The Biology of Canadian Weeds. 146. communis L.

Ardath Francis1, Stephen J. Darbyshire1, David R. Clements2, and Antonio DiTommaso3

1Agriculture and Agri-Food Canada, Eastern Cereal and Oilseed Research Centre, Wm. Saunders Bldg. #49, Ottawa, Ontario, Canada KIA 0C6 (e-mail: [email protected]); 2Biology Department, Trinity Western University, 7600 Glover Road, Langley, British Columbia, Canada V2Y 1Y1; and 3Department of Crop and Soil Sciences, 903 Bradfield Hall, Cornell University, Ithaca, NY 14853 USA. Received 17 August 2010, accepted 20 December 2010.

Francis, A., Darbyshire, S. J., Clements, D. R. and DiTommaso, A. 2011. The Biology of Canadian Weeds. 146. L. Can. J. Sci. 91: 553569. Nipplewort, Lapsana communis, is an annual weed of the native to and western , first detected in northeastern and Pacific northwestern regions of in the 19th century. It appears to have been introduced as a contaminant of imported garden material and seeds, but may also have been deliberately introduced as a medicinal herb. After a century of remaining close to its original points of introduction in gardens and ruderal habitats, it spread to neighbouring areas, and now occurs across southern Canada and in many areas of the United States. Possible reasons for this range expansion include forest clearance and changing crop management practices as was observed in Europe, where this plant has become an important weed in grain, forage and vegetable crops. In Ontario, L. communis has recently emerged as a weed in wheat (Triticum aestivum), corn (Zea mays) and soybean (Glycine max) fields. Various herbicides have been effective on L. communis in corn, but control has been less effective in winter wheat, where the herbicides MCPA and 2,4-D used alone have provided little or no control. Control in soybean has yet to be assessed. In Europe both mechanical methods and herbicides have been effective in controlling the weed, but L. communis has recently developed tolerance to MCPA. It is unclear whether this weed will continue to spread or will remain a localized or relatively minor crop pest in Canada.

Key words: Lapsana communis, lapsane commune, nipplewort, LAPCO, weed biology

Francis, A., Darbyshire, S. J., Clements, D. R. et DiTommaso, A. 2011. La biologie des mauvaises herbes au Canada. 146. Lapsana communis L. Can. J. Plant Sci. 91: 553569. La lapsane commune, Lapsana communis, est une annuelle de la famille des Aste´ race´ es indige` ne en Europe et dans l’ouest de l’Asie. En Ame´ rique du Nord, la plante a e´ te´ identifie´ e pour la premie` re fois dans le nord-est et dans la partie nord-ouest du Pacifique au XIXe sie` ce. Elle semble avoir e´ te´ introduite comme contaminant avec le mate´ riel de jardinage ou des graines, mais il se peut aussi qu’on l’ait de´ libe´ re´ ment apporte´ e comme herbe me´ dicinale. Apre` seˆ tre reste´ e pre` s d’un sie` cle a` proximite´ des points d’introduction originaux, dans les jardins For personal use only. et les habitats rude´ raux, la plante s’est e´ tendue aux re´ gions voisines, si bien qu’on la retrouve maintenant partout dans le sud du Canada et dans maintes re´ gions des E´ tats-Unis. Les explications possibles a` cette expansion comprennent le de´ boisement et la modification des pratiques agricoles, comme on l’a observe´ en Europe, ou` cette espe` ce est devenue une adventice importante dans les cultures ce´ re´ alie` res, fourrage` res et maraıˆ che` res. En Ontario, L. communis est depuis peu conside´ re´ e comme une adventice du ble´ (Triticum aestivum), du maı¨ s(Zea mays) et du soja (Glycine max). Divers herbicides donnent de bon re´ sultats dans les cultures de maı¨ s, mais la lutte s’ave` re plus ardue dans les champs de ble´ d’hiver, ou` l’usage du MCPA et du 2,4-D sans autre herbicide est inefficace ou presque. On n’a pas encore e´ value´ les moyens de lutte dans les champs de soja. En Europe, le de´ sherbage me´ canique et chimique permet de combattre cette mauvaise herbe, mais L. communis are´ cemment acquis la tole´ rance au MCPA. On ignore si cette adventice continuera de ce propager ou demeurera une mauvaise herbe d’importance relativement mineure pour les cultures au Canada.

