun doreacute sont produites engrand nombre principalement par autopollinisation et peuvent constituer une importante reacuteserve susceptibledrsquoatteindre selon certains auteurs plusieurs centaines de milliers par megravetre carreacute Bien qursquoelles demeurent le plussouvent agrave proximiteacute du plant megravere les graines peuvent se disperser sur de longues distances en adheacuterant auxveacutehicules aux gens ou agrave drsquoautres vecteurs gracircce agrave leurs teacuteguments mucilagineux Capsella bursa-pastoris nrsquoengendrepas drsquohybrides fertiles avec drsquoautres espegraveces drsquoimportance eacuteconomique ou eacutecologique Lrsquoapplication drsquoherbicide ausol ou aux feuilles (apregraves la leveacutee) est geacuteneacuteralement efficace mais la preacutesence de cette mauvaise herbe sur les terresagricoles peut donner lieu agrave drsquoimportantes pertes de rendement comme on lrsquoa observeacute dans les champs decrucifegraveres en Ameacuterique du Nord et ceux de ceacutereacuteales en Europe Lrsquoespegravece heacuteberge une grande varieacuteteacute drsquoinsectes

Received 6 March 2021 Accepted 8 October 2021

HT Ahmed and MK Upadhyaya Faculty of Land and Food Systems University of British Columbia Vancouver BC V6T 1Z4 Canada

A Francis and SL Martin Agriculture and Agri-Food Canada Ottawa Research and Development Centre Ottawa ON K1A 0C6 Canada

DR Clements E Dyck and N Ross Department of Biology Trinity Western University Langley BC V2Y 1Y1 Canada

LM Hall Agricultural Food amp Nutritional Science University of Alberta Edmonton AB T6G 2R3 Canada

Corresponding author David Clements (email clementstwuca)

copy 2021 Authors HT Ahmed DR Clements E Dyck N Ross MK Upadhyaya and LM Hall and her Majesty the Queen in Rightof Canada as represented by the Minister of Agriculture and Agri-Food Canada This work is licensed under a Creative CommonsAttribution 40 International License (CC BY 40) which permits unrestricted use distribution and reproduction in any mediumprovided the original author(s) and source are credited

529

Can J Plant Sci 102 529ndash552 (2022) dxdoiorg101139cjps-2021-0059 Published at wwwcdnsciencepubcomcjps on 5 November 2021


de neacutematodes ainsi que de parasites (champignons virus et bacteacuteries) susceptibles drsquoendommager les cultures[Traduit par la Reacutedaction]

Mots-cleacutes Capsella bursa-pastoris bourse-agrave-pasteur crucifegraveres dispersion des semences

1 NameCapsella bursa-pastoris (L) Medik mdash synonyms Thlaspi

bursa-pastoris L Bursa bursa-pastoris (L) Schull Bursa pasto-ris (L) Weber Common names shepherdrsquos purse(Darbyshire et al 2000) case weed common shepherdrsquos-purse pepper plant pick-pocket pickpocket pick-pursewitchesrsquo-pouches toothwort shovel-plant shepherdrsquosbag shepherdrsquos purse shepherdspurse (Hitchcock andCronquist 1973 Darbyshire 2003) bourse-agrave-pasteurbourse-agrave-berger boursette capselle capselle bourse-agrave-pasteur corne de lion tabouret tabouret des champsthlaspi thlaspi bourse agrave pasteur (Royer and Dickinson1999 Darbyshire 2003)

2 Description and Account of Variation(a) Species description

Capsella bursa-pastoris is a small summer or winterannual herb It has adapted to a wide range of environ-ments and is also phenotypically plastic contributing towide variation in size and life history traits It has adominant white taproot with few lateral fine roots(Hitchcock and Cronquist 1973 Aksoy et al 1998Defelice 2001) A solitary or several erect stems simpleor branched grow from the same root generally from10ndash60 cm tall but occasionally as high as 90 cm (Fig 1A)It forms a basal rosette with the first leaves at the groundsurface consisting of petiolate oblong leaves thatnarrow to the stalk and are usually hairy varying fromalmost entire to shallowly or deeply toothed 3ndash15 cmlong and 4 cm wide but occasionally longer with rosettediameters occasionally exceeding 40 cm (Neuffer andHurka 1986b) The stem leaves are smaller than therosette leaves stalkless alternate one per node areroughly linear entire to shallowly toothed to lanceolateon upper stem basal leaves sagittate (arrow shaped)amplexicaul (leaf grasping stem) or auriclate (ear-shaped) and densely to sparsely covered with finestar-shaped hairs or sometimes hairless (Hitchcock andCronquist 1973 Schultze-Motel 1986 Frankton andMulligan 1987 Alex 1992 Stace 1997 Defelice 2001Damgaard et al 2008 Al-Shehbaz 2012) Flowers aresmall (25ndash8 mm across) initially in rounded clusters atthe ends of stems and branches (Fig 1B) Sepals are greenor reddish (15ndash2 times 07ndash1 mm) Petals are white roundedand larger than the sepals generally 2ndash4 times 1ndash15 mm(occasionally slightly narrower or wider ranging to5 mm) Stamens number six with tetradynamousfilaments (1ndash2 mm) and with a shorter style (lt 08 mm)Flowers are present on a short glabrous terminalraceme and pedicels generally 05ndash15 cm long at matu-rity (Defelice 2001 Damgaard et al 2008) Fruits (silicles)

2-valved up to 3times as long as wide (4ndash10 times 34ndash8 mm) flat-tened at right angle to the stem triangular to heart-shaped with straight to slightly convex sides basecuneate apex emarginate or truncate notched at thetop valves each with subparallel lateral veins dividedby a narrow septum (membranous partition) (Fig 1C)Seeds numerous up to about 32 per fruit oblong08ndash1 mm long orange-yellow to light brown surfacedull and punctured (Fig 1C) (Schultze-Motel 1986Frankton and Mulligan 1987 Hurka and Neuffer 1991Alex 1992 Stace 1997 Al-Shehbaz 2012) Mucilage layervisible on seed surface when wetted (Swarbrick 1971)Pollen grains are small (lt 25 mm polar axis) isopolartricolpate prolate spheroidal to prolate and are distinctfrom other genera in the Camelineae in having interrup-tions in the tectum that create the appearance ofdimples on the pollen surface (Sagun and Auer 2017)

(b) Distinguishing featuresCapsella species are distinguished from other plants in

the mustard family by their triangular or heart-shapedseed pods that have a narrow septum or separatingmembrane between the halves of the pod (Alex 1992)Refer to Hitchcock and Cronquist (1973) for a diagnos-tic key

(c) Intraspecific variationCapsella bursa-pastoris has been observed to have high

intraspecific genetic morphological and phenologicalvariability (Hurka and Neuffer 1991 Neuffer andEschner 1995 Hurka and Neuffer 1997 Neuffer andMeyer-Walf 1996 Hawes et al 2005 Neuffer et al 2011Wesse et al 2021) However no particular genetic cyto-logical morphological or phenological variants havebeen described within Canadian populations althoughWesse et al (2021) incorporated Canadian accessions intheir global analysis of variation in C bursa-pastoris

In Canada a chromosome count of 2n= 32 is based oncytological specimens from Ontario Saskatchewan andBritish Columbia (Mulligan 1957 1984 Taylor andMulligan 1968) and 2n= 32 is given as the standard countin North America (Al-Shehbaz 2012) and Europe (Neuffer1990 Slotte et al2007) While counts of 2n = 16 haveoccasionally been reported these counts most likelyrepresent counts for Capsella rubella Reuter which hasextremely similar morphology (Neuffer 1990 Slotteet al2007) However C rubella has not yet been docu-mented as occurring in North America

Shull (1909 1929) examined and measured variationsin leaf morphology and segregated them into two spe-cies and ten subspecies Similarly Almquist (1923 1929)divided C bursa-pastoris taxa into some 200 microspecies

530 Can J Plant Sci Vol 102 2022

Published by Canadian Science Publishing


based mostly on small variations in fruit structure(Neuffer and Hurka 1986b Aksoy et al 1999) In theBritish Isles approximately 25 segregates have been rec-ognized showing variations in leaf and fruit shape(Stace 1997) An analysis by Iannetta et al (2007) of popu-lations in the United Kingdom (UK) concluded leaf-shapewas not associated with geographical distribution andonly loosely with life-history traits but studies in otherregions such as the Swiss Alps have shown stronger asso-ciations (eg Neuffer and Bartelheim 1989 Neuffer1990) Analysis of the genetic structure of these UK acces-sions using inter simple sequence repeat (ISSR) markersshowed a surprisingly large amount almost 60 of thegenetic variation was attributed to individuals withinan accession (Begg et al 2012) this result is similar tomore recent work by Wesse et al (2021) where 79 ofthe variation was found within populations in a regionalanalysis Begg et al (2012) also found three geneticallydifferentiated clusters the most defined of which wasassociated with the southern region earlier floweringand increased seed production and reduced secondarydormancy but not intensive cropping (Begg et al 2012)Given the key role of rosette morphology in life historyNeuffer et al (2018) examined the geographical distribu-tion of four distinct rosette leaf types across the globeand their association with morphological anatomical

and physiological characteristics under different condi-tions This revealed a complex pattern suggesting localadaptation of rosette characteristics overlaid with otherfactors such as genetic background

Numerous studies have examined intraspecific varia-tion in phenology in C bursa-pastoris plants and itsgenetic basis In general researchers have found thatthere are ecotypes with differentiated flowering timesthat occur in areas with different temperature regimeswhether as a result of latitude or elevation For exampletemperature-dependent variations in time to floweringand phenotypic plasticity were observed in wild popula-tions along a transect from northern to southernEurope (Neuffer and Hurka 1986a) In the Swiss Alpsvariations in such features as germination floweringtime and vegetative growth forms were correlated withaltitude Later flowering genotypes replaced earlier-flowering forms as elevation increased resulting inlater flowering winter annual forms at high altitudes(Neuffer and Bartelheim 1989 Neuffer 1990) SimilarlyCalifornia populations with early-flowering seem to havearisen from ancestral Spanish populations while later-flowering populations in temperate North America havearisen from cooler wetter northern European genepools (Neuffer and Hurka 1999) Karley et al (2008) alsofound the two flowering time variants in UK material

Fig 1 Mature Capsella bursa-pastoris plant (A) flower and developing seed pod stages (B) and open capsule and seed (C)Illustrations by Jessica Hsiung

Ahmed et al 531



and noted a strong but negative correlation betweenflowering time and seed production but none betweenseed production and reproductive duration ThereforeKarley et al (2008) concluded short flowering timecombined with greater resource allocation to reproduc-tion was the reason behind high fecundity (seed output)The genetic pathways that lead to these two floweringtime variants were investigated in early flowering typesobtained from Taiwan and late flowering types obtainedfrom Sweden by Slotte et al (2007) They found that theexpression of two circadian genes CCA1 and TOC1 andthe modified function of the circadian clock functionlikely caused variation in flowering time resulting intwo extreme (early and late) flowering types Linde et al(2001) identified three quantitative trait loci (QTL)responsible for the onset of flowering Given the likelylinkage between flowering rosette leaf developmentand other factors (Linde et al 2001) flowering inductionis complex and more research is needed to elucidate thegenetic pathway of flowering in C bursa-pastoris Overallthe presence of both high dormancylater flowering andlow dormancyearlier flowering appears to indicate ahedge betting strategy useful in variable environments

An unusual heritable variant in floral morphologyfirst observed two centuries ago in Europe and describedas Capsella apetala Opiz (Opiz 1821) is the recently redis-covered ldquodecandricrdquo or spermatogenesis-defective (spe)phenotype in which all of the petals have been trans-formed into additional stamens (reviewed by Hintz et al2006 Hameister et al 2009 2013 Ziermann et al 2009)A comparative study found that the flowers of the spephenotype matured two weeks later in Germanyallowing stable coexistence with the wild type (Neufferet al 2020)

(d) IllustrationsThe morphology of a mature C bursa-pastoris plant its

basal and stem leaves flower seed pod and seed areshown in Fig 1 Numerous photographic images areavailable online including httpucjepsberkeleyeduefloraeflora_displayphptid=17109 httplinnetgeogubccaAtlasAtlasaspxsciname=Capsella20bursa-pastoris httpwwweflorasorgflorataxonaspxflora_id=5amptaxon_id=200009292 httpswwwbrcacukplantatlasplantcapsella-bursa-pastoris httpswwwcalfloraorgcgi-binspecies_querycgiwhere-calrecnum=1472

3 Economic Importance and Environmental Impact(a) Detrimental

Capsella bursa-pastoris was the 20th most abundantweed in residual weed surveys in western Canada duringthe 2000s (Leeson et al 2005) It was found in 92 offields in densities as high as 140 plantsmiddotmminus2 It was mostabundant in the Peace Lowland Boreal TransitionAspen Parkland and Fescue Grasslands ecoregions andfound in lower abundance in Interlake Plain Moist

Mixed Grassland and least in Mixed Grasslands andLake Manitoba Plain Globally it is considered one ofthe most widespread plants on earth (Coquillat 1951Zhou et al 2001) and inevitably interferes with crop pro-duction infesting winter cereals horticultural cropsorchards and forages (Aksoy et al 1998)

Despite its observed frequency research quantifyingeconomic yield losses for C bursa-pastoris alone hasrarely been conducted While it can contribute to yieldlosses of field crops in the Canadian Prairies it is rela-tively non-competitive compared with other weeds inspring crops including cereals and canola (Welbank1963) Capsella bursa-pastoris can cause serious yield lossesin cole crops such as cabbage broccoli cauliflower orBrussel sprouts and in other horticultural crops such asonions because herbicides which control the weedwould also cause crop injury (Freyman et al 1992Bitterlich et al 1996 Dillard et al 2004 Sikkema et al2007) However it was less competitive than cultivatedradish in pot experiments (Perera and Ayres 1992) andcabbage grown in narrow rows and in both narrow andwide rows with 10 cm planting intervals were unaffectedby C bursa-pastoris (Freyman et al 1992) Due to its winterannual life cycle however C bursa-pastoris is common inCanadian winter wheat fields In a meta-analysis of her-bicide trials conducted in Sweden Milberg andHallgren (2004) reported that C bursa-pastoris was moreeconomically detrimental in winter crops based on yieldloss in cereal crops investigated in 1691 trials Theyconcluded that C bursa-pastoris was one of the two worstweeds for autumn-sown cereal crops Widespreadinfestation was also seen in Great Britain where 23 of2359 winter cereal fields were infested with C bursa-pastoris (Marshall et al 2003) Population densities ofC bursa-pastoris determined from barley and wheat fieldsover three seasons in New Zealand indicated a strongpresence and high degree of competition with crops intheir early developmental stages within fields under-going normal crop management practices includingpostemergence herbicide treatments (Bourdoumlt et al1998) In Denmark the observed weed frequency ofC bursa-pastoris increased for spring barley spring rapewinter rye and winter wheat in 2001ndash2004 comparedwith 1978ndash1989 but decreased in the multispecies assem-blies of grass leys (Andreasen and Stryhn 2008) Capsellabursa-pastoris is generally a component of the commonbroadleaf weed assemblage for which a wide range ofherbicides are available (see Section 11 Response toHerbicides and Other Chemicals)

A suspected nitrite poisoning of pigs in South Africawas attributed to consumption of C bursa-pastoris(Wiese and Joubert 2001) and cattle grazing on a mixtureof 40 C bursa-pastoris and 60 Sisymbrium irio L anothermember of the Brassicaceae died from polioencephalo-malacia a neurologic disease of ruminants as a resultof the sulfur content of the plants (McKenzie et al2009) However the plant is listed as having no known




poisoning risk and moderate palatability to goats(Simmonds et al 2000) and has been used as a folk rem-edy for treating ailments in livestock (see Section 3(b)Beneficial)

Populations of C bursa-pastoris can pose a risk to crophealth production and quality as it is a host to insectnematode fungal viral and bacterial pests includingspore-forming bacilli (Iannetta et al 2010 see Section 13Response to Herbivory Disease and Higher PlantParasites)

(b) BeneficialBecause of its widespread availability C bursa-pastoris

has a long tradition of use as a potherb (a plant used inseasoning of food prepared by boiling in a pot) and infolk medicine in the majority of cultures around theworld (Bussmann et al 2019) Young leaves were cookedas greens or eaten raw as salad seed pods were used asa peppery seasoning seeds were dried and ground intomeal and roots were used as a ginger substituteIn Japan the plant was an ingredient in a ceremonialbarleyndashrice gruel (Facciola 1990 Defelice 2001) and it iseaten frequently in Korea where its leaves and rootsare consumed as vegetables (Lee et al 2016) As a foodplant the species contains significant vitamins and min-erals (Zennie and Ogzewalla 1977 Choi et al 2014)However an analysis of heavy metal content in wild foodplants collected in an industrialized zone of Turkeyshowed higher than average levels of cobalt leadmanganese and iron in C bursa-pastoris placing itamong plants hazardous to health if eaten in large quan-tities (Pehlivan et al 2013)

Numerous medicinal properties ranging from anal-gesic to vermifuge (anti-parasite) have traditionally beenattributed to extracts from the plant both for humansand livestock (Duke 2002) but it has primarily been asso-ciated with reducing internal or external bleeding It hasbeen used to staunch bleeding and to heal infected andbleeding wounds (Gerard 1633) and to treat such condi-tions as dysentery bleeding menstrual disordersand stomach problems or as a diuretic (Defelice 2001Kozub et al 2012 Choi et al 2014) Hartwell (1982) citedpopular European sources dating to the medieval periodon the use of infusions of C bursa-pastoris to treat ulcersand cancers including those of the stomach and uterusMillspaugh (1974) indicated that the plant was used totreat diarrhoea in calves in England and its use wasreported as folk-remedy for livestock in Switzerland(Bischoff et al 2016) Based on these traditional uses sev-eral studies have investigated C bursa-pastoris or itsextracts for these properties in cell culture anti-thrombin (blood clotting) (Goun et al 2002) anti-cancer(Mazzio and Soliman 2009 Lee et al 2013) anti-bacterial(Fahey et al 2002) and anti-inflammatory properties(Hur et al 2013 Choi et al 2014) For example isothiocya-nate sulforaphane extracted from crucifers was shown toinhibit antibiotic-resistant strains of the bacterium