Mots cle´s: Lapsana communis, lapsane commune, nipplewort, LAPCO, biologie des mauvaises herbes Can. J. Plant Sci. Downloaded from pubs.aic.ca by Cornell University on 05/18/11

1. Name and Generic Status Asteraceae (Compositae): aster family Asterace´ es Lapsana communis L. * Synonym: Lampsana communis (Compose´ es). auct. Common names: nipplewort (Darbyshire et al. The genus Lapsana is a member of the 2000), nipple-wort, swine’s cress (Darbyshire 2003), (formerly Lactuceae) tribe (Reveal 1997; Kilian et al. dock-cress (UK); lapsane commune (Darbyshire et al. 2009). It consists of the single variable species Lapsana 2000), graveline, herbe aux mamelles (Darbyshire 2003), communis L., native to Europe and west Asia. The genus lampsane commune. European and Mediterranean formerly included nine species, five of which are now Plant Protection Organization (Bayer) code: LAPCO. treated either as variants or as taxonomically distinct

Can. J. Plant Sci. (2011) 91: 553569 doi:10.4141/CJPS10169 553 554 CANADIAN JOURNAL OF PLANT SCIENCE

subspecies of L. communis. Based on cladistic analysis of (Kiehn et al. 1991), California, USA (Stebbins et al. morphological characters, four East Asian species have 1952), the Ukraine (Stebbins et al. 1952), the United been transferred to the genus Lapsanastrum (Pak and Kingdom (Edmonds et al. 1974; Morton 1977), Portugal Bremer 1995). (Fernandez and Queiro´ s 1971), the Slovak Republic (Va´ chova and Ma´ jovskyˆ 1977; Uhrikova 1978), and 2. Description and Account of Variation Sweden (Lo¨ vkvist and Hultga˚ rd 1999). Mejı´ as (1986) (a) Species Description * The following description reported a count of n7 from Spain. Counts of 2n16 applies to the type subspecies, and is based on floras have been reported from Poland (Mizianty et al. 1981), (e.g., Provancher 1862; Gray 1884, 1889; Hegi 1929; Sell southeast Spain (Luque and Dı´ az Lifante 1991) and 1976, 1981; Stace 1991; Bogler 2006) and on personal Bulgaria (Kuzmanov and Georgieva 1977; Jurukova- observations of Canadian populations by the authors. Grancharova 1995). Measurements are given as the usual range with An early report of 2n12 (Marchal 1920) was treated extremes in parentheses. The whole mature plant, the as doubtful by Stebbins et al. (1952) whose counts were involucre, the achenes and two- and four- seedlings all of 2n14. However, Jovtchev et al. (2007) reported are illustrated in Fig. 1, AD. 2n12 for material from the German IPK genebank. Annual or winter annual with over-wintering rosette; Pak and Choi (1994) determined a somatic chromosome taproot with fibrous to thickened rootlets; stem (6) 30 number of 2n 14 for L. communis, and identified the 125 cm tall, cylindrical, slender to robust, often reddish- karyotype as consisting of 3pairs of metacentric, 3pairs green, slightly ridged, glabrous or usually with white of submetacentric and 1 pair of subtelocentric chromo- hairs that are sometimes glandular, branching above the somes. Pak and Bremer (1995) found only 2n14 in middle; alternate, thin and pliant, upper surfaces material from the United Kingdom, Sweden, the Neth- glabrate to sparsely hairy, lower surfaces with scattered erlands and the United States of America, and con- hairs mostly along the veins, margins usually hairy, 115 cluded that if the deviating numbers of 2n12 and (30) cm long, 17(10) cm wide, usually crenulate to 2n16 were to be confirmed, they would regard them as dentate, apex of the teeth or lobes with a small gland; derived, and therefore suggested that x7. Jovtchev basal leaves long-petiolate, ovate to suborbiculate to et al. (2007) found a negative correlation between lyrate-pinnatifid, with a large terminal lobe separated by endopolyploidy and temperature in L. communis, which a narrow constricted neck from smaller lateral lobes, the switched from non-endopolyploid at 22%C to being lateral lobes often vestigial; upper leaves sometimes endopolyploid when grown at 148C. entire, shortly petiolate to sessile, narrowly-ovate to lanceolate, gradually decreasing in size apically; capitula (b) Distinguishing Features * Superficially, Lapsana (flowering heads) 525 (100), in a more or less loose communis resembles other composites with yellow ray corymbose inflorescence; peduncles slender, smooth, such as dandelion (Taraxacum officinale Web. ex

For personal use only. usually more than twice as long as the involucre, slightly Wigg.), but has very different stems and leaves, parti- expanded distally, without ; involucre 510 mm cularly distinctive lyrate lobed lower leaves (Fig. 1A), long, 34 mm wide; calyculi (scale-like bractlets resem- and notable absence of a pappus on achenes (Fig. 1C). It bling a calyx) 0.51(2) mm long; phyllaries uniseriate, has been confused with sow-thistles (Sonchus spp.) or linear-lanceolate, (4)68(10), keeled toward the prickly lettuce ( serriola L.), but it lacks the base with a prominent expanded usually yellowish mid- spiny leaves and pappus on achenes found on these vein; receptacle flat, smooth, glabrous; ligules (spread- species (Cowbrough 2005). It can also be confused with ing limbs of ray florets) 815, up to 1.5 times as long as wall lettuce [Lactuca muralis (L.) Fresn.,Mycelis the involucre, with very fine longitudinally striped muralis (L.) Dumort.] with many similarities in mor- cuticle patterns (Baagøe 1977), pale to deep yellow, phology and habitat, but in this species the lyrate lower apex blunt, notched into 5 shallow teeth; anthers fused leaves are more prominently pinnate, the terminal lobe

Can. J. Plant Sci. Downloaded from pubs.aic.ca by Cornell University on 05/18/11 in cylindrical tube, brown, apical lobes not tailed; style triangular or 3-lobed, the lateral lobes are distinctly slender, pubescent on the upper part, stigma spreading; angular and less dissimilar in size, the capitula have only cypselae (achenes, often referred to as ‘‘seeds’’) di- five-ray florets (as compared with 815 in L. communis) morphic, outer much longer than inner, (3)3.54 and the achenes have a prominent pappus of hair-like mm long, tan to golden brown, slightly dorsiventrally bristles (illustrated in Douglas et al. 1998). Kno¨ rzer flattened, curved, 1820-ribbed, glabrous, gradually (1971) stated that the spindle-shaped, slightly-curved, tapered at the proximal end, terminating in a ring-like many-ribbed achenes of L. communis could not be bulge at the distal end (Fig. 1C); pappus absent. confused with those of any other composites. Cotyledons round or spoon-shaped (Fig. 1D). Chromosome counts of n7 and 2n12, 14, 16 have (c) Intra-specific Variation * Several subspecies have been reported. Canadian counts of 2n14 are from been recognized, although only the type, subsp. com- Haida Gwaii (Queen Charlotte Islands), BC (Taylor and munis, is known in most of Europe (e.g., Hegi 1929; Mulligan 1968), and Montreal, QC (Morton 1981). Hanf 1970; Sell 1981; Berkefeld 1988) and as an Other counts of 2n14 are reported from Austria introduction to North America (Bogler 2006). Although FRANCIS ET AL. * LAPSANA COMMUNIS L. 555 For personal use only. Can. J. Plant Sci. Downloaded from pubs.aic.ca by Cornell University on 05/18/11

Fig. 1. Lapsana communis. A. Drawing of flowering plant adapted from ‘‘Flora londinensis’’ by W. Curtis (17751798). B. Involucre after seed dispersal showing the small -like outer phyllaries and the eight longer inner phyllaries with the mid-vein keeled towards their base. C. Achenes; two at left in abaxial view, centre achene in lateral view, two at right in adaxial view. D. Seedlings at the two (above) and four (below) leaf stages.

from North Africa are usually included with the the latter has occasionally appeared elsewhere in Europe typical subspecies, those plants with larger involucres as an introduction (Sell 1981; Clapham et al. 1987; are sometimes differentiated as subsp. macrocarpa Buttler 1999); subsp. alpina (Boiss. & Balansa) P. D. Sell (Cosson) Arcangeli (Sell 1981). Subspecies adenophora is largely confined to the mountains of ; subsp. (Boiss.) Rech. f. and subsp. intermedia (M. Bieb.) Hayek pisidica (Boiss. & Heldr.) Rech. f. has been doubtfully are mainly confined to southeastern Europe, although recorded in mainland and extends 556 CANADIAN JOURNAL OF PLANT SCIENCE