Helicobacter pylori associated with gastric ulcers andstomach cancer in tissue culture (Fahey et al 2002)

Weeds such as C bursa-pastoris play a role in maintain-ing biological diversity within crop fields (Storkey andWestbury 2007 Begg et al 2012) For example the spe-ciesrsquo phenotypic and biochemical variability provides aheterogeneous resource for phloem-feeding aphids(Karley et al 2008) Five insect families 13 species twoof which are host specific and three of which are pestswere associated with C bursa-pastoris in winter cerealfields in Great Britain (Marshall et al 2003) Capsellabursa-pastoris was also deemed important for 2ndash3 UKseed-feeding farmland birds and 11ndash25 invertebrates(Marshall et al 2003) Andreasen and Stryhn (2008)suggest the increasing abundance of Brassicaceousweeds may improve food availability for birds andinsects in arable lands

Capsella bursa-pastoris extracts can be used as weed con-trol against annual ryegrass and wild radish thoughannual ryegrass is affected more (Seal et al 2009)Extract concentrations of 5 or more were able to signifi-cantly inhibit growth for both aforementioned weedsthis includes root growth A 400 concentrated extractwas able to inhibit annual ryegrass shoot length andweight by more than 70 when grown in a tray filledwith 5050 sandpeat moss (Seal et al 2009)

As an extremely abundant and widespread plant onthe planet C bursa-pastoris is an important model organ-ism for studies in a wide variety of areas including theevolutionary ecology of weeds (Nutt et al 2006 Hintzet al 2006 Choi et al 2019 Žerdoner Čalasan et al2021) and genome evolution following hybridizationand polyploidization (Hurka and Neuffer 1997 Slotteet al 2007 Kasianov et al 2017) Because it exhibits awide range of genetic variation among populationsmany studies have looked at patterns across its geo-graphic range to examine the evolutionary mechanismsinvolved (Slotte et al 2007 Neuffer 2011 Begg et al2012 Toorop et al 2012)

(c) LegislationIn Canada C bursa-pastoris is not listed under either

the federal Plant Protection Act or the Federal WeedSeeds Order 2016 under the Seed Act After its removalfrom Alberta noxious weed legislation Manitobaremains the only province that has continued to desig-nate the species a noxious weed (Noxious Weeds ActCCSM c N110 2010) In the United States C bursa-pastorisis not listed on either federal or state noxious weedslists but has been reported as invasive in several states[Invasive Plant Atlas of the United States (httpwwwinvasiveplantatlasorg)]

4 Geographical DistributionCapsella bursa-pastoris a species of Eurasian probably

eastern Mediterranean origin occurs broadly distributedaround the world in temperate regions in both

Ahmed et al 533



hemispheres and at scattered locations from tropicalhighlands to sub-arctic regions (Hulteacuten and Fries 1986)In Canada C bursa-pastoris is present throughout agricul-tural regions in all provinces including Newfoundlandand Labrador the Yukon and the Northwest territories(Darbyshire 2003 Fig 2) Collections in Canadian herbariashow particular abundance in southern British Columbiasouthern Manitoba and throughout the NiagaraPeninsula and the St Lawrence Valley as well as collec-tions from eastern Alaska southwestern Greenland andthe French islands of St Pierre and Miquelon (Fig 2)

It is relatively abundant throughout continental UnitedStates with a presence in all 50 states (Al-Shehbaz 2012)and greatest abundance in the Atlantic south-centraland Pacific states (Hulteacuten and Fries 1986) It is especiallycommon in southwestern Mexico (Frankton and Mulligan1987 Defelice 2001) Aksoy et al (1998) considered itnative to eastern Europe while Mukherjee et al (1984)

considered all the populations in SwitzerlandAfghanistan Germany Sweden Finland the Netherlandsand Scotland at various altitudes and latitudes to representnative populations Populations considered native werealso studied along a latitudinal transect from the KolaPeninsula to the Caspian Sea and from northern andsouthern Scandinavia by Neuffer (2011)

Wesse et al (2021) conducted a global survey of thegenetic variation of C bursa-pastoris from 1469 naturalprovenances from diverse locations in the native andintroduced range A moderate reduction in geneticdiversity was observed among introduced populationsand it was concluded that there were two broad climaticvariants one adapted for warm arid conditions and thesecond to temperate humid conditions and that by andlarge the world colonization was accomplished throughmultiple introductions of genotypes pre-adapted todiverse niches (Wesse et al 2021)

Fig 2 Distribution of Capsella bursa-pastoris in Canada based on herbarium collection from ACAD ALTA AUC BABY CAN DAOLEA LKHD MT NHIC OFRI PMAE QK QUE RBG ROM SASK SSMF UAC UBC ULF UNB V and WIN herbaria See Holmgrenet al (1990) for institutional abbreviations Esri Inc ArcMap (Version 1061) Software Redlands CA Esri Inc 2016 Basemapsource Esri HERE Garmin Tinermap increment P Corp GEBCO USGS FAO NPS NRCAN GeoBase IGN Kadaster NLOrdnance Survey Esri Japan METI Esric China (Hong Kong) copy OpenStreetMap contributors and the GIS User Community




5 Habitat(a) Climatic requirements

Capsella bursa-pastoris is adapted to a wide range ofmicro-climates around the world but is commonly foundgrowing in cool and warm (subtropical) temperateregions as indicated by its broad range in Canada whereit grows in all provinces and territories (Aksoy et al 1998Defelice 2001 Fig 2) However the species is alsowell-adapted to drought conditions (see Section 7(a)Morphology) Its presence was recorded in the Nile valleywhere the average rainfall was 20 mm in spring andmean temperature near 27 degC in May In Germany itsurvives as a rosette over winter when the temperaturecan be as low as minus12 degC (Aksoy et al 1998) Capsellabursa-pastoris is restricted to flat or gently sloped regionsbut is more common on south-facing slopes (Grimeet al 2014)

(b) SubstratumCapsella bursa-pastoris grows in various types of soils

however it grows predominantly on fertile-disturbedclay to sandy loam soil (Aksoy et al 1998 Defelice 2001Grime et al 2014) It can tolerate soil with pH 5ndash8(Aksoy et al 1998) but is absent from regions with a soilpH less than 5 (Grime et al 2014) Aksoy et al (1998)curated a list of soil types where C bursa-pastoris has beenrecorded including serpentine soils in southern Urals(Brooks 1987) loess soil in Lublin Poland (Lipecki 1989)alkaline sandy loam soils found in the Nile Valley inEgypt (El-Habibi and Youssef 1981) calcium carbonateenriched sandy loam soil in Turkey (Aksoy and Gemici1993) and wet humus-rich soil in Korea (Kang 1983)Capsella bursa-pastoris has also been recorded growing onsoil contaminated by cadmium (Liu et al 2015)

(c) CommunitiesApart from the cultivated grain and vegetable

crops where the species is a weed (see Section 3(a)Detrimental) C bursa-pastoris is present in a variety ofruderal and disturbed communities wherever it occursThis includes waste fields demolition plots manure pilescompost heaps roadsides and gravel parking lots (Alexand Switzer 1976 Aksoy et al 1998) In Canada it hasbeen found in gardens orchards vineyards pasturesmeadows and beaches (Canadian herbarium records)In the United States the species along with other win-ter annuals such as chickweed (Stellaria media L) fieldpennycress and henbit (Lamium amplexicaule L) havebeen moving into crop areas (Hill et al 2014) Withinthe United Kingdom the species has been dominant inseveral vegetation communities the chickweedndashCapsella and the chickweedndash nettle (Urtica urens L) com-munities and in the plantain (Plantago major L) andbindweed [Fallopia convolvulus (L) Aacute Loumlve] ndash speedwell(Polygonum aviculare Poir) subcommunities and is aminor component of other communities of herbsincluding other crucifers such as field pennycress

(Thlaspi arvense L) and grasses including meadow grass(Poa annua L) and rye-grass (Lolium perenne L) (Pigottet al 2000) while in other parts of Europe it is amongplant communities dominated by members of theChenopodioideae such as Amaranthus and Chenopodiumspp and among such communities in alpine pine-spruce stands and in vineyards (Aksoy et al 1998Konstantinovic and Blagojevic 2014) The species isubiquitous in Germany along with other species inthe above-mentioned communities (Hanzlik andGerowitt 2012)

6 HistoryIn Canada C bursa-pastoris was already established in

Quebec when collected in Montreal in 1821 (Rousseau1968) and it was recorded in Nova Scotia as early as1829 (Groh 1947) It continued to spread in areas alongthe St Lawrence River and by the 1950s was found at sub-arctic trading posts around James Bay In Ontario it wascollected as early as 1885 and was widespread in the firsthalf of the 20th century It was established across theprairies with a record in Victoria British Columbia in1894 and other early collections dated from 1899 1911and 1924 in Alberta Saskatchewan and Manitobarespectively It had reached the Northwest Territoriesand Yukon by the 1940s with a record collected forCape Dorset in Nunavut in 1936 (Groh 1947 Canadianherbarium records)

The introduction of Capsella bursa-pastoris to the UnitedStates and Mexico occurred before introductions intoCanada very early in the colonial period and was likelyintroduced repeatedly Indeed on investigating thegenetic makeup of populations in Europe (593 popula-tions) and North America (88 populations ndash 7 Canadian)Neuffer and Hurka (1999) suggested C bursa-pastoris wasintroduced to North America on at least 20 separateoccasions It was recorded as present in New England in1672 and by the 19th century was referred to as ldquoThecommonest of weeds introduced from Europerdquo (Gray1848) It is believed to have been introduced to Mexicoat the time of the Spanish conquest in the early 17thcentury to have reached California following the estab-lishment of the Spanish Missions there particularly dur-ing the late Spanish and Mexican eras after 1824 andduring the following gold rush seeds could have comeby transportation routes from the south and the eastas well as from Europe (Neuffer and Hurka 1999)

More broadly the genus Capsella originated in theeastern Mediterranean including Asia Minor as part ofthe diversification of the tribe Camelineae which alsoincludes Arabidopsis and Camelina (Žerdoner Čalasan et al2019) Capsella bursa-pastoris is likely a 100 000ndash300 000-year-old hybrid originating from Capsella orientalisKlokov and C grandiflora (Faucheeacute amp Chaub) Boiss orC rubella lineages Maternal contributions were madefrom the C orientalis lineage based on chloroplast DNAclustering while the Capsella grandiflorarubella lineage

Ahmed et al 535



made paternal contributions resulting in an allopoly-ploid hybrid (Hurka et al 2012 Douglas et al 2015Žerdoner Čalasan et al 2021) An analysis by ŽerdonerČalasan et al (2021) showed the hybridization resultingin C bursa-pastoris took place in the southwestern EastEuropean plain during Late Pleistocene interglacialcycles Early Neolithic records of C bursa-pastoris seedsare reported in Turkey between 5850 and 5600 BCwhereas in central Europe the earliest records date fromthe Neolithic approximately 4000 BC (Willerding 1986quoted in Hurka and Neuffer 1997) Presumably it wasspread from Central Europe via agriculture

7 Growth and Development(a) Morphology

Capsella bursa-pastoris like other ruderal species ischaracterized by phenotypic plasticity and genetic adapt-ability across a range of traits including height rosettesize floral biology and seed and fruit morphology(Hurka and Benneweg 1979 Neuffer and Hoffrogge2000 Neuffer 2011 Neuffer and Paetsch 2013) Severalcommon garden experiments have revealed variation inheight is driven by both genetic differentiation and phe-notypic plasticity (Neuffer and Hurka 1986b Neuffer andAlberts 1996 Neuffer and Hoffrogge 2000) It forms arosette an adaptation for overwintering and coldresponsive (COR) genes have been shown to be promotedwith rosette leaves in response to cold temperatures (Linet al 2016) Similarly variation in petal size is stronglyinfluenced by temperature with warmer temperaturespromoting larger petal growth (Neuffer and Paetsch2013) Prolific seed production enables widespreaddispersal of C bursa-pastoris and seeds produce a muci-laginous sheath upon hydration (myxospermy) whichcan enhance water absorption particularly in dry soil(Deng et al 2015) and has likely played a major role inlong-term dispersal success of the species (Neuffer et al2011) Its deep tap root (up to 33 cm) enables it to accesswater at considerable depth also contributing to its abil-ity to withstand drought conditions (Johnson et al 2011)

(b) PerennationCapsella bursa-pastoris is a summer or winter annual

It reproduces by seeds only (Neuffer 1990 Aksoyet al 1998)

(c) Physiology and biochemistryCapsella bursa-pastoris is a C3 facultative winter annual

that may overwinter as a rosette or emerge very earlyin spring Cici and Van Acker (2011) investigated thefreezing tolerancerecovery of several winter annualspecies and reported that C bursa-pastoris hadlower cold tolerance than narrow-leaved hawksbeard(Crepis tectorum L) stinkweedfield pennycress (Thlaspiarvense L) and field violet (Viola arvensis Murr) but simi-lar cold tolerance to downy brome (Bromus tectorum L)and common chickweed [Stellaria media (L) Vill]

Specifically C bursa-pastoris plants showed 50 freezingdamage at minus14 degC with freezing tolerance mediated by a21-fold increase in proline levels Wani et al (2018)analyzed cold stress responses of 30-day-old seedlingsby exposing them to 10 degC and collecting plant tissuesat 24 48 72 96 and 120 h Results indicated that coldstress reduced photosynthesis but that turgor andosmotic pressure were maintained by increased levelsof soluble sugars saturated and unsaturated fatty acids(Wani et al 2018)

The performance of C bursa-pastoris has been evalu-ated under light water and nutrient stress (Aksoy et al1998) The plant grows in both open and shaded areasthough leaf lengths were shorter under light flux reduc-tion compared with full sun Capsella bursa-pastoris hadthe highest total dry weight when it was watered for 4consecutive days out of 14 compared with treatmentswith fewer or more (2 6 8 or 10) consecutive wateringdays Nutrient requirements were tested in sand culturesover a 14 h day Calcium treatments ranging from 5 to200 μgmiddotmLminus1 increased total dry weight while calciumlevels between 5 and 15 μgmiddotmLminus1 resulted in the rosetteleaves to curl indicating deficiency Fertilization withphosphorus resulted in maximum root and shootdry weight when supplied at 16 μgmiddotmLminus1 Nitrogen sup-plied at various concentrations increased total dryweight until 81 μgmiddotmLminus1 but declined significantly at243 μgmiddotmLminus1 Potassium supplied at various concentra-tions increased total dry weight until 32 μgmiddotmLminus1 andthen declined (Aksoy et al 1998) Fertilization withammonium nitrate may cause injury with retention ofthe solution enhanced by trichomes on C bursa-pastorisleaves (Bitterlich and Upadhyaya 1990)

The average lipid content of C bursa-pastoris seed isreported to be 30 though higher lipid contents areobserved in plants from temperate regions comparedwith those from colder regions The fatty acid profilehas a relatively large proportion of very long-chain fattyacids (gt C18) as is characteristic of seeds from theBrassicaceae (Mukherjee et al 1984) Specifically thefatty acid profile of C bursa-pastoris seed is dominatedby 25ndash40 linolenic acid (C183) 20 linoleic acid(C182) and has noteworthy levels of polyunsaturatedfatty acids icosadienoic (C202 10ndash20) and icosatrie-noic acids (C203 5ndash15) but has little erucic acid(C221) often a major component of brassicaceous seeds(Mukherjee et al 1984 Moser and Vaughn 2012 Al-Snafi2015) The roots and the aerial portions of the plantsalso contain these fatty acids (Al-Snafi 2015 Grosso et al2011) The levels of flavonoids organic acids and sterolsamong other chemicals have also been assessed includ-ing their relationship to light and temperature at placesof origin (Eschmann-Grupe et al 1990 Grosso et al 2011)

(d) PhenologyIn Canada C bursa-pastoris can flower from

early spring to late fall (Frankton and Mulligan 1987)




Aksoy et al (1998) detailed the phenology of plants inBritain where seeds germinate primarily at the begin-ning of March with a small germination event afterAugust The first rosette leaves are produced 12ndash14 dafter germination If germinated early the rosettecontinues to grow until the beginning of June whilethe first shoot appears by the beginning of May Flowerformation is initiated 3ndash4 d after shoot developmentstarts ripe seeds and fruits appear at the end of Maywith seeds released from June on (Aksoy et al 1998)The time required before the onset of flowering has beenreported to vary widely for European populations ofC bursa-pastoris (see section Intraspecific Variation)Iannetta et al (2007) reported that early floweringvariants required 70 d to flower while other variantsrequiredgt130 d

(e) MycorrhizaTraditionally plants of the Brassicaceae family and

C bursa-pastoris in particular were thought to be non-mycorrhizal (Gerdeman 1968 Medve 1983) Demars andBoerner (1994 1995) observed vesicular-arbuscularmycorrhizal fungi colonization of C bursa-pastoris inplants grown alone and a greater level of colonizationin plants grown in a grass matrix However this doesnot necessarily mean that C bursa-pastoris is mycorrhizalas it could mean that the mycorrhizae were attackingsenescent roots Alternatively colonization did occurbut only on a sporadic basis with the mycorrhizaemainly colonizing the grass species Populations weresampled from both lawn and waste area habitatsFungal colonization was significantly higher in lawnhabitats most likely due to the presence of stronglymycorrhizal plants Internal hyphae vesicles chlamydo-spores and extramatrical hyphae were found fromC bursa-pastoris root segments investigated but noarbuscles (Demars and Boerner 1994) Chawla et al(2011) found arbuscules and extramatrical hyphae butno vesicular structures from populations in India andconcluded C bursa-pastoris may aid in maintainingmycorrhizal inoculum in the soil during winter

8 Reproduction(a) Floral biology

Capsella bursa-pastoris is self-compatible and primarilyself-pollinating (autogamous) the extent to which varieswith environmental conditions and other interactionsNearly exclusive self-pollination occurs when the atmos-pheric humidity is high temperature is over 15 degC andlight intensity is low Outcrossing is favoured underdry sunny conditions (Hurka et al 1976) with up to 10outcrossing recorded under field conditions (Hurka et al1989) Sterile fruits are produced under extremely coldor hot conditions and this has been attributed to thefailure of the anthers opening Compared with self-incompatible Capsella species such as C grandifloraC bursa-pastoris has smaller petals lower pollen

production shorter styles and more rapid fertilizationafter pollination from compatible pollen (Hurka et al1976 Neuffer and Paetsch 2013) Examples of flowerinsect visitors included hoverflies (Syrphidae) bees(Apidae) beetles (Coleoptera) and thrips (Thysanoptera)for a population studied in Germany (Ziermann et al2009) The unique spe floral type where petals arereplaced by stamens tends to attract hoverflies ratherthan bees as typical of the wild type (Neuffer et al2020) Homeotic mutants with stamenoid petals foundclose to Mainz Germany exhibited half the number ofinsect visitations and no emission of volatile monoter-penes and benzenoids compared with wild type plantsBoth the mutant and wild type plants attracted the sametypes of visitors (Ziermann et al 2009) Day-lengthinfluences the onset of flowering time C bursa-pastorisbehaves as a facultative long-day plant (Hurka et al 1976)

(b) Seed production and dispersalCapsella bursa-pastoris is a prolific seed producer

but production per plant is highly variable Hurka andNeuffer (1991) reported seed production from individualsfrom seven European populations ranging from 100 to91 000 seeds plantminus1 Hill et al (2014) reported seed pro-duction from naturally occurring stands at 800 to40 000 seed mminus2 from 40 to 230 plantsmiddotmminus2 Individualplant seed production ranged from a minimum of5000 to a maximum of 90 000 seeds in a German study(Hurka and Haase 1982) Seed production per plant wasincreased by fertilization and linked to increasedbranching (Yang 2018) The seed is 1 mm long and weighsapproximately 01 mg on average but is highly variableSeed weights reported for a variety of environments arerelatively consistent Mukherjee et al (1984) reportedseed weights from 0093ndash0156 g per 1000 seeds formaterial collected from a variety of elevations (10 to2400 m) and latitudes (36 to 69 degN) Similarly Werle et al(2014) reported weights of 00110 plusmn 00001 and 00108 plusmn00002 g per 100 seeds in two different years (2010and 2011) from a farm field in Nebraska USA andBenvenuti (2007) reported 0092 plusmn 0071 per 1000 seedsfrom farm fields in Asciano Italy Seed size affects thegermination rate and hypocotyl length of seedlings withhypocotyl length longer in seedlings from larger seeds(Hurka and Benneweg 1979) Seed count varies from 10to 40 seeds per fruit Seeds are dormant at the time ofdispersal When the seed pod is ripe it opens along itssepta but the seeds are not released immediatelylengthening the time over which seeds disperse andseedlings emerge (Hurka and Haase 1982) The smallspherical smooth seeds disperse unassisted within50 cm of the parent plant (Aksoy et al 1998) while forwind-aided dispersal 80 of seed fell within 50 cm but20 was scattered between 50 and 105 cm The size andshape of the seed increases the probability of seed burialeven in the absence of tillage (Benvenuti 2007) It wasobserved the seeds were equally distributed in the first

Ahmed et al 537



10 cm of the soil after which the frequency declined Noseeds were observed at 40 cm soil depth this was attrib-uted to the soil conditions at the field station (Hurka andHaase 1982) The mucilaginous sheath around the seedmay enable long-distance dispersal by facilitating attach-ment to animals vehicles and people Earthworms(Lumbricus terrestris L) ingest the seeds and release themin their casts This contributes to short-distance verticaldispersion and germination (Hurka and Haase 1982)

(c) Seed banks seed viability and germinationCapsella bursa-pastoris has a persistent seed bank that

can vary in size Hurka and Neuffer (1991) reported abroad range of seed banks from 500 to 300 000 seed mminus2

in various German environments Sanderson et al (2014)reported seed banks (as determined by germinableseeds) in organic dairy hay permanent and recentlyestablished pastures at between 11 to 8580 seedmiddotmminus2 Incottonndashtomato rotations in California seed banksranged between 8 and 1220 seedmiddotmminus2 with the highestseed bank exhibited in conservation tillage treatmentswith cover crops (Shrestha et al 2015) Larger seed banksmay be favored by a lack of soil disturbance as viableseeds survive longer in undisturbed soil than in culti-vated soil In experiments conducted in the UnitedKingdom C bursa-pastoris seed was buried in disturbedand undisturbed soil and seed emergence and viabilitymonitored over 6 years (Roberts and Feast 1973) In culti-vated soil they recorded 18 and 12 emergence in thefirst and second years with a total of 46 emergenceover the 6 years of the study and 4 of the seeds remain-ing viable in the soil In uncultivated soil the emergencerates were lower 5 and 1 in the first and second yearsand 12 total emergence over the 6 years however23 of the seeds remained viable in the seed bankSimilarly Kivilaan and Bandurski (1981) reported thatC bursa-pastoris remained viable in Dr Bealrsquos Alaska seedviability experiment for gt35 yr while Conn and Deck(1995) reported that seed germination declined from aninitial 48 germination rate to 42 42 30 9 andlt1 after27 37 47 67 and 97 years respectively However afterthis initial sharp decline in germination rate seedsshowed long-term persistence with viability remainingat a constant low level to 247 years Specifically viabilityfor C bursa-pastoris was 13 at 197 yr and 28 at 247 yrand further unlike the majority of species tested overa third of the seed still exhibited dormancy after 247 yr(Conn and Werdin-Pfisterer 2010) Baskin and Baskin(2006) combined data from the Duvel experiment whichlasted 39 yr and the Beal experiment which lasted 120 yrand suggested C bursa-pastoris seeds can remain viable inthe soil after 39ndash40 yr However the seed half-life accord-ing to Roberts and Feast (1973) is 5 yr which is furtherreduced to 1 yr if the soil is annually disturbed throughcultivation (Aksoy et al 1998) This suggests that in theabsence of seed bank replacement seed banks decreasemore rapidly in cultivated soils while C bursa-pastoris

can persist longer in wastelands rights-of-way andperennial crops

Temperature alters germination success with lowtemperatures inhibiting germination and growth (Waniet al 2018) Seed germination of populations fromScandinavia the European Alps and the Middle Eastwas tested in growth chambers and greenhouses underfive to seven different temperature treatments showinga trend in greater germination with increased tempera-ture (Neuffer and Hurka 1988) Neuffer and Hurka (1988)also observed that seed age influenced both germinationcapacity the proportion of seed that germinated andgermination rate the time taken for 50 of the seeds togerminate with decreased germination with seed ageSeed dormancy level also influences germinationtiming (Neuffer and Hurka 1988 Toorop et al 2012)Germination occurred from 10ndash30 degC while soil pHranged from 3 to 11 for seeds collected from a wheat fieldfrom Qarakheyl Crop Research Station Iran (Rezvaniet al 2014) At 30 degC the greatest germination rate wasobtained under a 1212-h lightdark treatment Inanother study conducted in the Nile delta the highestgermination rates were obtained at 30ndash35 degC (Rayia et al2020)

Germination rates seedling fresh mass fresh rootlength and other traits indicative of germination andestablishment were found to be higher when the plantswere germinated in the presence of nematodes (Robertset al 2018)

In Canada C bursa-pastoris is a facultative winterannual with two distinct emergence peaks in latesummerfall and in spring Cici and Van Acker (2009)reported that in Ontario seeds from seedlings thatemerged in August flowered in early spring (mid-April)and seeds from seedlings that emerged in springflowered in May In a Michigan study seed maturityexpressed as 50 of seed release from the plant occurredby 31 May and 28 May for 840 and 920 growing degreedays (GDD) with a base temperature of 0 degC in 2009and 2010 respectively (Hill et al 2014)

Dormancy triggers (release and re-entry) and germina-tion triggers are an ecological adaptation mechanismthat prevents germination under conditions unfavoura-ble for survival of C bursa-pastoris Freshly harvested seedis almost completely dormant (primary dormancy)(Popay and Roberts 1970a Baskin et al 2004 Hillet al 2014) and not all seed is released from dormancyin one year After release from primary dormancy un-germinated seed may become conditionally dormantdepending on environmental conditions Seed dor-mancy both primary and (or) conditional must be mini-mal to allow for seed germination Baskin and Baskin(1989) reported that C bursa-pastoris seed freshlyharvested (dormant) in May became non-dormant (after-ripening) and capable of germinating after beingexposed to high temperatures (2515 to 3520 degC daynight temperatures) Seeds that fail to germinate in fall




or become conditionally dormant at 5 degC germinate inspring Baskin et al (2004) reported that seed collectedfrom spring and fall germinated plants grown at highlatitudes was dormant and neither was capable of germi-nation in the fall but rather it was only possible inspring the following year

In the case of a small seeded species depth of seedplacement can be critical Popay and Roberts (1970b)reported C bursa-pastoris germination is influenced bylight (red light stimulation) increased temperaturefluctuations between cool and warm temperaturescarbon dioxide (anoxia) soil nitrate and nitrite concen-tration all of which could be influenced by depth of seedplacement or by tillage Under field conditions Cici andVan Acker (2009) reported the primary microsite condi-tions temperature moisture and light were modifiedby CO2 nitrate and nitrite concentrations Optimal soildepths are reported to belt 2 cm

In agricultural systems C bursa-pastoris co-evolved withcrops and predictable periodic disturbance (by tillageandor herbicide) Annuals respond to the environmentvia dormancyrelease germination and phenotypic plas-ticity to avoid disturbance and successfully produceseed Predictable emergence patterns may be useful forguiding the timing of weed control (Cici and Van Acker2009) Werle et al (2014) planted seeds of C bursa-pastorisin July at four sites over two years in Nebraska andmeasured emergence for one year For C bursa-pastoris30 emerged in fall with a further 70 emerging in latewinter and spring Soil temperature was the most usefulparameter in modeling emergence although soilmoisture was necessary for germination The time ofemergence of the maternal plant may affect the seedgermination and morphology of the seed and plantVan Acker and Cici (2012) reported that spring emergingplants produced seed that germinated faster floweredearlier and resulted in differential allocation of biomassto roots and reproductive tissue

(d) Vegetative reproductionThis species does not reproduce vegetatively

9 HybridsNatural triploid hybrids between the tetraploid

C bursa-pastoris and its diploid relative C rubella Reut(C times gracilis Gren) have occurred in mixed populationsIn the UK such hybrids tend to have very long inflores-cences but very little seed (Stace 1997) indicating failureof the seed to develop Successful hybrids are thought tobe unlikely for several reasons the chromosomenumber difference C bursa-pastoris and C rubella areboth primarily self-fertilizing both possess very smallnectaries reducing insect visitation and the species havedifferences in flowering time with a tendency for thetetraploid species to flower earlier than the diploid(Neuffer and Eschner 1995 Hawes et al 2005)

Several studies have investigated the inter-compatibilityof C bursa-pastoris and the emerging oilseed Camelinasativa (L) Crantz another member of the Camelineaetribe (Al-Shehbaz 2012) to assess the risk of transgeneintrogression Seacuteguin-Swartz et al (2011) observed thatwhen C sativa was the male parent pollen tubes grew tothe ovules indicating that no pre-fertilization barriersappear to exist between the species Julieacute-Galau et al(2014) recorded the production of eight hybrids in handfrom 95 hand crosses (1 hybrid for 15 ovules pollinated)with C sativa as the male parent though the use of ahemizygous C sativa marker (DsRed) to detect hybridiza-tion may mean that even this high estimate of hybridiza-tion could have underestimated the number of hybridsproduced The stamens in these hybrids failed to elon-gate and did not produce pollen Martin et al (2015) pro-duced seven hybrids with pollination of Canadianaccessions of C bursa-pastoris by C sativa detected byDNA content using flow cytometry and species specificinternal transcribed spacer (ITS) markers from 1864crosses and estimated a much lower hybridization rateof 15 hybrids per 10 000 ovules pollinated As with thoseproduced by Julieacute-Galau et al (2014) hybrids had low pol-len viability based on staining with a 2 acetocarminesolution and neither pollination by the parental speciesnor intentional self-pollination resulted in viable seedleading to the conclusion that genome duplication maybe the only route to F2 progeny between the species(Martin et al 2015) Zhang and Auer (2020) obtainedhybrids at rates lower than Julieacute-Galau et al (2014) buthigher than Martin et al (2015) which produced low pol-len and ovule numbers from bidirectional crosses with Csativa as both the female (31 hybrids per 1000 ovules) andthe male parent (29 hybrids per 1000 ovules) Thesehybrids also were unsuccessful in backcrosses

Tissue culture techniques have also been used toattempt wider crosses For example somatic hybridsfrom C bursa-pastoris protoplast and rapid-cyclingBrassica oleracea have been generated to determine thepotential for transferring Alternaria brassicicola resistanceto the crop Hybrid lines that resulted in rooted plantswere planted in the soil and grown until floweringThey displayed combined morphological features leaveswere lanceolate with trichomes similar to Capsella andhad serrated margins similar to B oleracea Flowersshowed intermediate morphology but male sterilityWhen hybrids were pollinated with B oleracea no seedproduction was observed indicating poor fertilityAlternaria brassicicola resistance was detected amongone of the hybrids tested indicating its use for breedingresistance Unfortunately these plants did not survivefor a long period in the greenhouse (Sigareva andEarle 1999)

10 Population DynamicsCapsella bursa-pastoris is an opportunistic annual plant

that can colonize newly disturbed open or dry

Ahmed et al 539



environments forming a high percent cover and isfound ubiquitously in cultivated lands in Canada Inannual crops in western Canada C bursa-pastoris hasbeen one of the 20 most abundant weeds since weedsurveys were first conducted in 1970 In Canada plantstend to emerge in two peaks in spring and late summerfall (see Section 8(c) Seed banks seed viability and ger-mination) It is found growing in various climates andniches however abundance decreases in less disturbedareas to exclusion once perennial grasses establish(Bosbach et al 1982 Aksoy et al 1998 Begg et al 2012)For example Monzeglio and Stoll (2005) describeC bursa-pastoris as a weak competitor and determinedthat the species has higher fitness when in a monocul-ture than when mixed with other annual speciesBy evaluating accessions of C bursa-pastoris from both acolonization front and from the core area of the naturalrange Orsucci et al (2020) demonstrated that althoughthe ecotypes from the colonization showed less fitnessas measured through various growth and reproductiveparameters they were better able to avoid competitiondue to a shift in phenology

11 Response to Herbicides and Other ChemicalsCapsella bursa-pastoris is susceptible to most foliar

(post-emergence) herbicides recommended for the con-trol of dicot annual weeds in a range of crops (OMAFRA2020 Saskatchewan Guide to Crop Protection 2020)Herbicide resistant populations have been selected butare generally managed through the use of alternativeherbicides or herbicide mixtures

Capsella bursa-pastoris can be controlled with mostbroadleaf herbicides Exceptions include group 3 mitoticinhibitors group 4 auxinic herbicides in the pyridinecarboxylic acid family and group 6 photosystem IIinhibitors Control is influenced by the timing of herbi-cides application(s) in relation to annual and winter croprotations and the time of emergence of this facultativewinter annual weed Residual control is often desirablebecause multiple flushes of emergence usually occurthroughout the spring and fall emergence period It canbe readily controlled by non-selective herbicides suchas glyphosate pre-seeding and glyphosate and glufosi-nate and with group 2 ALS inhibitors in herbicideresistant crops with the exception of ALS resistant popu-lations (see below)

Capsella bursa-pastoris can be controlled (lt 90) inalfalfa and alfalfa grass mixtures with metribuzinapplied in fall spring applied imazethapyr and imaza-mox while spring applied MCPA provided an average of81 control (Wilson and Orloff 2008) In turf grass thereare many available herbicides for control the most com-monly used herbicides are 24-D 24-DP mecoprop anddicamba (PennState Center for Turfgrass Scienceaccessed 10 July 2021 httpsextensionpsueduweed-management-in-turfsection-47) Capsella bursa-pastorispresents challenges to postemergence herbicide control

in certain crops such as cole crops because of its similar-ity to the crop (Freyman et al 1992)

Capsella bursa-pastoris has been selected for resistanceto a number of herbicides Resistance to ALS inhibitorswas reported in Israel in 2000 (imazapyr) in Canada in2008 (imazamox imazethapyr thifensulfuron methodand tribenuron methyl) in China in 2009 (tribenuron-methyl) in Demark in 2012 (florasulam and tribe-nuron-methyl) and in Norway in 2019 (iodosulfuron-methyl-Na) (Wang et al 2011 Zhang et al 2017 Heap2021) Resistance to ALS inhibitor tribenuron methyl inpopulations from China was due to a single amino acidchange at position 197 (Jin et al 2011 Cui et al 2012)

Resistance to the herbicide hexazine was reported inOregon due to a change in the PSII target site changefrom Phe to Ile in the psbA gene at position Phe255(Perez-Jones et al 2009) This alteration conferred 22-foldresistance to hexazine compared with the susceptiblepopulation The hexazinone-resistant population wascross-resistant to metribuzin but susceptible to atrazinediuron and terbacil Other reported cases of C bursa-pastoris herbicide resistance include simazine-resistancein 1984 in Poland (Heap 2021)

12 Response to Other Human ManipulationsMany agronomic factors including tillage timing and

intensity nutrient regime crop type use of cover cropsall can influence populations of C bursa-pastorisIncreasing competition through cover crops or greenmanure and changing row spacing and flaming can beeffective means of controlling or suppressing growthThe density of C bursa-pastoris increased in the upper soillayer that was subjected to reduced tillage relative toconventional tillage in a study conducted to observethe effects of tillage on weed density in California(Fennimore and Jackson 2003)