from the eastern Aegean islands through Turkey into gardens (e.g., Miller 1752, 1768; Hegi 1929) and as an west Asia; and, subsp. grandiflora (M. Bieb.) P. D. Sell easily controlled weed on arable land (Morse and occurs in the Caucasus and in eastern and north-eastern Palmer 1925). However, after centuries of attracting Anatolia. Sell (1981) has provided a key to the little attention as a weed, it has recently become more subspecies of Lapsana communis, in which most are weedy and problematic, spreading in a number of distinguished from the typical subspecies by ligules more cropping systems, including fodder crops, cereals, vege- than twice as long as the involucre, and by individual tables, orchards and vineyards, particularly in the east- differences such as numerous stems, glaucous leaves, ern and northern parts of its range (Weber and Gut and a perennial habit (subsp. alpina), an annual to 2005). The species has become an important weed in perennial habit (subsp. adenophora, pisidica, intermedia, cereal crops throughout northern Europe including and grandiflora), dense crispate glandular hairs on the Denmark (Jensen 1991), the United Kingdom (Marshall lower stem (subsp. pisidica), or ovate undivided leaves 1989; Bond et al. 2007), Estonia (Vesik 2001; Reintam and very large ligules (subsp. grandiflora). and Koster 2000), Finland (Raatikainen and Raatikai- Within the typical subspecies, Berkefeld (1988) noted nen 1979; Salonen and Ervio 1988; Salonen 1993; differences in morphology which he treated as distinct Hyvo¨ nen et al. 2003; Haukkapa¨ a¨ et al. 2005; Hyvo¨ nen ecotypes or races. Plants growing in fields matured more 2007), France (Barralis et al. 1988), Norway (Semb and quickly, branched more profusely, flowered slightly Skuterud 1996; Skuterud et al. 1998; Berge et al. 2008), earlier and for longer, and produced achenes much Poland (Hocho 1990; Wojcik 1998; Snarska 2004), and larger than those growing in woodlands, but remained Sweden (Hallgren 1996). shorter than their woodland counterparts. The latter In the United Kingdom (Froud-Williams and were not only taller, but less branched, with longer Chancellor 1987), L. communis ranked 16th among the internodes, looser heads, shorter lateral shoots, 25 most frequent broadleaved weeds in ‘‘winter oilseed and were less aggressively weedy. These differences rape’’ (canola, Brassica napus L.) fields that had either appear to be phenotypic responses to environmental survived herbicide treatment or had not been sprayed. conditions and are not taxonomically significant. Its total occurrence in the 450 fields surveyed was 3%, divided nearly equally between the margins, headlands, (d) Illustrations * The whole plant (Fig. 1A), an empty and field areas; and was also among a group of species involucre (Fig. 1B), achenes (Fig. 1C) and seedlings associated with canola, but either totally or virtually (Fig. 1D) are illustrated. An excellent colour illustration absent from cereals. Lapsana communis was among the can be found in Thome´ (1905). Other illustrations can be 16 most common weed species in spring cereal and found in Hegi (1929), Muenscher (1955), Blamey and vegetable field plots in southern and central Finland Grey-Wilson (1989), Douglas et al. (1998), and Bogler (Ervio et al. 1994). In Denmark, L. communis was (2006). among those weeds requiring control in a variety of

For personal use only. spring- and autumn-sown crops including cereals, 3. Economic Importance and Environmental canola, sugarbeet (Beta vulgaris L.) and vegetables Impact (Jensen 1991). More than 1000 field trials were con- (a) Detrimental * Early reports from North America ducted in a variety of spring- and autumn-sown crops (See Sections 5c and 6) treated L. communis as a weed of over a period of almost two decades and showed that L. gardens, ruderal sites and waste places but did not cite communis remained moderately competitive in both crop areas, apart from an isolated report from Quebec crop types, with an average ranking among the most (Provancher 1862); nor has it been recognized as a weed common weed species of 5th in autumn-sown crops and of crops in more recent provincial and state floras of of 10th in spring-sown crops, and with average fresh North America (e.g., Douglas et al. 1988; Zinck 1998; weights of 6 and 3g per plant, respectively (Jensen Bogler 2006), although specimens in Canadian herbaria 1991). It has been reported in Danish crops of potato

Can. J. Plant Sci. Downloaded from pubs.aic.ca by Cornell University on 05/18/11 have occasionally been collected from cleared fields and (Solanum tuberosum L.), pea (Pisum sativum L.), carrot pastures. In southern Ontario it has recently become (Daucus carota L.), parsnip (Pastinaca sativa L.), celery more prevalent in field corn (Zea mays L.), soybean (Apium graveolens L.) and onions (Allium cepa L.) [Glycine max (L.) Merr.] and winter wheat (Triticum (Brendstrup and Koster 1998), and has also been among aestivum L.), particularly under reduced tillage systems the major weeds of pasture seed crops, such as timothy (Cowbrough 2005). It is also a species of concern in (Phleum pratense L.), Kentucky blue grass (Poa praten- natural environments, such as Garry oak (Quercus sis L.), red fescue (Festuca rubra L.), meadow fescue (F. garryana Hook.) ecosystems in British Columbia where pratensis Huds.), and red clover (Trifolium pratense L.) it now occurs widely (Fuchs 2001; Lilley 2007). In the (Aamisepp 1982). United States, its recent appearance in Texas was as a In Poland, increased infestation by several weeds, weed in a landscaped area (O’Kennon et al. 1999). including L. communis, was noted in winter rye (Secale In Europe the species appears to have spread with the cereale L.) fields under conservation tillage systems expansion of agriculture (see Section 6) and has long (Kraska and Pays 2007; see also Section 12). In Turkey been reported occurring around dwellings and in it is among the dominant weeds of commercial hazelnut FRANCIS ET AL. * LAPSANA COMMUNIS L. 557

(Corylus avellana L.) orchards (Mennan et al. 2006). chlorosis (Manning et al. 2002; Manning and Godzic In the Russian Federation of the former USSR, L. 2004). communis was among important weeds of fodder beet (Kameneva et al. 1987). In Sweden, it has been among (c) Legislation * The species is not listed as noxious or weeds requiring control in meadow fescue seed crops invasive in weed legislation in either Canada or the (Pettersson 1984).Weed surveys in fields, winter wheat, United States. winter and spring barley (Hordeum vulgare L.), and one- year fallow, along a north-south European climate 4. Geographic Distribution gradient at locations in Italy, Hungary, Germany and This introduced species is reported from all Canadian Sweden found L. communis to be among the typical provinces, although no specimen from Prince Edward weed species of the more northern climate zones Island, where it had been reported as present (see (Glemnitz et al. 2000). Section 6), was located during this study (Fig. 2). It is In the United Kingdom it has been reported as a local and may be ephemeral in the three Prairie contaminant in local and imported forage grass seeds, Provinces. In the United States, it has now been with a gradual increase from ca. 6% to ca. 13% of seed reported from 38 states, including those in New samples (origin not specified) tested between 1927 and England, where its populations are concentrated, all 1957 (Bond et al. 2007). Gooch (1963) reported up to Pacific states, Hawaii (two islands: Maui and Hawaii), 12.3% contamination of grass seed commodities pro- and the Alaskan Panhandle (Bogler 2006; USDA, duced in the United Kingdom and up to 29% of grass NRCS 2009). seed produced in Sweden and Denmark, noting that In its native range, it occurs in Europe east to Russia, L. communis was relatively more frequent than other Ukraine, the Caucasus and West Asia, southwest to weed seeds in Italian ryegrass (Lolium multiflorum Lam.) Northwest Africa, scattered through southern Scandi- seed stocks. navia, Finland, Russia and parts of Central Asia. It has been introduced to Canada, the United States of (b) Beneficial * The common name ‘‘nipplewort’’ was America, Argentina, Chile, Tasmania and apparently based on the use of the plant’s milky latex to (Holm et al. 1979; Hulte´ n and Fries 1986). It has been soothe cracking and inflammation of the breasts of recently recorded in the Balearic Islands (Orell Casano- vas 1985), the Vladivostok area of eastern Siberia nursing mothers, a use reported by the 16th century (Nechaeva 1992), and in Korea (Park 1999). German Camerarius for the plant known as ‘‘papillaris’’ in Prussia, and ‘‘docke cresses’’ in England (Gerard 5. Habitat 1633). Pratt (1855) and Hedrick (1919) reported that (a) Climatic Requirements * If its distribution is young spring leaves were eaten in Turkey as a salad compared with plant hardiness zone maps for Europe herb, and that leaves were eaten boiled by the ‘‘peasan-

For personal use only. and North America, L. communis is found in temperate try’’ in England as well as being used medicinally in climate zones of both hemispheres in areas with warm villages, observations that fit Gerard’s (1633) reference summers and moderate rainfall, where neither summer to the plant as a ‘‘potherb’’. Such references to culinary drought nor the early severe frosts and harsh winters of uses may belong primarily to the past (Polunin 1969; continental climate zones are common. In North Plants for a Future 2010), although the species is among America it is found mainly in Zones 57, but extends wild Asteraceae believed to have potential as a vegetable into the moderate climate of Zone 8 in the Pacific in Romania (Munteanu and Sirbu 2008). region. It is bounded roughly by eastern maritime Fontanel et al. (1998b) suggested that the large Canada and New England in the east, through south- quantity of triterpene alcohols in L. communis could eastern Quebec, southern Ontario and south central explain its healing properties. The volatile oil has United States west to the eastern Pacific states and north inflammatory and antiseptic properties with potential

Can. J. Plant Sci. Downloaded from pubs.aic.ca by Cornell University on 05/18/11 into British Columbia, average minimum temperatures for exploitation in the treatment of dermatological corresponding roughly to those cited below for the same diseases (Stanciu et al. 2007; see also Section 7c). In zones in Europe. In Europe, it has adapted to the short, Tennessee, L. communis was among local plant species but long-day summers of the Nordic region as far north studied as potential sources of oil and other industrial as southern Norway, Sweden and Finland, an area raw materials (Carr and Bagby 1987; see also Section whose climate has been moderated by the Gulf Stream, 7c). An earlier U.S. study (White et al. 1971) concluded placing it within Hardiness Zone 5 in Finland to that, although the seed oil contained crepenynic acid, Hardiness Zone 8 in coastal Norway, with average used in protective coatings, resins and other products, minimum temperatures of 23to 298Candof12 the small achenes were not well retained on plants and to 78C respectively. Elsewhere in Europe it is found the crop potential was poor. The species is among 16 primarily in Zones 68, bounded by west-central Europe native plants tested as bioindicators for the presence of from the Baltic to the western Black Sea and northern ambient ozone in Central and Eastern Europe, its leaves in the east through northern Italy and north showing ozone injury symptoms of brown stipple and central Spain to France and the United Kingdom, 558 CANADIAN JOURNAL OF PLANT SCIENCE