A variety of cover crops and green manures have beenreported to reduce C bursa-pastoris emergence or densityBrassica napus L or Sinapis alba L planted in fall andincorporated into the soil in spring prior to plantingof peas provided 76 and 97 suppression ofC bursa-pastoris emergence respectively in Mt VernonWashington USA (Al-Khatib et al 1997) In Germany inorganic Triticum aestivum L fields legume cover crops amixture of Trifolium repens L Trifolium subterraneum LMedicago truncatula Gaertner and Lotus corniculatus L wereable to suppress C bursa-pastoris at one site comparedwith the control treatment (Hiltbrunner et al 2007)Buckwheat residues reduced emergence and growth ofC bursa-pastoris compared with bare soil by reducingavailable nitrogen but the addition of nitrogen fertilizernegated this effect (Kumar et al 2008) Mennan et al(2009) reported that cover crop residue from grain sor-ghum [Sorghum bicolor (L) Moench] sudangrass [Sorghumtimesdrummondii (Nees ex Steud) Millsp amp Chase] hairy vetch(Vicia villosa Roth) grain amaranth (Amaranthus sp) orpea (Pisum sativum L) residue suppressed emergence of




C bursa-pastoris for organic kale production Franczuket al (2010) reported that cover crops phacelia (Phaceliatanacetifolia Benth) vetch (Vicia sativa L) serradella(Ornithopus sativus Brot) and oat (Avena sativa L)suppressed C bursa-pastoris emergence in onion (Alliumcepa L) and cabbage (Brassica oleraceae L) crops Plantingcabbage at higher densities can also reduce C bursa-pastoris growth between the rows (Freyman et al 1992)Weed flaming can also effectively control C bursa-pastorisin the cotyledon stage but requires a higher flaming dosein the rosette stage (2 to 5 leaves) (Sivesind et al 2009)Harvest weed seed control promises to provide a tool forreducing populations of seed banking plants likeC bursa-pastoris a Danish study identified it as a reason-ably good target ie ldquointermediaterdquo for this controlmethod (Bitarafan and Andreasen 2020)

Capsella bursa-pastoris is common in annual pasturesand perennial forages in western Canada It wasreported to be more common in annual than perennialforages especially in the spring with increased grazingintensity leading to increased density (Harker et al2000) Disturbances and fertilizer application generallyincrease C bursa-pastoris abundance and fecundity inpastures While soil compacted due to trampling resultsin short and twisted roots trampling provided betterdispersal rapid germination and establishment(Ellenberg 1988 Aksoy et al 1998) Neuffer and Meyer-Walf (1996) reported that by comparison to an arablefield C bursa-pastoris growing in a trampled area exhib-ited later but more plastic flowering onset with morevigorous rosettes and greater variation in other growthparameters but less seed production Plants in the tram-pling area also showed a greater response to nutrientadditions

13 Response to Herbivory Disease and HigherPlant Parasites(a) Herbivory(i) Mammals

In annual cattle pastures in Alberta C bursa-pastorisand other annual forbs declined in numbers over theseason because although the cattle grazed mainly onsown forage grasses grazing removed the apicalmeristem of the weeds leaving little opportunityfor the weed seedlings to re-establish later in the sea-son (Harker et al 2000) In Great Britain C bursa-pastoris grazed by cattle sheep and other grazers suchas yaks (Aksoy et al 1998) and by rabbits in grasslandshad reduced populations and exhibited delayedflowering in damaged plants for up to four weeks(Crawley 1990)

(ii) Birds or other vertebratesMarshall et al (2003) recorded feeding by several bird

species on seeds of C bursa-pastoris

(iii) InsectsLepidoptera

Capsella bursa-pastoris is among the more frequentlyvisited wild cruciferous plants by the butterfly Anchariscardamines L (Pieridae) (Wiklund and Friberg 2009)Eggs are laid on the flowering ramets which providefood for the developing larvae as the fruits matureOver a five-year study period 93ndash124 of larvaesurvived on C bursa-pastoris with the leading causes oflarval mortality being starvation in very dry summerperiods and attacks by braconid wasps Compared withother summer-flowering mustards C bursa-pastorisencountered less herbivory by Pieris rapae L the cabbagewhite butterfly and supported less relative growth rateof the first instar in common garden conditions(Lariviere et al 2015) Similarly C bursa-pastoris is amongbrassicaceous host species of the diamondback mothPlutella xylostella (L) (Plutellidae) and despite supportinglow insect growth and survival rates their overwinteringseedlings can be bridge hosts until more-favourableannual wild or crop plants become available (Sarfrazet a 2011) In British Columbia vineyards C bursa-pastorisis a host of the climbing cutworm pest of grapevinesAbagrotis orbis (Grote) (Noctuidae) (Mostafa et al 2011)but the cutworm larvae did not survive beyond the thirdinstar on Capsella suggesting that it could reducecutworm damage to the vines In China female adults ofP xylostella produced more eggs (over 300 per adult) onC bursa-pastoris than on other wild host plants (Niu et al2014)

Hymenoptera

The parasitoid wasp Cotesia saltator Thunb(Braconidae) frequently feeds on and kills the larvae ofthe butterfly Anthocharis cardamines found on C bursa-pastoris and other wild cruciferous plants (Wiklund andFriberg 2009) Anaphes iole Girault (Mymaridae) a waspparasitic on the eggs of Lygus spp was not able to obtainmeaningful food resources from C bursa-pastoris animportant host of Lygus lineolaris P Beauv (Williams andHendrix 2008) Among hosts of diamondback mothlarvae parasitism by the wasp Diadegma insulare(Cresson) as well as its growth rates and longevity arelowest on C bursa-pastoris (Sarfraz et al 2012)

Thysanoptera

The western flower thrips Frankliniella occidentalisPergande is the primary vector of viruses that infectcrops and crop weeds including C bursa-pastoris inCalifornia (Kuo et al 2014 Section 13(b) iii Viruses)

Coleoptera

Different species of ground beetles (Carabidae) feed onthe seeds of C bursa-pastoris in many parts of the worldwhile at least one feeds on C bursa-pastorisrsquo rootsCalathus ruficollis Dejean and Tanystoma maculicolle Dejeanshow very high seed predation rates in California

Ahmed et al 541



vineyards the highest rates of 64 plusmn 9 for the formerand of 41 plusmn 11 for the latter occurred in the cover cropand untreated control (Sanguankeo and Leon 2011)Indeed in a lab experiment Sanguankeo and Leon(2011) showed C bursa-pastoris was one of the two out ofeight weed species that was voluntarily eaten by carabidbeetles In the Czech Republic seed consumption byAmara aenea DeGeer A familiaris (Duftschmid) A similata(Gyllenhal) and (Pseudophonus) Harpalus rufipes DeGeerwas more discriminating at the larval than at the adultstages A similata preferred seeds of C bursa-pastoris atthe first instar and adult stages and A aenea andA similata showed higher reproductive rates on eithersingle-seed Capsella diets or mixed-seed diets (Saska2008a Klimeš and Saska 2010 Saska et al 2014) Theweevil Ceutorhynchus typhae (Herbst) feeds on seeds ofC bursa-pastoris in Europe and in eastern Canada (Mulleret al 2011) In Japan (Sasakawa 2011) C bursa-pastoris is afood source for A chalcites Dejean and A congruaMorawitz with 73 survival rates of the former and 60of the latter Mixed seed and larval diets were somewhatmore important than single-seed diets in developmentand growth of new adults Root herbivory by Phylloperthahorticola (L) has been documented to result in substantialbiomass loss (Gange and Brown 1989)

Hemiptera

Capsella bursa-pastoris is an accidental host of thecabbage aphid Brevicoryne brassicae L (Aphididae) permit-ting short-term development of the aphid followingstylet penetration and sap ingestion and a considerabledelay between finding and accepting the phloem by theinsect suggesting a deterrent factor in the sieve ele-ments of the plant (Gabryś and Pawluk 1999) The aphidMyzus ascolonicus Donc (Aphididae) is known to transmitthe beet mild yellowing virus (BMYV) and the beetwestern yellows virus (BWYV) to C bursa-pastoris inEurope (Stevens et al 1994) In China C bursa-pastoris ishost of the small brown planthopper Laodelphax striatellus(Falleacuten) (Delphacidae) (Qiao et al 2009) Three aphidspecies have been reported on C bursa-pastoris inIndonesia Aphis craccivora Koch Myzus ornatus Laing andRhopalosyphum padi L (Noordam 2004) Intraspecificvariation within C bursa-pastoris resulted in differentialresponses by the phloem-feeding aphids Aphis fabaeScopoli and Myzus persicae Sulzer (Aphididae) to suchvariants as greater tissue water content a low carbonnitrogen ratio or lower phloem nitrogen (Karley et al2008) In arable field plots sap-feeding insects weremore attracted to early-flowering than to late-floweringecotypes of C bursa-pastoris (Karley et al 2011) Capsellabursa-pastoris is a spring host of the tarnished plant bugLygus lineolaris P Beauv (Miridae) in cotton crops in theMississippi Delta (Snodgrass et al 2006) The species isalso a host of the wheat bug Nysius huttoni White(Lygaeidae) which damages wheat and cultivated

cruciferous crops (Wei 2008) However C bursa-pastorisshowed resistance towards Lipaphis erysimi (Kalt) in acaged pot experiment (Singh et al 2014)

Diptera

In cruciferous vegetable crops in southern OntarioC bursa-pastoris was among hosts of the swede midgeContarina nasturtii (Kieffer) (Cecidomyiidae) (Hallett2007) Flower galls have been produced on C bursa-pastoris by the gall midge Gephyraulus capsellae Skuhrava(Cecidomyiidae) (Skuhrava 2011)

(iv) Nematodes and (or) other non-vertebratesCapsella bursa-pastoris was among weed hosts of the

sugar-beet nematode Heterodera schachtii Schmidt inGermany cysts were formed regularly and root diffusatesincreased hatching of the larvae (Gleissl et al 1989) InOhio soybean crops C bursa-pastoris was identified as aminor alternative host of the soybean cyst nematodeH glycines Ichinohe but was one of only four such hostson which reproduction of the nematode occurred(Venkatesh et al 2000) Attention has recently focusedon alternative hosts of H glycines among winter annualweeds such as C bursa-pastoris which have the potentialto provide a niche for reproduction and populationincrease of this nematode pest in the seasonal absenceof the soybean crop (Johnson et al 2008) There isevidence of C bursa-pastoris root consumption by ecto-parasitic nematode species Trichodorus and Paratrichodorus(Iannetta et al 2010) The land slug Agriolimax caruanaePollinera ate whole or parts of leaves of C bursa-pastorisresulting in reduced plant size but almost never in deathof the plant (Dirzo and Harper 1980) Herbivory by slugson crucifers including C bursa-pastoris resulted in asignificant reduction in stem mass and fruit production(Rees and Brown 1992) The land slugs Arion lusitanicus(= A vulgaris Mabille) and Deroceras reticulatum(OF Muumlller) are attracted to C bursa-pastoris andpresence of the weed in oilseed rape (Brassica napus L)crops considerably reduced the number of rape plantsdestroyed by the slugs (Frank and Friedli 1999) Indeedthe leaves of C bursa-pastoris are highly palatable toD reticulatum as shown in leaf preference tests betweenC bursa-pastoris and Triticum aestivum L (Cook et al 1996)The woodlice Armadillidium vulgare Latreille and Porcellioscaber Latreille species of terrestrial isopods wereobserved feeding on seeds of C bursa-pastoris in cropfields and adjacent non-crop habitats (Saska 2008bSaska et al 2014)

(b) Diseases(i) Fungi and oomycetes

Capsella bursa-pastoris is host to numerous fungalpathogens listed in detail in Farr and Rossman (2020)These are summarized according to the type of diseasetransmitted to the plants Unless otherwise indicatedthe reference is (Farr and Rossman 2020)




Black leg

Both virulent and weakly-virulent strains ofLeptosphaeria maculans (Sowerby) P Kaarst isolated fromsymptomless canola (Brassica napus L) C bursa-pastorisand other weeds in Saskatchewan could act as a reser-voir of inoculum of black leg disease in the absence of acanola crop (Petrie et al 1995) This fungus has beenreported in New Zealand

Club root

Plasmodiophora brassicae Woronin was reported inCanada (Connors 1967) a few US states Australia andNew Zealand

Leaf curl and wilt

The seed-borne Verticillium dahlia Kleba was reportedin British Columbia Canada (Ginns 1986) It is a majorcause of wilt in lettuce crops in California where viru-lent isolates of this fungus in C bursa-pastoris and otherweeds serve as inoculum in crops (Vallad et al 2005)

Leaf spot

Mycosphaerella brassicicola (Duby) Lindau is a source ofringspot in Saskatchewan (Ginns 1986) Pseudocercosporellacapsellae (Ellis amp Everh) Deighton produced white leafspot in Ontario (Braun 1995) Saskatchewan (Ginns1986) a few central states in the US several countries innorthern Europe and in South Korea Cylindrosporiumcapsellae Ellis and Everh was reported in several centralUS states south to Texas Sphaerella passeriniana Sacc wasreported in Spain and Cercospora nasturtii var capsellaePass in the former Soviet Union and Ukraine

Mildews

Capsella bursa-pastoris can be host to powdery mildewsof Erysiphe spp particularly E cruciferarum Opiz exL Junell which are widespread in Europe and have alsobeen reported from Japan and India As well as thedowny mildews Hyaloperonospora (= Peronospora)spp notably H parasitica (Pers) Constant werereported from British Columbia and Saskatchewanin Canada (Ginns 1986) from Alaska (Connors 1967)from throughout the northern US from Europe(Constantinescu and Fatehi 2002) Algeria Central AsiaChina and India Additionally the species has beenreported to host Golovinomyces cichoracearum (DC) VPHeluta was reported in Korea G orontii (Castagne) VPVeluta in Switzerland Germany Poland (Farr andRossman 2020) and Slovenia (Radisek et al 2018) andOidium sp in Australia

Moulds

Cultural filtrates of the saprophytes Penicillium sp andAspergillus niveus Blochwitz suppressed the growth ofseeds of C bursa-pastoris in Ukraine (Savchuk 2012) Theyeast-like saprophyte Tilletiopsis minor Nyland identifiedin British Columbia Canada forms colonies on leaves

(Urquhart et al 1997) The saprophytes Trichodermakoningii Oudem and T viride Pers reported in Polandcause green mould rot Sclerotinia spp reported onC bursa-pastoris in alfalfa fields in Maryland US causedleaf and stem blight (Morgan 1971) Other reports ofwhite and grey moulds on C bursa-pastoris includeSclerotinia sclerotiorum (Lib) De Bary in China andTaiwan Botrytis cinerea Pers in China and Cladosporiumcladosporioides (Fresen) GA de Vries and Scopulariopsisbrumptii Salv-Duval in Poland

Root rot

Capsella bursa-pastoris was among hosts of Lagenaradicicola Vanterp amp Ledingham from Nova Scotia westto Alberta in Canada (Barr and Deacutesaulniers 1990)Rhizophydium graminis was reported on the species inOntario (Ginns 1986) Other root rot fungi in Canadainclude Ligniera pilorum Fron amp Gaillet in OntarioPythium spp in British Columbia and P polymastumDrechsler in Saskatchewan The saprophytic soil-bornepathogen Rhizoctonia solani Kuumlhn reported fromWashington State causes lesions on the collet betweenthe stem and root progressing from collar to root rotand also attacks seeds [United States Department ofAgriculture (USDA) 1960] Aphanomyces euteichesDrechsler was reported in New Zealand and Humicolagrisea Traaen in Poland

Rusts

White blister rusts caused by the parasitic fungusAlbugo candida (Pers) Kuntze (= A cruciferarum (DC)A Gray Cystopus candidus (Pers) Leacutev) result in white orcream-coloured sori found on leaves shoots and flower-ing parts of C bursa-pastoris (Heller and Thines 2009Mirzaee and Sajedi 2015) The species is the type host ofrace 4 of this fungus and is among Brassicaceae thatbecame resistant to their particular race of A candidafollowing transfer of the white rust resistance geneWWR4 from Arabidopsis thaliana (L) Heynh (Borhan et al2008 2010) Virulent isolates from C bursa-pastoris cellsrevealed very rapid spread and development of this fun-gus including sporangia production in the absence ofhost cell necrosis (Soylu et al 2003) In Canada A candidahas been reported in British Columbia andSaskatchewan (Ginns 1986) and is common on all conti-nents A new species A koreana YJChoi Thines ampHDShin infecting C bursa-pastoris was identified inKorea (Choi et al 2007) A case of white blister rustcaused by A candida and A koreana has been reported inIran (Mirzaee and Sajedi 2015) The rust Puccinia aristidaeTracy is found on C bursa-pastoris in several US statesDouble infection by A candida and Hyaloperonosporaparasitica (= Peronospora) has been observed in diseasedinflorescences of C bursa-pastoris (Sansome and Sansome1974) and may reduce the number of individuals in estab-lished stands and any recruitment for future generations(Alexander and Burdon 1984) Of the 17 races or

Ahmed et al 543



pathotypes of A candida races Ac1 to Ac6 were found tobe specific to the host C bursa-pastoris in Australia(Petkowski et al 2010) A strain of A candida isolatedfrom C bursa-pastoris in western Australia was patho-genic on Brassica juncea (L) Czern but the B junceaisolate was not pathogenic on C bursa-pastoris (Kaur et al2011)

Stem disease

Colletotrichum dematium (Pers) Grove was reportedto have infected C bursa-pastoris in Saskatchewan(Ginns 1986) In the United Kingdom C bursa-pastoriswas among weed hosts of crown and stem rot diseasescaused by Fusarium spp particularly F avenaceum (Fr)Sacc pathogenic to seedlings of winter wheat(Jenkinson and Parry 1994) Seedling blight for C bursa-pastoris was caused by F culmorum (WCSm) Sacc inPoland