Fig. 2. Distribution of Lapsana communis in Canada, based on 670 herbarium specimens from ACAD (22), ALTA (4), CAN (50), DAO (95), HAM (21), LKHD (13), MAN (2), MT (80), NSPM (12), OAC(36), QFA (103), QK (23), QUE (39), SASK (11), TRTE (30), UAC (4), UBC (41), UNB (14), UWO (14),V(43), and WAT (13). Herbarium abbreviations follow Holmgren et al. (1990).

minimum temperatures averaging 23to 78C. It is communis was reported to grow best in mineral or generally found inland from the sub-Atlantic and sub- organic rather than in clay soils (Ervio et al. 1994). In Mediterranean climate zones, in low-lying areas such as the United Kingdom and northern Europe it is reported the Rhone valley, or in warm temperate sites at 900 as adapted to ‘‘slightly acid to calcareous soils’’ (Blamey 1700 m altitude (Waldis 1984). It is not generally and Grey-Wilson 1989). In hazelnut orchards in Turkey, adapted to maritime habitats (Plants for a Future L. communis is present on a mixed soil consisting of 42% 2010), although it is present as a crop weed in coastal sand, 15% silt, 41% clay, 2.1% organic matter, and pH regions of the Gulf of Bothnia in Finland (Riesinger and 6.4 (Mennan et al. 2006). It was among plants showing For personal use only. Hyvo¨ nen 2006) and on the Black Sea Coast in Turkey a relatively low tolerance of copper-contaminated soil in (Mennan et al. 2006). Denmark, providing a minimum of 4% and a maximum In Belgium, Godefroid et al. (2006) investigated of 12% cover in the study area, and mostly present near microclimate and plant species composition variation the border of the study area (Strandberg et al. 2006). In within clearcuts of an old (Fagus sylvatica L.) the Czech Republic, L. communis was among species of forest, with a focus on gradients of air temperature and ruderal habitats whose populations increased in forest humidity, soil temperature and light intensity correlated reserves where grazing by deer (Cervus spp.) and with distance to the forest margin. Among these species, mouflon (Ovis musimon Pallas) had depleted many L. communis never occurred in sites above 35% humid- native forest species, created soil disturbance, and ity, but was otherwise among the small number of increased the organic composition of the soil (Chytry species studied that did not show a significant change in and Danihelka 1993). Can. J. Plant Sci. Downloaded from pubs.aic.ca by Cornell University on 05/18/11 expected occurrence in response to the microclimatic parameters considered. In response to moderate light (c) Communities in Which the Species Occurs * intensity, for example, change in estimated percentage Information on flora associated with L. communis in cover values was B0.03%. Canada reported below is derived primarily from speci- men labels in Canadian herbaria. In eastern Canada, L. (b) Substratum * In Canada, L. communis has been communis has been found most frequently in lowland collected from rocky, gravelly, calcareous and sandy areas and along rivers and streams, often on the margins areas, clay and rich loam soils, brackish tidal marshes, of deciduous forest zones in association with sugar and, rarely, on gypsum, shale and silica soil (herbarium maple (Acer saccharum Marsh.), oak (Quercus spp.), specimen labels). The species grows best on nutrient-rich poplar (Populus spp.), eastern white cedar (Thuja damp loamy and clay soils which are fairly rich in occidentalis L.) and various shrubs and wild flowers nitrogen (Hanf 1970); especially neutral and basic alka- such as currant (Ribes spp.), rose (Rosa spp.), climbing line soils (Plants for a Future 2010). In Finland, L. nightshade (Solanum dulcamara L.), Canada goldenrod FRANCIS ET AL. * LAPSANA COMMUNIS L. 559