(ii) BacteriaWild hosts including C bursa-pastoris of Spiroplasma

citri a bacterial causative agent of brittle root disease ofhorseradish (Armoracia rusticana Gaertn Mey amp Sherb)were found to be sources for transmission of the bacte-rium by the beet leafhopper (Circulifer tenellus Baker) inIllinois (OrsquoHayer et al 1984) The bacterial pathogenXanthomonas campestris pv campestris was recovered fromC bursa-pastoris in cruciferous crop fields in Oklahomaand was found to be the only weed that harbouredbacterial pathogens in those fields (Zhao et al 2002)The survey indicated that C bursa-pastoris was not onlyan alternative host for this pathogen but might also playa role in the secondary disease cycle of black rot and leafspot of cruciferous field crops Other causal agents ofbacterial leaf spots were not recovered from C bursa-pastoris In California almond orchards C bursa-pastorishas been infected by the bacterium Xylella fastidiosa acause of almond leaf scorch usually transmitted byhemipteran vectors such as the blue-green sharpshooterGraphocephala atropunctata Signoret (Shapland et al2006) The bacterium Rhizobacter dauci the causal agentof carrot bacterial gall produced galls on the roots of awide range of host species including C bursa-pastoris inJapan (Kawarazaki et al 2012)

Lee et al (2016) identified nine species of spore-forming bacilli bacteria from fresh samples of C bursa-pastoris in South Korea Bacillus drentensis B acidicelerB aryabhattai B asahii B firmus B pseudomycoidesB psychrodurans B simplex Bacillus sp Paenibacillus lautusP barcinonensis P tundra and Brevibacillus reuszeri Thesebacteria are ubiquitously present in nature their endo-spores are generally found in soil and all isolates are ableto produce enzymes that are responsible for food spoil-age and can make the consumption of plant materials afood safety concern (Lee et al 2016)

(iii) VirusesCertain strains of the aphid-transmitted beet western

yellows virus (BWYV) caused severe yellowing and stunt-ing of infected C bursa-pastoris (Falk and Duffus 1984Sanger et al 1994) Severe symptoms following inocula-tion with the BWYV strain ST9 did not arise from anychange in confinement of the infection to the phloemIn Great Britain C bursa-pastoris was susceptible toBWYV and to beet mild yellowing virus (BMYV) but notto beet yellows virus (BYV) (Stevens et al 1994) When aCalifornia legume isolate of BWYV was purified from Cbursa-pastoris root tissue yielded four times as much asthe shoots (DrsquoArcy et al 1983) The satellite RNA ofBarley Yellow Dwarf Virus-RPV is transmitted to Cbursa-pastoris by aphids but only in conjunction withBWYV and its ST9 strain (Rasochovaacute et al 1997) A verysmall percentage of C bursa-pastoris plants were infectedby BWYV in sugarbeet seed crops in Oregon (Hamptonet al 1999) BMYV is able to overwinter on C bursa-pastoris and the latter is susceptible to most strains ofbeet yellowing viruses except for a strain of BMYV nowclassified as a new species beet chlorosis virus (BChV)(Stevens et al 2005) and the BMYV-2ITB isolate (Lemaireet al 1995) A German isolate of BMYV used for bothagrinoculation and aphid transmission of the virusproduced systemic infection of C bursa-pastoris by bothmethods (Stephan and Maiss 2006) Visible symptomsincluded both yellowing and leaf-rolling of older leavesArtificially infected C bursa-pastoris is able to transmitbeet mosaic virus through the aphid Myzus ascalonicusDoncaster (Semal 1956) As one of the more abundantweeds in areas adjacent to potato and onion crops inNew York State C bursa-pastoris is host to the potatovirus Y (PVY) and the potato leafroll virus (PLRV) bothtransmitted to crops by aphids particularly the greenpeach aphid Myzus persicae (Selzer) (HomopteraAphididae) (Smith et al 2012) Several genotypes of thataphid are common on C bursa-pastoris in Greece(Blackman et al 2007) In contaminated soil C bursa-pastoris is among alternative hosts for the beet necroticyellow vein virus (BANYVV) the beet soil-borne virus(BASBV) and spores of their protozoan vector Polymyxabetae Keskin (Mouhanna et al 2008) Capsella bursa-pastoris is a potential alternative host of the blackberryyellow vein associated virus (BYVaV) in the UnitedStates (Poudel et al 2013) In California lettuce-growingareas C bursa-pastoris is among crops and weeds infectedby the thrips-transmitted disease Impatiens necrotic spotvirus (INSV) and as a winter annual is a probable virusreservoir and source of primary inoculum forlettuce planted in early spring and for maintaining thevirus between summer- and fall-planted crops (Kuo et al2014) Curly top disease (CTD) caused by viruses in thegenus Curtovirus and spread by leafhoppers severelyinfects C bursa-pastoris causing stunted growth and




distorted and twisted leaves and stems (Chen andGilbertson 2009 Chen et al 2011) Capsella bursa-pastorisis also susceptible to the tobacco rattle virus TRV (genusTobravirus) which is spread by nematodes speciesTrichodorus and Paratrichodorus (Iannetta et al 2010) TRVhas a well-known persistent history of causing economicdamage to potato tubers which appears as arcs ofdiscolouration referred to as spraing

(iv) Other diseasesThe beet leafhopper Circulifer tenellus (Baker)

(Cicadellidae) transmits the phytoplasma BLTVA thecausal agent of the potato purple top disease to bothcrops and several weeds including C bursa-pastoris(Munyaneza et al 2006) The causal agent of clubrootdisease on Brassica spp Plasmodiophora brassicaeWoronin (Rhizaria) has been found on C bursa-pastorisin oilseed rape fields in China with an incidence of62 and 100 respectively Rapid spread of the diseasein both the weed and a cabbage crop was observed (Kimet al 2011 Ren et al 2014)

(c) Higher plant parasitesCapsella bursa-pastoris is host of the field cow-wheat

Melampyrum arvense L a hemi-parasite which attachesitself by haustoria to the roots of the host plant to obtainadditional moisture and nutrients (Lechowski 1995)There are unconfirmed data from Bulgarian floras thatCapsella is a host of the parasitic species Orobanche nanaNoeuml (Stoyanov 2005) A greenhouse study done in DijonFrance showed that Phelipanche ramosa (L) Pomel a para-sitic plant had a low number of successful infections rel-ative to other species in the study (Moreau et al 2016)

AcknowledgementsWe are very grateful for the generous help we received

from the following herbarium curatorial staff ShannonAnescio at the Department of Agriculture Ottawa(DAO) Hugo Cota-Saacutenchez and Denver Falconer at theWP Fraser Herbarium Richard Caners at the RoyalAlberta Museum Kristi Dysievick at the Claude GartonHerbarium and Natalie Iwanycki and Joseph Mentlik atthe Royal Botanic Gardens herbarium We thank JessicaHsiung from Agriculture and Agri-Food Canada (AAFC)for creating the beautiful illustrations of this species fea-tured in Fig 1 Furthermore we thank Matthieu Brouardfor initial work gathering references for this paper Weare very grateful for the input from two anonymousreviewers on an earlier version of the manuscript to helpgenerate a much better overview of this well-studiedplant

ReferencesAksoy A and Gemici Y 1993 Contribution a 1 etude de la flore

du Mahmud dagi (Kemalpasa-Izmir) I J Faculty Sci EgeUniviersity 15 43ndash53

Aksoy A Dixon JM and Hale WHG 1998 Capsella bursa-pastoris (L) Medikus (Thlaspi bursa-pastoris L Bursa bursa-

pastoris (L) shull Bursa pastoris (L) Weber) J Ecol 86171ndash186 doi101046j1365-2745199800260x

Aksoy A Hale WH and Dixon JM 1999 Towards asimplified taxonomy of Capsella bursa-pastoris (L) Medik(Brassicaceae) Watsonia 22 243ndash250

Al-Khatib K Libbey C and Boydston R 1997 Weed suppres-sion with Brassica green manure crops in green pea WeedSci 45 439ndash445 doi101017S0043174500093139

Al-Shehbaz IA 2012 A generic and tribal synopsis of theBrassicaceae (Cruciferae) Taxon 61 931ndash954 doi101002tax615002

Al-Snafi AE 2015 The chemical constituents and pharmaco-logical effects of Capsella bursa-pastoris - A review Int JPharmacol Toxicol 5 76ndash81

Alex JF and Switzer CM 1976 Ontario weeds Descriptionillustrations and keys to their identification OntarioAgricultural College University of Guelph Guelph Ontario

Alex JF 1992 Ontario Weeds Publication 505 Ministry ofAgriculture and Food Queenrsquos Printer Toronto

Alexander HM and Burdon JJ 1984 The effect of diseaseinduced by Albugo candida (white rust) and Peronospora para-sitica (downy mildew) on the survival and reproduction ofCapsella bursa-pastoris (shepherdrsquos purse) Oecologia 64314ndash318 doi101007BF00379127 PMID28311445

Almquist E 1923 Studien tiber Capsella bursa-pastoris II ActaHorti Bergiani 7 41ndash95

Almquist E 1929 Zur Artbildung in der freien Natur Acta HortiBergiani 9 37ndash76

Andreasen C and Stryhn H 2008 Increasing weed flora inDanish arable fields and its importance for biodiversityWeed Res 48 1ndash9 doi101111j1365-3180200800603x

Barr DJ and Deacutesaulniers NL 1990 The life cycle Lagena radi-cola an oomycetous parasite of wheat roots Can J Bot 682112ndash2118 doi101139b90-276

Baskin JM and Baskin C 1989 Germination responses ofburied seeds of Capsella bursa-pastoris exposed to seasonaltemperature changes Weed Res 29 205ndash212 doi101111j1365-31801989tb00860x

Baskin CC and Baskin JM 2006 The natural history ofsoil seed banks of arable land Weed Sci 54 549ndash557doi101614WS-05-034R1

Baskin CC Milberg P Andersson L and Baskin JM 2004Germination ecology of seeds of the annual weeds Capsellabursa-pastoris and Descurainia sophia originating from highnorthern latitudes Weed Res 44 60ndash68 doi101046j1365-3180200300373x

Begg GS Wishart J Young MW Squire GR and IannettaPPM 2012 Genetic structure among arable populations ofCapsella bursa-pastoris is linked to functional traits and in-fieldconditions Ecography 35 446ndash457 doi101111j1600-0587201107030x

Benvenuti S 2007 Natural weed seed burial effect of soil tex-ture rain and seed characteristics Seed Sci Res 17 211ndash219doi101017S0960258507782752

Bischoff R Vogl CR Ivemever S Klarer F Meier B andHamgurder M and Walkenhorst 2016 Plant and naturalproduct based homemade remedies manufactured and usedby farmers of six central Swiss cantons to treat livestockLivest Sci 189 110ndash125 doi101016jlivsci201605003

Bitarafan Z and Andreasen C 2020 Seed retention of tencommon weed species at oat harvest reveals the potentialfor harvest weed seed control Weed Res 60 343ndash352doi101111wre12438

Bitterlich I and Upadhyaya MK 1990 Leaf surface ultrastruc-ture and susceptibility to ammonium nitrate injury Can JBot 68 1911ndash1915 doi101139b90-251

Bitterlich I Upadhyaya MK and Shibairo SI 1996 Weedcontrol in cole crops and onion (Allium cepa) using

Ahmed et al 545



ammonium nitrate Weed Sci 44 952ndash958 doi101017S0043174500094984

Blackman RL Malarky G Margaritopoulos JT and TsitsipisJA 2007 Distribution of common genotypes of Myzus persi-cae (Hemiptera Aphididae) in Greece in relation to life cycleand host plant Bull Entomol Res 97 253ndash263 doi101017S0007485307004907 PMID17524157

Borhan MH Gunn N Cooper A Gulden S Toumlr MRimmer SR and Holub EB 2008 WRR4 encodes a TIR-NB-LRR protein that confers broad-spectrum white rust resis-tance in Arabidopsis thaliana to four physiological races ofAlbugo candida Mol Plant Microbe Interact 21 757ndash768doi101094MPMI-21-6-0757 PMID18624640

Borhan MH Holub EB Kindrachuk C Omidi MBozorgmanesh-Frad G and Rimmer SR 2010 WRR4 abroad-spectrum TIR-NB-LRR gene from Arabidopsis thalianathat confers white rust resistance in transgenic oilseed bras-sica crops Mol Plant Pathol 11 283ndash291 doi101111j1364-3703200900599x PMID20447277

Bosbach K Hurka H and Haase R 1982 The soil seed bank ofCapsella bursa-pastoris (Cruciferae) Its influence on populationvariability Flora 172 47ndash56 doi101016S0367-2530(17)31310-5

Bourdoumlt GW Hurrell GA and Saville DJ 1998 Weed floraof cereal crops in Canterbury New Zealand N Z J CropHortic Sci 26 233ndash47

Braun U 1995 A monograph of Cercosporella Ramularia andallied genera (phytopathogenic Hyphomycetes) Vol 1 IHW-Verlag Eching

Brooks RR 1987 Serpentine and its Vegetation Croom HelnmLondon

Bussmann RW Batsatsashvili K Kikvidze Z Khajoei NasabF Ghorbani A Paniagua-Zambrana NY et al 2019 Capsellabursa-pastoris (L) Medik B Pages 1ndash10 in K BatsatsashviliZ Kikvidze and R Bussmann eds Ethnobotany ofMountain Regions Springer Cham

Chawla A Singh YP Singh P Rawat S Das S and SinghN 2011 Ecological significance of mycotrophy in some tropi-cal weeds Trop Ecol 52 303ndash310

Chen LF and Gilbertson RL 2009 Curtovirus-cucurbit inter-action acquisition host plays a role in leafhopper transmis-sion in a host-dependent manner Phytopathology 99101ndash108 doi101094PHYTO-99-1-0101 PMID19055441

Chen LF Vivoda E and Gilbertson RL 2011 Geneticdiversity in curtoviruses a highly divergent strain of Beetmild curly top virus associated with an outbreak of curlytop disease in pepper in Mexico Arch Virol 156 547ndash555doi101007s00705-010-0884-9 PMID21193937

Choi Y-J Shin H-D Hong S-B and Thines M 2007Morphological and molecular discrimination among Albugocandidamaterials infecting Capsella bursa - pastoris world-wideFungal Divers 27 11ndash34

Choi WJ Kim SK Park HK Sohn UD and Kim W 2014Anti-inflammatory and anti-superbacterial properties of sulfor-aphane from shepherdrsquos purse Korean J Physiol Pharmacol18 33ndash39 doi104196kjpp201418133 PMID24634594

Choi B Jeong H and Kim E 2019 Phenotypic plasticity ofCapsella bursa-pastoris (Brassicaceae) and its effect on fitnessin response to temperature and soil moisture Plant SpeciesBiol 34 5ndash10 doi1011111442-198412227

Cici SZH and Van Acker RC 2009 A review of the recruit-ment biology of winter annual weeds in Canada Can JPlant Sci 89 575ndash589 doi104141CJPS08131

Cici SZH and Van Acker RC 2011 Relative freezing toler-ance of facultative winter annual weeds Can J Plant Sci91 759ndash763 doi104141cjps2010-001

Conn JS and Deck RE 1995 Seed viability and dormancy of17 weed species after 97 years of burial in Alaska Weed Sci43 583ndash585

Conn JS and Werdin-Pfisterer NR 2010 Variation in seedviability and dormancy of 17 weed species after 247 years ofburial The concept of buried seed safe sites Weed Sci 58209ndash215 doi101614WS-D-09-000841

Connors IL 1967 An annotated index of plant diseases inCanada and fungi recorded on plants in Alaska Canadaand Greenland Res Branch Canada Dept Agric 1251 1ndash381

Constantinescu O and Fatehi J 2002 Peronospora-like fungi(Chromisia Peronosporales) parasitic on Brassicaceae andrelated hosts Nova Hedwigia 74 291ndash338 doi1011270029-503520020074-0291

Cook RT Bailey SER and McCrohan CR 1996 Slug prefer-ences for winter wheat cultivars and common agriculturalweeds J Appl Ecol 33 866ndash872 doi1023072404957

Coquillat M 1951 Sur les plantes les plus communes aacute la sur-face du globe Bull Mensuel Soc Linn Lyon 20 165ndash170doi103406linly19517425

Crawley MJ 1990 Rabbit grazing plant competition and seed-ling recruitment in acid grassland J Appl Ecol 27 803ndash820doi1023072404378

Cui HI Li X Wang G Wang J Wei S and Cao H 2012Acetolactate synthase proline (197) mutations confertribenuron-methyl resistance in Capsella bursa-pastoris popu-lations from China Pestic Biochem Physiol 102 229ndash232doi101016jpestbp201201007

DrsquoArcy CL Hewings AD Burnett PA and Jedlinski H 1983Comparative purification of two luteoviruses Phytopathology73 755ndash759

Damgaard C Mathiassen SK and Kudsk P 2008 Modelingeffects of herbicide drift on the competitive interactionsbetween weeds Environ Toxicol Chemi 27 1302ndash1308doi10189707-2671

Darbyshire SJ Favreau M and Murray M and CanadaAgriculture and Agri-Food Canada 2000 Common and scien-tific names of weeds in Canada Noms populaires et scientifi-ques des plantes nuisibles du Canada Agriculture andAgri-Food Canada = Agriculture et agroalimentaire CanadaOttawa pp 24

Darbyshire SJ 2003 Inventory of Canadian agriculturalweeds Agriculture and Agri-Food Canada Ottawa [Online]Available from httpdsp-psdpwgscgccaCollectionA42-100-2003Epdf [24 June 2020]

Defelice MS 2001 Shepherdrsquos-purse Capsella bursa-pastoris (L)Medic Weed Technol 15 892ndash895 doi1016140890-037X(2001)015[0892SSPCBP]20CO2

Demars BG and Boerner REJ 1994 Vesicular-arbuscularmycorrhizal fungi colonization in Capsella bursa-pastoris(Brassicaceae) Am Midl Nat 132 377ndash380 doi1023072426593

Demars BG and Boerner REJ 1995 Arbuscular myccorhizaldevelopment in three crucifers Mycorrhiza 5 405ndash408doi101007BF00213440

Deng W Hallett PD Jeng DS Squire GR Toorop PE andIannetta PPM 2015 The effect of natural seed coatings ofCapsella bursa-pastoris L Medic (shepherdrsquos purse) on soil-water retention stability and hydraulic conductivity PlantSoil 387 167ndash176 doi101007s11104-014-2281-8

Dillard HR Bellinder RR and Shah DA 2004 Integratedmanagement of weeds and diseases in a cabbage croppingsystem Crop Prot 23 163ndash168 doi101016S0261-2194(03)00172-8

Dirzo R and Harper JL 1980 Experimental studies on slug-plant interactions II The effect of grazing by slugs on highdensity monocultures of Capsella bursa-pastoris and Poa annuaJ Ecol 68 999ndash1011 doi1023072259471

Douglas GM Gos G Steige KA Salcedo A Holm KJosephs EB et al 2015 Hybrid origins and the earlieststages of diploidization in the highly successful recent




polyploid Capsella bursa-pastoris Proc Natl Acad Sci 1122806ndash2811 doi101073pnas1412277112

Duke JA 2002 Handbook of medicinal herbs 2nd ed CRCPress New York 870 pp

El-Habibi AM and Youssef MM 1981 Contribution to theauto-ecology of three Cruciferous species Journa1 of Collegeof Science University of Riyadh 12 315ndash328

Ellenberg H 1988 Vegetation ecology of Central Europe 4thed Cambridge pp 626

Eschmann-Grupe G Laufkoumltter D and Hurka H 1990 Licht-und temperature influumlsse auf die intraspezifische variationder flavonoid profile bei Capsella bursa-pastoris (L) MedVerh GfOuml 19 82ndash86

Facciola S 1990 Cornucopiamdasha source book of edible plantsKampong Publications Vista

Fahey JW Haristoy X Dolan PM Kensler TW SscholtusI Stephenson KK et al 2002 Sulfurophane inhibitsextracellular intracellular and antibiotic-resistant strainsof Helicobacter pylori and prevents benzo[a]pyrene-inducedstomach tumors Proc Natl Acad Sci (US) 99 7610ndash7615doi101073pnas112203099

Falk BW and Duffus JE 1984 Identification of small single-and double-stranded RNAs associated with severe symptomsin beet western yellows virus-infected Capsella bursa-pastorisPhytopathology 74 1224ndash1229 doi101094Phyto-74-1224

Farr DF and Rossman AY 2020 Fungal databasesSystematic Mycology and Microbiology Laboratory ARSUSDA [Online] Available from httpntars-gringovfungaldatabases [24 Jul 2020]

Fennimore SA and Jackson LE 2003 Organic amendmentand tillage effects on vegetable field weed emergence andseedbanks Weed Technol 17 42ndash50 doi1016140890-037X(2003)017[0042OAATEO]20CO2

Franczuk J Kosterna E and Zaniewicz-Bajkowska A 2010Weed control effects on different types of cover-cropmulches Acta Agric Scand B Soil Plant Sci 60 472ndash479

Frank T and Friedli J 1999 Laboratory food choice trials toexplore the potential of common weeds to reduce slug feed-ing on oilseed rape Biol Agric Hortic 17 19ndash29 doi1010800144876519999754821

Frankton C and Mulligan GA 1987 Weeds of CanadaAgriculture Canada Ottawa ON Publ A22-831986E 143 p

Freyman S Brookes VR and Hall JW 1992 Effect of plant-ing pattern on intra-row competition between cabbage andshepherdrsquos purse (Capsella bursa-pastoris) Can J Plant Sci 721393ndash1396 doi104141cjps92-172

Gabryś B and Pawluk M 1999 Acceptability of differentspecies of Brassicaceae as hosts for the cabbage aphidEntomol Exp Appl 91 105ndash109 doi101046j1570-7458199900471x

Gange AC and Brown VK 1989 Effects of root herbivory byan insect on a foliar-feeding species mediated throughchanges in the host plant Oecologia 81 38ndash42 doi101007BF00377007 PMID28312154

Gerard J 1633 The herball or generall historie of plantes Verymuch enlarged and amended by Thomas Johnson Facsimilereprint 1975 Dover Puśblications Inc New York NY1630 pp

Gerdeman JW 1968 Vesicular-Arbuscular mycorrhiza andplant growth Annu Rev Phytopathol 6 397ndash418

Ginns JH 1986 Compendium of plant disease and decay fungiin Canada Research Branch Agriculture Canada Publication1813 Ottawa ON 416 p

Gleissl W Bachthaler G and Hoffmann GM 1989Investigations on the suitability of weeds of various geo-graphic origins as hosts of the sugar-beet nematodeHeterodera schachtii Schmidt Weed Res 29 221ndash228 [In

German English summary] doi101111j1365-31801989tb00862x

Goun EA Petrichenko VM Solodnikov SU Suhinina TVKline MA Cunningham G et al 2002 Anticancer andantithrombin activity of Russian plants J Ethnopharmacol81 337ndash342 doi101016S0378-8741(02)00116-2 PMID12127234

Gray A 1848 A manual of the botany of the northern UnitedStates from New England to Wisconsin and south to Ohioand Pennsylvania inclusive (the mosses and liverworts byWm S Sullivant) arranged according to the natural systemJ Munroe Boston

Grime JP Hodgson JG and Hunt R 2014 Comparative plantecology A functional approach to common British speciesSpringer Netherlands Dordrecht

Groh H 1947 Canadian weed survey fourth report 1945Canada Department of Agriculture Ottawa ON 56 p

Grosso C Vinholes J Silva LR Guedes de Pinho PGonccedilalves RF Valentao P et al 2011 Chemical composi-tion and biological screening of Capsella bursa-pastoris BrazJ Pharm Sci 21 635ndash644

Hallett RH 2007 Host plant susceptibility to the swede midge(Diptera Cecidomyiidae) J Econ Entomol 100 1335ndash1343doi101093jee10041335 PMID17849887

Hameister S Neuffer B and Bleeker W 2009 Genetic differen-tiation and reproductive isolation of a naturally occurring flo-ral homeotic mutant within a wild-type population of Capsellabursa-pastoris (Brassicaceae) Mol Ecol 18 2659ndash2667doi101111j1365-294X200904216x PMID19457178

Hameister S Nutt P Theiszligen G and Neuffer B 2013Mapping a floral trait in Shepherds pursendashlsquoStamenoid petalsrsquoin natural populations of Capsella bursa-pastoris (L) MedikFlora 208 641ndash647 doi101016jflora201309008

Hampton RO Keller KE and Burt GE 1999 Incidence andeffects of beet western yellows virus in Western Oregon sug-arbeet seed crops J Sugar Beet Res 36 15ndash32 doi105274jsbr36115

Hanzlik K and Gerowitt B 2012 Occurrence and distributionof important weed species in German winter oilseed rapefields J Plant Dis Protect 119 107ndash120 doi101007BF03356429

Harker KN Baron VS Chanasyki DS Naeth MA andStevenson FC 2000 Grazing intensity effects on weed popu-lations in annual and perennial pasture systems Weed Sci48 231ndash238 doi1016140043-1745(2000)048[0231GIEOWP]20CO2

Hartwell JL 1982 Plants used against cancer a surveyFacsimile reprint of Lloydia 30ndash34 1967ndash1971 QuartermanPublications Lawrence Mass USA 710 pp

Hawes C Begg GS Squire GR and Iannetta PPM 2005Individuals as the basic accounting unit in studies of ecosys-tem function functional diversity in shepherdrsquos purseCapsella Oikos 109 521ndash534 doi101111j0030-1299200513853x

Heap I 2021 The International Survey of Herbicide ResistantWeeds [Online] Available from wwwweedscienceorg [7 Jul2021]

Heller A and Thines M 2009 Evidence for the importance ofenzymatic digestion of epidermal walls during subepidermalsporulation and pustule opening in white blister rusts(Albuginaceae) Mycol Res 113 657ndash667 doi101016jmycres200901009 PMID19484808

Hill EC Renner KA and Sprague CL 2014 Henbit (Lamiumamplexicaule) common chickweed (Stellaria media) shep-herdrsquos-purse (Capsella bursa-pastoris) and field pennycress(Thlaspi arvense) Fecundity seed dispersal dormancy andemergence Weed Sci 62 97ndash106 doi101614WS-D-13-000741

Ahmed et al 547



Hiltbrunner J Jeanneret P Liedgens M Stamp P and StreitB 2007 Response of weed communities to legume livingmulches in winter wheat J Agron Crop Sci 193 93ndash102doi101111j1439-037X200700250x

Hintz M Bartholmes C Nutt P Ziermann J and HameisterS 2006 Catching a lsquohopeful monsterrsquo shepherdrsquos purse(Capsella bursa-pastoris) as a model system to study the evolu-tion of flower development J Exp Bot 573531ndash3542doi101093jxberl158 PMID17018770

Hitchcock CL and Cronquist A 1973 Flora of the PacificNorthwest An illustrated manual Seattle University ofWashington Press pp 146ndash157

Holmgren PK Holmgren NH and Barnett LC (eds) 1990Index herbariorum Part 1The herbaria of the world 8th edNew York Botanical Garden New York NY 693 p

Hulteacuten E and Fries M 1986 Atlas of North European vascularplants Part IndashIII maps and commentaries Koeltz ScientificBooks Koumlnigstein Germany 1172 pp

Hur J Yoo M Shin D-B and Lee S 2013 Inhibition of nitricoxide production corresponds to the sulforaphane contentin Korean shepherdrsquos purse (Capsella bursa-pastoris)and related species in BV-2 cell Food Sci Biotechnol 221085ndash1089 doi101007s10068-013-0187-5

Hurka H and Benneweg M 1979 Patterns of seed sizevariation in populations of the common weed Capsellabursa-pastoris (Brassicaceae) Biol Zentralbl 98 699ndash709

Hurka H and Haase R 1982 Seed ecology of Capsella-bursa-pas-toris (Cruciferae) - dispersal mechanism and the soil seed bankFlora 172 35ndash46 doi101016S0367-2530(17)31309-9

Hurka H and Neuffer B 1991 Colonizing success in plantsGenetic variation and phenotypic plasticity in life historytraits in Capsella bursandashpastoris Pages 77ndash96 in G Esser andD Overdieck eds Modern Ecology Basic and AppliedAspects Elsevier Amsterdam

Hurka H and Neuffer B 1997 Evolutionary processes in thegenus Capsella (Brassicaceae) Plant Syst Evol 206 295ndash316doi101007BF00987954

Hurka H Krauss R Reiner T and Woumlhrmann K 1976 Dasbluumlhverhalten von capsella bursa-pastoris (Brassicaceae)theflowering behaviour of Capsella bursa-pastoris (Brassicaceae)Plant Syst Evol 125 87ndash95 doi101007BF00986774

Hurka H Freundner S Brown AH and Plantholt U 1989Aspartate aminotransferase isozymes in the genus Capsella(Brassicaceae) subcellular location gene duplication andpolymorphism Biochem Genet 27 77ndash90 doi101007BF00563019 PMID2712824

Hurka H Friesen N German DA Franzke A and NeufferB 2012 lsquoMissing linkrsquospecies Capsella orientalis and Capsellathracica elucidate evolution of model plant genus Capsella(Brassicaceae) Mol Ecol 21 1223ndash1238 doi101111j1365-294X201205460x PMID22288429

Iannetta PPM Begg G Hawes C Young M Russell J andSquire GR 2007 Variation in Capsella (shepherdrsquos purse)An example of intraspecific functional diversity PhysiolPlant 129 542ndash554 doi101111j1399-3054200600833x

Iannetta PPM Begg GS Valentine TA andWishart J 2010Sustainable disease control using weeds as indicatorsCapsella bursa-pastoris and tobacco rattle virus Weeds and sus-tainable disease control Weed Res 50 511ndash514 doi101111j1365-3180201000816x

Jenkinson NP and Parry DW 1994 Isolation of Fusariumspecies from common broad-leaved weeds and their pathoge-nicity to winter wheat Mycol Res 98 776ndash780 doi101016S0953-7562(09)81054-X

Jin T Liu J Huan Z Wu C Bi Y and Wang J 2011Molecular basis for resistance to tribenuron in shepherdrsquos

purse (Capsella bursa-pastoris (L) Medik) Pestic BiochemPhysiol 100 160ndash164 doi101016jpestbp201103005

Johnson WG Creech JE and Mock VA 2008 Role of winterannual weeds as alternative hosts for soybean cyst nema-tode Crop Manag 7 1ndash9 doi101094CM-2008-0701-01-RV

Johnson SN Staley JT McLeod FAL and Hartley SE 2011Plant-mediated effects of soil invertebrates and summerdrought on above-ground multitrophic interactions J Ecol99 57ndash65 doi101111j1365-2745201001748x

Julieacute-Galau S Bellec Y Faure J-D and Tepfer M 2014Evaluation of the potential for interspecific hybridizationbetween Camelina sativa and related wild Brassicaceae inanticipation of field trials of GM camelina Transgenic Res23 67ndash74 doi101007s11248-013-9722-7 PMID23793580

Kang MS 1983 A study of variation of Capsella bursa- pastoris (L)Medicus Korean J Pl Taxon 13 77ndash88

Karley AJ Hawes C Iannetta PPM and Squire GR 2008Intraspecific variation in Capsella bursa-pastoris in plantquality traits for insect herbivores Weed Res 48 147ndash156doi101111j1365-3180200700617x

Karley AJ Hawes C Valentine T Johnson S Toorop PSquire G et al 2011 Can arable weeds contribute to ecosys-tem service provision Functional diversity in shepherdrsquospurse (Capsella bursa-pastoris (L) Medik) Asp Appl Biol 10931ndash38

Kasianov AS Klepikova AV Kulakovskiy IV Evgeny SFedotova AV Besedina EG et al 2017 High-quality genomeassembly of Capsella bursa-pastoris reveals asymmetry of regula-tory elements at early stages of polyploid genome evolutionPlant J 91 278ndash291 doi101111tpj13563 PMID28387959

Kaur P Sivasithamparam K and Barbetti MJ 2011 Hostrange and phylogenetic relationships of Albugo candida fromcruciferous hosts in western Australia with special referenceto Brassica juncea Plant Dis 95 712ndash718 doi101094PDIS-10-10-0765 PMID30731906

Kawarazaki H Goto M Kato K Kijima T and Takikawa Y2012 Isolation and plant host range of Rhizobacter daucicausal agent of carrot bacterial gall Jpn J Phytopath 78293ndash300 doi103186jjphytopath78293

Kim WG Lee SY Choi HW Hong SK and Lee YK 2011Occurrence of clubroot on shepherdrsquos-purse caused byPlasmodiophora brassicae Mycobiology 39 233ndash234doi105941MYCO2011393233 PMID22783109

Kivilaan A and Bandurski RS 1981 The one hundred-yearperiod for Dr Bealrsquos seed viability experiment Am J Bot68 1290ndash1292 doi101002j1537-21971981tb07838x

Klimeš P and Saska P 2010 Larval and adult seed consump-tion affected by the degree of food specialization in Amara(Coleoptera Carabidae) J Appl Entomol 134 659ndash666doi101111j1439-0418200901463x

Konstantinovic B and Blagojevic M 2014 Weed seed distribu-tion in the soil profile in extensive and intensive vineyardsHerbologia 14 16ndash22

Kozub A Wagner D Studinska-Sroka E and Bylka W 2012Capsella bursa-pastoris ndash a common weed and little-knownmedicinal plant Postepy Fitoterapii 4 250ndash253 [in Polish]

Kumar V Brainard DC and Bellinder RR 2008 Suppressionof Powell amaranth (Amaranthus powellii) shepherdrsquos-purse(Capsella bursa-pastoris) and corn chamomile (Anthemis arven-sis) by buckwheat residues Role of nitrogen and fungalpathogens Weed Sci 56 271ndash280 doi101614WS-07-1061

Kuo Y-W Gilbertson RL Turini T Brennan EB SmithRF and Koike ST 2014 Characterization and epidemiologyof outbreaks of Impatiens necrotic spot virus on lettuce incoastal California Plant Dis 98 1050ndash1059 doi101094PDIS-07-13-0681-RE PMID30708789




Lariviere A Limeri LB Meindl GA and Traw MB 2015Herbivory and relative growth rates of Pieris rapae arecorrelated with host constitutive salicylic acid andflowering time J Chem Ecol 41 350ndash359 doi101007s10886-015-0572-z PMID25893789

Lechowski Z 1995 Element contents and guard cell physiologyof the root hemiparasite Melampyrum arvense L beforeand after attachment to the host plant J Plant Nutr 182551ndash2567 doi10108001904169509365084

Lee KE Shin J Hong IS Cho NP and Cho SD 2013Effect of methanol extracts of Cnidium officinale Makino andCapsella bursa-pastoris on the apoptosis of HSC-2 human oralcancer cells Exp Ther Med 5 789ndash792 doi103892etm2012871 PMID23403540

Lee WJ Kim HB and Kim KS 2016 Isolation and characteri-zation of spore-forming bacilli (SFB) from shepherdrsquos purse(Capsella bursa-pastoris) Characters of SFB from shepherdrsquospurse J Food Sci 81 M684ndashM691 doi1011111750-384113231 PMID26822957

Leeson JY Thomas AG Hall L Brenzil CA Andrews CABrown KR and Van Acker RC 2005 Prairie Weed surveycereal oilseed and pulse crops 1970s to the 2000s WeedSurvey Series Publ 05ndash1 Agriculture and Agri-Food CanadaSaskatoon Research Centre Saskatoon SK 395 pp

Lemaire O Herrbach E Stevens M Bouchery Y and SmithHG 1995 Detection of sugar beet-infecting beet mildyellowing luteovirus isolates with a specific RNA probePhytopathology 85 1513ndash1518 doi101094Phyto-85-1513

Lin P Wu L Wei D Chen H Zhou M Yao X and Lin J2016 Promoter analysis of cold-responsive (COR) genefrom Capsella bursa-pastoris and expression character inresponse to low temperature Int J Agric Biol 18 346ndash352doi1017957IJAB150093

Linde M Diel S and Neuffer B 2001 Flowering ecotypes ofCapsella bursa-pastoris (L) Medik(Brassicaceae) analysed by acosegregation of phenotypic characters (QTL) and molecularmarkers Annals of Botany 87(1) 91ndash99 doi101006anbo20001308

Lipecki J 1989 Capsella bursa-pastoris (L) Med another weedresistant to simazine Acta Soc Bot Pol 57 187ndash189doi105586asbp1988018

Liu Y Lin L Jin Q and Zhu X 2015 Cadmium accumulationand tolerance in the Cd-accumulator Capsella bursa-pastorisEnviron Prog Sustain Energy 34 663ndash668 doi101002ep12037