(Solidago canadensis L.) and wild lettuce (Lactuca spp.). from roadsides in Charlottetown, PE, in 1914, but there In British Columbia, it has been found in lowland, are no recent reports from that province (Catling et al. steppe and montane zones, mainly in the southeastern 1985). In other provinces, a collection was made from part of the province (Douglas et al. 1998) where it has eastern Newfoundland in 1958, and isolated collections been collected from Douglas fir [Pseudotsuga menziesii have been made from city gardens, as in Winnipeg, MB (Mirb.) Franco], arbutus (Arbutus menziesii Pursh), (1943), in Edmonton, AB (1971), in Regina, SK (1972) Garry oak and other forested zones as well as from (where it is reported to have arrived with transported roadsides and around shrubs and in gardens in urban garden plants from BC), in St. John’s, NL (1978), and areas. It is reported as a frequent non-native species in most recently in 2009 in a garden in Calgary, AB. There Garry oak meadow communities in British Columbia is no indication of a spread in those provinces with (Fuchs 2001; Lilley 2007). In the United States, it has climates outside of its typical zones. In Regina, for been reported occurring in gardens, hedges, orchards, example, it was collected again from the same garden in deciduous woodland trails, streambanks, roadsides and 1982, suggesting that the plant could be persistent in a waste areas at 501900 m (Muenscher 1955; Voss 1996; sheltered location, but was not spreading. No additional Bogler 2006), but there is little published information on sites have been reported for Newfoundland (Rouleau the associated flora. and Lamoureux 1992). In Europe, the earliest archaeological remains of L. In the United States L. communis was recorded by communis achenes were found in association with seeds Gray (1884, 1889) and by Britton (1901) as present in of Rumex spp. and Poa spp. (Kno¨ rzer 1971; see Section New England and on the Columbia River as well as in 6). Its presence as a weed of gardens, hedgerows, and Canada. From New England it began to spread to the various ruderal and waste sites has been noted in many midwest, appearing in Michigan in the early 20th parts of Europe (e.g., Miller 1768; Hegi 1929; Hanf century, where its population began to increase drama- 1970). In the United Kingdom, it has been prevalent in tically in the 1970s (Voss 1996). It was recently collected damp open woods, hedgerows, on walls, in cereal and in Georgia, possibly having spread from Tennessee or root crops, in gardens; on waste and disturbed ground; North Carolina (Stiles and Howel 1998); has spread to and at altitudes up to 450 m (Salisbury 1961; Hanf 1970; Texas (O’Kennon et al. 1999); and has been spreading in Stace 1991). In Poland, L. communis is found in cereal North Carolina, where it is treated as an introduced but fields in the southeastern foothills in association with not invasive ‘‘exotic’’ (Pointdexter 2006). It was first four-seeded vetch [Vicia terasperma (L.) Schreb.] and collected on Maui in 1916 at the Haleakala Crater and common hemp-nettle (Galeopsis tetrahit L.) (Wojcik was first collected on the Big Island (Hawaii) in 1981 1998), and is frequent in ruderal habitats along with a (Wagner et al. 2005). variety of chenopods, grasses, crucifers, members of the Hulten and Fries (1986) suggested that L. communis is pink family and composites, as well as infesting culti- ´ probably indigenous to central and southeastern Eur-

For personal use only. vated fields (Korniak and Kalwasinska 2001). In hazel- nut orchards in Turkey, Lapsana communis occurs with ope, spreading with the migration of farming commu- such species as bracken, Pteridium aquilinum (L.) Kuh., nities. Seeds of L. communis have been found with those lamb’s-quarters, Chenopodium album L., Himalayan of grasses and chenopods at sites in the fertile loess soils blackberry, Rubus armeniacus Focke (reported as R. of the Rhineland dating from the Ceramic period of the discolor Weihe & Nees), mugwort, Artemisia vulgaris L., fifth millennium BC to the Bronze age around 1250 BC dog nettle, Urtica urens L., Bermuda grass, Cynodon (Kno¨ rzer 1971). It is believed that most of these plants dactylon (L.) Pers., black grass, Alopecurus myosuroides grew originally in the same vegetation zones including Huds., green foxtail, Setaria viridis (L.) P. Beauv., and forest margins and hedges surrounding fields as is still annual blue grass, Poa annua L. (Mennan et al. 2006). the case in the Rhineland, where they have rarely been found in weed-crop complexes (Kno¨ rzer 1971; Groenman-van Waateringe 1979). At seven neolithic Can. J. Plant Sci. Downloaded from pubs.aic.ca by Cornell University on 05/18/11 6. History In Canada, L. communis was first collected from Quebec sites in other parts of Germany where L. communis was (probably Quebec City) as early as 1833 (Hooker 1840) present, only two sites showed any evidence of a weed- and later Provancher (1862) mentioned it as a weed at cereal crop complex (Kno¨ rzer 1971). The later spread of St. Joachim. A few years later (1871), it was collected in L. communis into crop areas has been attributed in part Owen Sound, ON. Between 1883and 1905 it was to changes in cultivation practices leading to transfer of collected from numerous locations in southern Quebec, seed, such as forest clearance and transport of sod from Ontario and British Columbia as well as at one location heath, peat, meadows, field edges, etc. as fertilizer for each in New Brunswick (1883) and Nova Scotia (1890) areas where soils were nutrient-depleted (Groenman-van (herbarium specimens). From the 1950s it was collected Waateringe 1979). Further spread throughout Europe widely around those same areas at an increasing number and to other continents could have followed the of locations, and distribution maps in recent floras introduction of cereal and forage crops and their (Zinck 1998; Hinds 2000) indicate a spread from contaminants as well as of garden plants and their previously isolated locations. It was reportedly collected associated weeds (See Sections 3a and 5c). 560 CANADIAN JOURNAL OF PLANT SCIENCE