Marshall EJP Brown VK Boatman ND Lutman PJWSquire GR and Ward LK 2003 The role of weeds in sup-porting biological diversity within crop fields Weed Res43 77ndash89 doi101046j1365-3180200300326x

Martin SL Sauder CA James T Cheung KW Razeq FMKron P and Hall L 2015 Sexual hybridization betweenCapsella bursa-pastoris (L) medik () and Camelina sativa (L)crantz () (Brassicaceae) Plant Breed 134 212ndash220doi101111pbr12245

Mazzio EA and Soliman KFA 2009 In vitro screening forthe tumoricidal properties of international medicinalplants Phytother Res 23 385ndash398 doi101002ptr2636PMID18844256

McKenzie RA Carmichael AM Schibrowski ML DuiganSA Gibson JA and Taylor JD 2009 Sulfur-associatedpolioencephalomalacia in cattle grazing plants from theFamily Brassicaceae Aust Vet J 87 27ndash32

Medve RJ 1983 The mycorrhizal status of the Cruciferae AmMidl Nat 109 406ndash408 doi1023072425422

Mennan H Ngouajio M Kaya E and Isik D 2009 Weed man-agement in organically grown kale using alternative cover

cropping systems Weed Technol 23 81ndash88 doi101614WT-08-1191

Milberg P and Hallgren E 2004 Yield loss due to weeds incereals and its large-scale variability in Sweden Field CropsRes 86 199ndash209 doi101016jfcr200308006

Millspaugh CF 1974 American Medicinal Plants DoverPublications New York

Mirzaee MR and Sajedi S 2015 First confirmed report ofwhite blister rust disease caused by Albugo candida onCapsella bursa-pastoris in Iran J Plant Pathol 97 S71

Monzeglio U and Stoll P 2005 Spatial patterns and speciesperformances in experimental plant communitiesOecologia 145 619ndash628 doi101007s00442-005-0168-3PMID16001215

Moreau D Gibot-Leclerc S Girardin A Pointurier O ReibelC Strbik F et al 2016 Trophic relationships between theparasitic plant species Phelipanche ramosa (L) and differenthosts depending on host phenological stage and host growthrate Front Plant Sci 7 1033 doi103389fpls201601033PMID27468293

Morgan OD 1971 A study of four weed hosts of Sclerotinia spe-cies in alfalfa fields Plant Disease Reporter 55 1097ndash1089

Moser BR and Vaughn SF 2012 Efficacy of fatty acid profileas a tool for screening feedstocks for biodiesel productionBiomass Bioenerg 37 31ndash41 doi101016jbiombioe201112038

Mostafa AM Lowery DT Jensen LBM and Deglow EK2011 Host plant suitability and feeding preferences of thegrapevine pest Abagrotis orbis (Lepidoptera Noctuidae)Environ Entomol 40 1458ndash1464 doi101603EN11049PMID22217761

Mouhanna AM Langen G and Schlosser E 2008 Weeds asalternative hosts for BSBV BNYVV and the vector Polymyxabetae (German isolate) J Plant Dis Prot 115 193ndash198doi101007BF03356263

Mukherjee DK Kiewitt I and Hurka H 1984 Lipid contentand fatty acid composition of seeds of Capsella species fromdifferent geographical locations Phytochemistry 23117ndash119 doi1010160031-9422(84)83088-5

Muller FJ Dosdall LM Mason PG and Kuhlmann U 2011Larval phenologies and parasitoids of two seed-feedingweevils associated with hoary cress and shepherdrsquos purse(Brassicaceae) in Europe Can Entomol 143 399ndash410doi104039n11-020

Mulligan GA 1957 Chromosome numbers of Canadian weedsI Can J Bot 35 779ndash789 doi101139b57-064

Mulligan GA 1984 Chromosome numbers of some plantsnative and naturalized in Canada and Alaska Nat Can 111447ndash449

Munyaneza JE Crosslin JM and Upton JE 2006 Beet leaf-hopper (Hemiptera Cicadellidae) transmits the ColumbiaBasin potato purple top phytoplasma to potatoes beetsand weeds J Econ Entomol 99 268ndash272 doi101093jee992268 PMID16686123

Neuffer B 1990 Ecotype differentiation in Capsella Vegetatio89 165ndash171 doi101007BF00032168

Neuffer B 2011 Native range variation in Capsella bursa-pastoris(Brassicaceae) along a 2500 km latitudinal transect Flora206 107ndash119 doi101016jflora201003001

Neuffer B and Albers S 1996 Phenotypic and allozyme variabil-ity in Capsella populations with different ploidy levels fromdifferent continents Bot Jahrb Syst Pflanzengesch 118433ndash450

Neuffer B and Bartelheim S 1989 Gen-ecology of Capsella bursa-pastoris from an altitudinal transsect in the Alps Oecologia 81521ndash527 doi101007BF00378963 PMID28312648

Ahmed et al 549



Neuffer B and Eschner S 1995 Life history traits and ploidylevels in the genus Capsella (Brassicaceae) Can J Bot 731354ndash1365 doi101139b95-147

Neuffer B and Hoffrogge R 2000 Ecotypic and allozymevariation of Capsella (Brassicaceae) along an altitudinalgradient on the Iberian Peninsula An Jard Bot Madr 57299ndash315

Neuffer B and Hurka H 1986a Variation of development timeuntil flowering in natural populations of Capsella bursa-pastoris (Cruciferae) Plant Syst Evol 152 277ndash296doi101007BF00989433

Neuffer B and Hurka H 1986b Variation of growth formparameters in Capsella (Cruciferae) Plant Syst Evol 153265ndash279 doi101007BF00983693

Neuffer B and Hurka H 1988 Germination behaviour inpopulations of Capsella bursa-pastoris (Cruciferae) Plant SystEvol 161 35ndash47 doi101007BF00936010

Neuffer B and Hurka H 1999 Colonization history and intro-duction dynamics of Capsella bursa-pastoris (Brassicaceae) inNorth America Isozymes and quantitative traits Mol Ecol 81667ndash1681 doi101046j1365-294x199900752x PMID10583830

Neuffer B and Meyer-Walf M 1996 Ecotypic variation in rela-tion to man made habitats in Capsella Field and tramplingarea Flora 191 49ndash57 doi101016S0367-2530(17)30689-8

Neuffer B and Paetsch M 2013 Flower morphology and pol-len germination in the genus Capsella (Brassicaceae) Flora208 626ndash640 doi101016jflora201309007

Neuffer B Bernhardt KG Hurka H and Kropf M 2011Monitoring population and gene pool dynamics of theannual species Capsella bursa-pastoris (Brassicaceae) A reviewof relevant species traits and the initiation of a long-termgenetic monitoring programme Biodivers Conserv 20309ndash323 doi101007s10531-010-9957-z

Neuffer B Wesse C Voss I and Scheibe R 2018 The role ofecotypic variation in driving worldwide colonization by acosmopolitan plant AoB Plants 10(1) pply005 doi101093aobplaply005

Neuffer B Schorsch M Hameister S Knuesting J SelinskiJ and Scheibe R 2020 Physiological and anatomical differ-entiation of two sympatric weed populations Peer J 8e9226 doi107717peerj9226 PMID32587795

Niu Y-Q Sun Y-X and Liu T-X 2014 Development andreproductive potential of diamondback moth (LepidopteraPlutellidae) on selected wild crucifer species EnvironEntomol 43 69ndash74 doi101603EN13206 PMID24367918

Noordam D 2004 Aphids of Java Part V Aphidini (HomopteraAphididae) Zool Verh 346 7ndash83

The Noxious Weeds Act CCSM c N110 2010 [Online] Availablefrom httpscanliicat53n16 [14 July 2021]

Nutt P Ziermann J Hintz M Neuffer B and Theiszligen G2006 Capsella as a model system to study the evolutionaryrelevance of floral homeotic mutants Plant Syst Evol 259217ndash235 doi101007s00606-006-0420-2

OrsquoHayer KW Schultz GA Eastman CE and Fletcher J1984 Newly-discovered plant hosts of Spiroplasma citri PlantDis 68 336ndash338

Ontario Ministry of Agriculture Food and Rural Affairs[OMAFRA] 2020 Guide to Weed Control Publication 75Toronto 396 p

Opiz PM 1821 2 Capsella apetala Opiz Eine neue merkwuumlrdigePflanze Flora Nr 28 oder Botanische Zeitung Regensburg[28 Juli 1821]

Orsucci M Milesi P Hansen J Girodolle J Gleacutemin S andLascoux M 2020 Shift in ecological strategy helps marginalpopulations of shepherdrsquos purse (Capsella bursa-pastoris) toovercome a high genetic load Proc R Soc B 287(1927)20200463 doi101098rspb20200463 PMID32429810

Pehlivan M Akguumll H and Yayla F 2013 Some nutrient andtrace elements content of wild plants using as ethno botani-cal and grown in the Gazientep region J Appl Pharm Sci3 143ndash145

Perera KK and Ayres PG 1992 Effects of shepherdrsquos purse(Capsella bursa-pastoris L Medic) on the growth of radish(Raphanus sativus L) Weed Res 32 329ndash335 doi101111j1365-31801992tb01893x

Perez-Jones A Intanon S and Mallory-Smith C 2009Molecular analysis of hexazinone-resistant shepherdrsquos-purse(Capsella bursa-pastoris) reveals a novel psbA mutation WeedSci 57 574ndash578 doi101614WS-09-0891

Petkowski JE Cunnington JH Minchinton EJ and CahillDM 2010 Molecular phylogenetic relationships betweenAlbugo candida collections on the Brassicaceae in AustraliaPlant Pathol 59 282ndash288 Jen doi101111j1365-3059200902204x

Petrie GA Seacuteguin-Swartz G and Gugel RK 1995 Latentinfection of Brassicaceae in the field by Leptosphaeria maculans(Blackleg) Can J Plant Pathol 17 75ndash81

Pigott CD Ratcliffe DA Malloch AJC Birks HJB ProctorMCF Shimwell DW et al 2000 British PlantCommunities Pages 370ndash373 in J S Rodwell ed MaritimeCommunities and Vegetation of Open Habitats Vol 5Cambridge University Press Cambridge doi101017CBO9780511541834

Popay AI and Roberts EH 1970a Factors involved in the dor-mancy and germination of Capsella bursa-pastoris (L) Medikand Senecio vulgaris L J Ecol 58 103ndash122 doi1023072258171

Popay AI and Roberts EH 1970b Ecology of Capsella bursa-pastoris (L) Medik and Senecio vulgaris L in relation to germi-nation behavior J Ecol 58 123ndash139 doi1023072258172

Poudel B Wintermantel WM Cortez AA Ho T Khadgi Aand Tzanetakis IE 2013 Epidemiology of blackberry yellowvein associated virus Plant Dis 97 1352ndash1357 doi101094PDIS-01-13-0018-RE PMID30722181

Qiao H Liu F Luo J Lai F-X Wang H-D and Dai D-J2009 Fitness of the small brown planthopper (Laodelphaxstriatellus) on different plants Zhongguo Shuidao Kexue 2371ndash78

Radisek S Jakse J Zhao TT Cho SE and Shin HD 2018First report of powdery mildew of Capsella bursa-pastoriscaused by Golovinomyces orontii in Slovenia J Plant Pathol100 359 doi101007s42161-018-0071-5

Rasochovaacute L Passmore BK Falk BW and Miller WA 1997The satellite RNA of barley yellow dwarf virus-RPV issupported by beet western yellows virus in dicotyledonousprotoplasts and plants Virology 231 182ndash191 doi101006viro19978532 PMID9168880

Rayia A Abu Ziada ME and Al-Halboosi SR 2020Autecology and Economic Importance of Weed Flora of theNile Delta Capsella bursandashpastoris L J Plant Prod 11(1) 49ndash56

Rees M and Brown VK 1992 Interactions between inverte-brate herbivores and plant competition J Ecol 80353ndash360 doi1023072261017

Ren L Fang XP Sun CC Chen KR Liu F Li M and XuL 2014 First report of clubroot on Capsella bursa-pastoriscaused by Plasmodiophora brassicae in Sichuan province ofChina Plant Dis 98 687 doi101094PDIS-04-13-0395-PDNPMID30708514

Rezvani M Zaefarian F and Amini V 2014 Effects of chemi-cal treatments and environmental factors on seed dormancyand germination of shepherdrsquos purse (Capsella bursa-pastoris(L) Medic) Acta Bot Brasilica 28 495ndash501 doi1015900102-33062014abb3337

Roberts HA and Feast PM 1973 Emergence and longevity ofseeds of annual weeds in cultivated and undisturbed soil JAppl Ecol 10 133ndash143 doi1023072404721




Roberts HR Warren JM and Provan J 2018 Evidence forfacultative protocarnivory in Capsella bursa-pastoris seedsSci Rep 8 10120ndash10125 doi101038s41598-018-28564-xPMID29973685

Rousseau C 1968 Histoire habitat et distribution de 220plantes introduites au Queacutebec Nat Can 95 49ndash171

Royer F and Dickinson R 1999 Weeds of Canada and theNorthern United States A guide for identificationEdmonton Lone Pine Publishing 270 p

Sagun VG and Auer C 2017 Pollen morphology of selectedCamelineae (Brassicaceae) Palynology 41 255ndash266doi1010800191612220161163517

Sanderson MA Stout R Goslee S Gonet J and Smith RG2014 Soil seed bank community structure of pastures andhayfields on an organic farm Can J Plant Sci 94 621ndash631doi104141cjps2013-288

Sanger M Passmore B Falk BW Bruening G Ding B andLucas WJ 1994 Symptom severity of beet western yellowvirus strain ST9 is conferred by the ST9-associated RNA andis not associated with virus release from the phloemVirology 200 48ndash55 doi101006viro19941161 PMID8128637

Sanguankeo PP and Leon RG 2011 Weed management prac-tices determine plant and arthropod diversity and seed pre-dation in vineyards Weed Res 51 404ndash412 doi101111j1365-3180201100853x

Sansome E and Sansome FW 1974 Cytology and life-historyof Peronospora parasitica on Capsella bursa-pastoris and ofAlbugo candida on C bursa-pastoris and on Lunaria annuaTrans Br Mycol Soc 62 323ndashIN24 doi101016S0007-1536(74)80041-0

Sarfraz RM Dosdall LM Keddie BA and Myers JH 2011Larval survival host plant preferences and developmentalresponses of the diamondback moth Plutella xylostella(Lepidoptera Plutellidae) on wild brassicaceous speciesEntomol Sci 14 20ndash30 doi101111j1479-8298201000413x

Sarfraz RM Dosdall LM and Keddie BA 2012 Influence ofthe herbivore hostrsquos wild food plants on parasitism survivaland development of the parasitoid Diadegma insulare BiolControl 62 38ndash44 doi101016jbiocontrol201203004

Sasakawa K 2011 Laboratory studies on larval food habits oftwo syntopic related graniverous grounds beetles Amarachalcites and A congrua (Coleoptera Carabidae) a comparisonwith stable isotope analysis Appl Entomol Zool 46 511ndash518doi101007s13355-011-0070-x

Saska P 2008a Effect of diet on the fecundity of three carabidbeetles Physiol Entomol 33 188ndash192 doi101111j1365-3032200800618x

Saska P 2008b Granivory in terrestrial isopods Ecol Entomol33 742ndash747

Saska P Koprdova S Martinkova Z and Honěk A 2014Comparing methods of weed seed exposure to predatorsAnn Appl Biol 164 301ndash312 doi101111aab12102

Saskatchewan Guide to Crop Protection 2020 Guide to CropProtection For the chemical management of weedplant diseases and insects Saskatchewan Ministry ofAgriculture [Online] Available from httpswwwsaskatchewancabusinessagriculture-natural-resources-and-industryagribusiness-farmers-and-rancherscrops-and-irrigationcrop-guides-and-publicationsguide-to-crop-protection [10 Jul 2021]

Savchuk YI 2012 Herbicide activity of some micromycetesMikrobiol Zh 74 43ndash48

Schultze-Motel W 1986 Capsella Pages 346ndash356 in Illustrierteflora von Mittel-europa G Hegi ed 3rd ed Vol 4 VerlagPaul Peray Berlin Hamburg Germany [in German]

Seal AN Pratley JE Haig TJ An M and Wu H 2009Phytotoxic potential of shepherdrsquos purse on annual ryegrassand wild radish Allelopathy J 24 55ndash66

Seacuteguin-Swartz G Nettleton J Sauder C Warwick SI andGugel RK 2011 Hybridization potential between the oilseedcrucifer Camelina sativa and canola mustard and relatedweeds Proc 13th Internat Rapeseed Congress 5ndash9 June2011 Prague pp 716ndash718

Semal J 1956 Transmission of beet mosaic virus from Stellariamedia and Capsella bursa-pastoris by Myzus ascalonicusDoncaster Nature 178 501ndash502 doi101038178501a0

Shapland EB Daane KM Yokota GY Wistrom C ConnellJJ Duncan RA and Viveros MA 2006 Ground vegetationsurvey for Xylella fastidiosa in California almond orchardsPlant Dis 90 905ndash909 doi101094PD-90-0905

Shrestha A Mitchell JP and Hembree KJ 2015 Weed seed-bank characterization in long-term cottonndashtomato rotationsin California Agron J 107 597ndash604 doi102134agronj140443

Shull GH 1909 Bursa bursa-pastoris and Bursa heegeri biotypesand hybrids Carnegie Institution Publications No 112Washington DC 57 pp

Shull GH 1929 Species hybridization among old and newspecies of shepherdrsquos purse Proc Int Cong Plant Sci 1837ndash888

Sigareva MA and Earle ED 1999 Regeneration of plantsfrom protoplasts of Capsella bursa-pastoris and somatichybridization with rapid cycling Brassica oleracea Plant CellRep 18 412ndash417 doi101007s002990050595

Sikkema PH Soltani N and Robinson DE 2007 Responsesof cole crops to pre-transplant herbicides Crop Prot 261173ndash1177 doi101016jcropro200610013

Simmonds H Holst P and Bourke C 2000 The palatabilityand potential toxicity of Australian weeds to goats RuralIndustries Research and Development CorporationKingston Australia166 pp

Singh SP Kumar S Singh YP and Singh R 2014 Reliablescreening technique for evaluation of wild crucifers againstmustard aphid Lipaphis erysimi (Kalt) Indian J Exp Biol 521201ndash1205 PMID25651614

Sivesind EC Leblanc MI Cloutier DC Seguin P andStewart KA 2009 Weed response to flame weeding at differ-ent developmental stages Weed Technol 23 438ndash443doi101614WT-08-1551

Skuhrava M 2011 A new genus and eight new species of gallmidges (Diptera Cecidomyiidae) from Greece Acta SocZool Bohemicae 75 265ndash295

Slotte T Holm K McIntyre LM Ulf L and Lascoux M 2007Differential expression of genes important for adaptationin Capsella bursa-pastoris (Brassicaceae) Plant Physiol 145160ndash173 doi101104pp107102632 PMID17631524

Smith EA DiTommaso A Fuchs M Shelton AM andNault BA 2012 Abundance of weed hosts as potentialsources of onion and potato viruses in western New YorkCrop Protect 37 91ndash96 doi101016jcropro201202007

Snodgrass GL Scott WP Abel CA Robbins JT Gore Jand Hardee DD 2006 Suppression of tarnished plant bugs(Heteroptera Miridae) in cotton by control of early seasonwild host plants with herbicides Environ Entomol 351417ndash1422 doi101093ee3551417

Soylu S Keshavarzi M Brown I and Mansfield JW 2003Ultrastructural characterisation of interactions betweenArabidopsis thaliana and Albugo candida Physiol Mol PlantPath 63 201ndash211 doi101016jpmpp200312002

Stace C 1997 New flora of the British Isles 2 ed CambridgeUniversity Press 1130 pp

Stephan D and Maiss E 2006 Biological properties of Beet mildyellowing virus derived from a full-length cDNA clone J GenVirol 87 445ndash449 doi101099vir081565-0 PMID16432033

Stevens M Smith HG and Hallsworth PB 1994 The hostrange of beet yellowing viruses among common arable weed

Ahmed et al 551



species Plant Pathol 43 579ndash588 doi101111j1365-30591994tb01593x

Stevens M Patron NJ Dolby CA Weekes R HallsworthPB Lemaire O and Smith HG 2005 Distribution andproperties of geographically distinct isolates of sugar beetyellowing viruses Plant Pathol 54 100ndash107 doi101111j1365-3059200501155x

Storkey J and Westbury DB 2007 Managing arable weeds forbiodiversity Pest Manag Sci 63 517ndash523 doi101002ps1375PMID17437252

Stoyanov K 2005 Floristic materials and critical notes on thegenus Orobanche subgen Phelipanche in Bulgaria Fl Medit15 461ndash476

Swarbrick JT 1971 External mucilage production by the seedsof British plants J Linn Soc Bot 64 157ndash162 doi101111j1095-83391971tb02142x

Taylor RL and Mulligan GA 1968 Flora of the QueenCharlotte Islands part 2 cytological aspects of the vascularplants Queenrsquos Printer Ottawa ON 148 pp

Toorop PE Cuerva RC Begg GS Locardi B Squire GRand Iannetta PPM 2012 Co-adaptation of seed dormancyand flowering time in the arable weed Capsella bursa-pastoris(shepherdrsquos purse) Ann Bot 109 481ndash489 doi101093aobmcr301 PMID22147546

United States Department of Agriculture 1960 Index of plantdiseases in the United States USDA Agricultural Handbook165 1ndash531

Urquhart EJ Sun LJ and Punja ZK 1997 Identification ofspecies of Tilletiopsis using random amplified polymorphicDNA analyses Can J Plant Pathol 19 380ndash389 doi10108007060669709501064

Van Acker RC and Cici SZH 2012 Timing of stinkweed andshepherdrsquos-purse recruitment affects biological characteris-tics of progeny Can J Plant Sci 92 933ndash936 doi104141cjps2012-024

Vallad GE Bhat RG Koike ST Ryder EJ and SubbaraoKV 2005 Weedborne reservoirs and seed transmissionof Verticillium dahlia in lettuce Plant Dis 89 317ndash324doi101094PD-89-0317 PMID30795356

Venkatesh R Harrison SK and Riedel RM 2000 Weed hostsof soybean nematode (Heterodera glicines) in Ohio WeedTechnol 14 156ndash160 doi1016140890-037X(2000)014[0156WHOSCN]20CO2

Wang G-Q Cui H-l Zhang H-J Zhang Y-Q Liu X Li X-Jand Fan C-Q 2011 Tribenuron-methyl resistant shepherdrsquospurse (Capsella bursa-pastoris(L) Medik) in Hebei province ofChina Agr Sci China 10 1241ndash1245 doi101016S1671-2927(11)60115-6

Wani MA Jan N Qazi HA Andrabi KI and John R 2018Cold stress induces biochemical changes fatty acid profileantioxidant system and gene expression in Capsella bursa pas-toris L Acta Physiol Plant 40 1ndash14

Wei YJ 2008 Studies of life history and some aspects of fieldbiology and ecology of Nysius huttoni White (HemipteraLygaeidae) J R Soc N Z 38149ndash162 doi10108003014220809510552

Welbank PJ 1963 A comparison of competitive effects of somecommon weed species Ann Appl Biol 51 107ndash125doi101111j1744-73481963tb03679x

Werle R Bernards ML Arkebauer TJ and Lindquist JL2014 Environmental triggers of winter annual weed

emergence in the midwestern United States Weed Sci 6283ndash96 doi101614WS-D-13-000911

Wesse C Welk E Hurka H and Neuffer B 2021Geographical pattern of genetic diversity in Capsella bursa-pastoris (Brassicaceae)mdashA global perspective Ecol Evol 11199ndash213 doi101002ece37010 PMID33437423

Wiese WJ and Joubert JPJ 2001 Capsella bursa-pastorisNitrate poisoning and pigs J S Afr Vet Assoc 72 170ndash171doi104102jsavav72i3644 PMID11811708

Wiklund C and Friberg M 2009 The evolutionary ecology ofgeneralization among-year variation in host plant use andoffspring survival in a butterfly Ecology 90 3406ndash3417doi10189008-11381 PMID20120809

Wilson RG and Orloff SB 2008 Winter annual weed controlwith herbicides in alfalfa-orchardgrass mixtures WeedTechnol 22 30ndash33 doi101614WT-07-0701

Williams L III and Hendrix DL 2008 Comparing differentfloral resources on the longevity of a parasitic wasp AgricForest Entomol 10 23ndash28 doi101111j1461-9563200700355x

Yang W 2018 Effect of nitrogen phosphorus and potassiumfertilizer on growth and seed germination of Capsella bursa-pastoris (L) Medikus J Plant Nutr 41 636ndash644 doi1010800190416720171415350

Zennie TM and Ogzewalla D 1977 Ascorbic acid and VitaminA content of edible wild plants of Ohio and Kentucky EconBot 31 76ndash79 doi101007BF02860657

Žerdoner Čalasan A Seregin AP Hurka H Hofford NPand Neuffer B 2019 The Eurasian steppe belt in time andspace phylogeny and historical biogeography of the falseflax (Camelina Crantz Camelineae Brassicaceae) Flora 260151477 doi101016jflora2019151477

Žerdoner Čalasan A Hurka H German DA Pfanzelt SBlattner FR Seidl A and Neuffer B 2021 Pleistocenedynamics of the Eurasian steppe as a driving force ofevolution Phylogenetic history of the genus Capsella(Brassicaceae) Ecol Evol 00 1ndash17 httpsdoiorg101002ece38015

Zhang CJ and Auer C 2020 Hybridization between Camelinasativa (L) Crantz and common Brassica weeds Ind CropsProd 147 112240 doi101016jindcrop2020112240

Zhang L Li W Guo W Wu C Wang H Liu W and WangJ 2017 Herbicides cross resistance of a tribenuron-methylresistant Capsella bursa-pastoris (L) Medik population inwheat field Chil J of Agric Res 77 65ndash70 doi104067S0718-58392017000100008

Zhao Y Damicone JP and Bender CL 2002 Detection sur-vival and sources of inoculum for bacterial diseases of leafycrucifers in Oklahoma Plant Dis 86 883ndash888 doi101094PDIS2002868883 PMID30818643

Zhou TY Lu LL Yang G and Al-Shehbaz IA 2001Brassicaceae (Cruciferae) Pages 1ndash193 in ZY Wu and PHRaven eds Flora of China 8 Science PressMissouriBotanical Garden Press BeijingSt Louis

Ziermann J Ritz MS Hameister S Abel C Hoffmann MHNeuffer B and Theiszligen G 2009 Floral visitation and repro-ductive traits of stamenoid petals a naturally occurring flo-ral homeotic variant of Capsella bursa-pastoris (Brassicaceae)Planta 230 1239ndash1249 doi101007s00425-009-1018-zPMID19784670




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ARTICLE

The Biology of Canadian Weeds 159 Capsella bursa-pastoris (L)MedikHafsa T Ahmed Ardath Francis David R Clements Elyse Dyck Natalie RossMahesh K Upadhyaya Linda M Hall and Sara L Martin

Abstract Capsella bursa-pastoris (L) Medik shepherdrsquos purse is a cosmopolitan summer or winter annual weedspecies distributed throughout temperate and subtropical regions of the world and is considered one of the mostcommon plants on earth It is an opportunistic annual that colonizes newly disturbed open or dry environmentsand is ubiquitous in cultivated lands in Canada In annual crops in western Canada C bursa-pastoris has beenamong the 20 most abundant weeds since the first weed surveys in 1970 It is most easily distinguished by its smallwhite four-petalled flowers and its heart-shaped seed-pods but exhibits considerable variation in leaf shape andflowering time It has been used for food and medicine by numerous cultures Its golden-brown seeds areproduced in large numbers predominantly through self-pollination and can form a substantial seed bank withreported values ranging to several hundred thousand seeds mminus2 While seeds usually disperse near the motherplant long-distance dispersal by attaching to vehicles people and other vectors may be facilitated by its mucilagi-nous coat Capsella bursa-pastoris does not produce fertile hybrids with other species of economic or ecologicalsignificance It is generally well controlled by soil-applied and foliar (post-emergence) herbicides although itspresence in agricultural fields may result in substantial yield loss as documented in cole crops in North Americaand grain crops in Europe The species can host a wide range of insect nematode fungal viral and bacterial peststhat may damage crop species

Key words Capsella bursa-pastoris shepherdrsquos purse cole crops weed dispersal

Reacutesumeacute La bourse-agrave-pasteur [Capsella bursa-pastoris (L) Medik] est une adventice annuelle cosmopolite qursquoon ren-contre lrsquoeacuteteacute ou lrsquohiver dans toutes les reacutegions agrave climat tempeacutereacute ou subtropical du globe On estime qursquoil srsquoagit drsquounedes plantes les plus courantes sur la Terre Opportuniste lrsquoannuelle colonise les endroits deacutegageacutes ou aridesreacutecemment perturbeacutes et on la recense sur toutes les terres cultiveacutees au Canada C bursa-pastoris figure parmi lesvingt adventices les plus abondantes dans les cultures annuelles canadiennes depuis qursquoon a commenceacute agravereacutepertorier les mauvaises herbes en 1970 La plante se reconnaicirct aiseacutement en raison de ses petites fleurs agrave quatrepeacutetales et de ses gousses en cœur mais la forme des feuilles et la peacuteriode de floraison varient consideacuterablementBeaucoup drsquoethnies lrsquoutilisent comme plante vivriegravere ou meacutedicinale Les graines brun doreacute sont produites engrand nombre principalement par autopollinisation et peuvent constituer une importante reacuteserve susceptibledrsquoatteindre selon certains auteurs plusieurs centaines de milliers par megravetre carreacute Bien qursquoelles demeurent le plussouvent agrave proximiteacute du plant megravere les graines peuvent se disperser sur de longues distances en adheacuterant auxveacutehicules aux gens ou agrave drsquoautres vecteurs gracircce agrave leurs teacuteguments mucilagineux Capsella bursa-pastoris nrsquoengendrepas drsquohybrides fertiles avec drsquoautres espegraveces drsquoimportance eacuteconomique ou eacutecologique Lrsquoapplication drsquoherbicide ausol ou aux feuilles (apregraves la leveacutee) est geacuteneacuteralement efficace mais la preacutesence de cette mauvaise herbe sur les terresagricoles peut donner lieu agrave drsquoimportantes pertes de rendement comme on lrsquoa observeacute dans les champs decrucifegraveres en Ameacuterique du Nord et ceux de ceacutereacuteales en Europe Lrsquoespegravece heacuteberge une grande varieacuteteacute drsquoinsectes

Received 6 March 2021 Accepted 8 October 2021

HT Ahmed and MK Upadhyaya Faculty of Land and Food Systems University of British Columbia Vancouver BC V6T 1Z4 Canada

A Francis and SL Martin Agriculture and Agri-Food Canada Ottawa Research and Development Centre Ottawa ON K1A 0C6 Canada

DR Clements E Dyck and N Ross Department of Biology Trinity Western University Langley BC V2Y 1Y1 Canada

LM Hall Agricultural Food amp Nutritional Science University of Alberta Edmonton AB T6G 2R3 Canada

Corresponding author David Clements (email clementstwuca)

copy 2021 Authors HT Ahmed DR Clements E Dyck N Ross MK Upadhyaya and LM Hall and her Majesty the Queen in Rightof Canada as represented by the Minister of Agriculture and Agri-Food Canada This work is licensed under a Creative CommonsAttribution 40 International License (CC BY 40) which permits unrestricted use distribution and reproduction in any mediumprovided the original author(s) and source are credited

529

Can J Plant Sci 102 529ndash552 (2022) dxdoiorg101139cjps-2021-0059 Published at wwwcdnsciencepubcomcjps on 5 November 2021






















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Ahmed et al 539

























Hymenoptera


Thysanoptera


Coleoptera


Ahmed et al 541




Hemiptera



Diptera









Black leg


Club root


Leaf curl and wilt


Leaf spot


Mildews


Moulds



Root rot


Rusts


Ahmed et al 543




Stem disease









































Ahmed et al 545















































































Ahmed et al 547











































































Ahmed et al 549















































































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Ahmed et al 531




























Ahmed et al 533






















Ahmed et al 535


























Ahmed et al 537

























Ahmed et al 539

























Hymenoptera


Thysanoptera


Coleoptera


Ahmed et al 541




Hemiptera



Diptera









Black leg


Club root


Leaf curl and wilt


Leaf spot


Mildews


Moulds



Root rot


Rusts


Ahmed et al 543




Stem disease









































Ahmed et al 545















































































Ahmed et al 547











































































Ahmed et al 549















































































Ahmed et al 551
































































Ahmed et al 533






















Ahmed et al 535


























Ahmed et al 537

























Ahmed et al 539

























Hymenoptera


Thysanoptera


Coleoptera


Ahmed et al 541




Hemiptera



Diptera









Black leg


Club root


Leaf curl and wilt


Leaf spot


Mildews


Moulds



Root rot


Rusts


Ahmed et al 543




Stem disease









































Ahmed et al 545















































































Ahmed et al 547











































































Ahmed et al 549















































































Ahmed et al 551


























































Ahmed et al 535


























Ahmed et al 537

























Ahmed et al 539

























Hymenoptera


Thysanoptera


Coleoptera


Ahmed et al 541




Hemiptera



Diptera









Black leg


Club root


Leaf curl and wilt


Leaf spot


Mildews


Moulds



Root rot


Rusts


Ahmed et al 543




Stem disease









































Ahmed et al 545















































































Ahmed et al 547











































































Ahmed et al 549















































































Ahmed et al 551






























































Ahmed et al 537

























Ahmed et al 539

























Hymenoptera


Thysanoptera


Coleoptera


Ahmed et al 541




Hemiptera



Diptera









Black leg


Club root


Leaf curl and wilt


Leaf spot


Mildews


Moulds



Root rot


Rusts


Ahmed et al 543




Stem disease









































Ahmed et al 545















































































Ahmed et al 547











































































Ahmed et al 549















































































Ahmed et al 551





























































Ahmed et al 539

























Hymenoptera


Thysanoptera


Coleoptera


Ahmed et al 541




Hemiptera



Diptera









Black leg


Club root


Leaf curl and wilt


Leaf spot


Mildews


Moulds



Root rot


Rusts


Ahmed et al 543




Stem disease









































Ahmed et al 545















































































Ahmed et al 547











































































Ahmed et al 549















































































Ahmed et al 551





























































Hymenoptera


Thysanoptera


Coleoptera


Ahmed et al 541




Hemiptera



Diptera









Black leg


Club root


Leaf curl and wilt


Leaf spot


Mildews


Moulds



Root rot


Rusts


Ahmed et al 543




Stem disease









































Ahmed et al 545















































































Ahmed et al 547











































































Ahmed et al 549















































































Ahmed et al 551








































Hemiptera



Diptera









Black leg


Club root


Leaf curl and wilt


Leaf spot


Mildews


Moulds



Root rot


Rusts


Ahmed et al 543




Stem disease









































Ahmed et al 545















































































Ahmed et al 547











































































Ahmed et al 549















































































Ahmed et al 551







































Black leg


Club root


Leaf curl and wilt


Leaf spot


Mildews


Moulds



Root rot


Rusts


Ahmed et al 543




Stem disease









































Ahmed et al 545















































































Ahmed et al 547











































































Ahmed et al 549















































































Ahmed et al 551








































Stem disease









































Ahmed et al 545















































































Ahmed et al 547











































































Ahmed et al 549















































































Ahmed et al 551






































































Ahmed et al 545















































































Ahmed et al 547











































































Ahmed et al 549















































































Ahmed et al 551



















































































































Ahmed et al 547











































































Ahmed et al 549















































































Ahmed et al 551















































































































Ahmed et al 549















































































Ahmed et al 551



















































































































Ahmed et al 551







































The Biology of Canadian Weeds. 159. Capsella bursa - BioOne

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Transcript of The Biology of Canadian Weeds. 159. Capsella bursa - BioOne