7. Growth and Development components of volatile oil extracted from L. communis (a) Morphology * The numerous yellow flowers are plants harvested at the flowering stage consisted of attractive to small insect pollinators. As with most limonene at a concentration of 22.5 g L1, acetophe- annuals, the species is highly variable in stem height, none, nonanal, ethyl-3-hydroximandelic acid ester, de- achene size and other features (see end of Section 2c), canal, heptadecane, octadecane, dibuthyl phthalate and for example, under adverse conditions plants may grow squalen, the limonene providing protection against to only 610 cm and produce 23capitula (Canadian other potentially harmful constituents in the volatile herbarium specimens). Ennos and Fitter (1992) recorded oil (Stanciu et al. 2007). The mineral content of the a 12% allocation of resources to root anchorage (as achenes, as represented by the percentage of ash, was measured in dry matter), with approximately half of this reported by Fenner (1983) as 4.1% in the embryo and devoted to the taproot and the other half to fibrous 1.7% in the seed coat. roots, and a further 8% of the dry matter of L. communis was invested in absorption roots. (d) Phenology * Germination occurs mostly in the spring following achene dispersal the previous year, but (b) Perennation * Lapsana communis reproduces only may occur in the late summer or fall of the flowering by seed. Late germinating seedlings sometimes over- year. In Ontario, achenes of L. communis germinate in winter as rosettes. early spring or late autumn (Cowbrough 2005). In a greenhouse study in the United Kingdom to determine (c) Physiological Data * Lapsana communis uses the C3 maximum seedling weight attained using only the photosynthetic pathway typical of its family. Like embryo resources at a constant temperature of 208C, lettuce (Lactuca spp.) and other members of its tribe, L. communis achenes exhausted endosperm resources at L. communis possesses lactiferous canals (i.e., milky 5 wk, the plants having a minimum of two leaves in latex) in both the subterranean and aerial parts (Kilian addition to the cotyledons (Fenner 1983). Once the roots et al. 2009). Like all but a few members of its tribe, the have developed, the rate of further growth depends on species lacks endodermal oil ducts in the roots, while climate and soil conditions, but can occur rapidly. dedoublement of the endodermis without formation of Larger lyrate leaves form a rosette, followed by bolting, ducts has been reported (Kilian et al. 2009). Oil has been with progressively smaller leaves forming on the upper extracted from achenes and aerial parts, and a number parts of the stem. In Ontario, flowering has been of chemical compounds from different parts of the plant observed to occur from July to September (Cowbrough have been identified. Lapsana communis is among 2005) and the time between germination and first members of the tribe containing 1575% crepenynic capitulum production in greenhouse plants in Ottawa, acid, its achenes having 50% of this fatty acid in the oil ON, was about three months. In Europe, flowering can (White et al. 1971; Hegnauer 1977). In a Tennessee study occur from May to September (Hanf 1970). In the

For personal use only. of aerial plant parts, L. communis gave the highest yield United Kingdom, Miller (1752) observed that plants of oil (6.1%) of 51 species analysed, and also yielded flowered in April and achenes ripened in June; whereas 12.1% ash, moderate amounts of polyphenol (5.5%) Smith (1829) referred to flowering as ‘‘June, July’’. After and protein (9.3%), and contained a very low level of achene dispersal, the lower leaves begin to rapidly hydrocarbons (Carr and Bagby 1987). In France, senesce, but dried-up leaves and flower heads may Fontanel et al. (1998a) isolated caffeic, chlorogenic, remain on the stem until well into the fall (personal 3,5-O-dicaffeoylquinic, caftaric and chicoric acid (the observations). major phenylpropanoic constituent in the species) from aerial parts of the plant, as well as the flavonoids, (e) Mycorrhiza * A vesicular-arbuscular mycorrhizal isoquercitrin, luteolin and luteolin-7-O-b-glucuronide. association was reported by Polish and German sources Although the high oil content detected in the Tennessee for L. communis in Europe (Harley and Harley 1987).

Can. J. Plant Sci. Downloaded from pubs.aic.ca by Cornell University on 05/18/11 study was not confirmed by Fontanel et al. (1998b), they extracted 2.01% oil, consisting of 43.2% nonsaponifi- 8. Reproduction able matter, a 42.5% mix of nonsaponifiable matter and (a) Floral Biology * Lapsana communis is a protandrous triterpene alcohols, and 18.4% triterpene alcohols; fatty ( mature prior to stigmas being receptive) acids consisting of myristic, palmitic, 10, 13- or 11, 14- sexually reproducing species (Jurukova-Grancharova octadecadienoic, a-linolenic, stearic and arachidic acids; 1995), pollinated by insects or often self-pollinated, and triterpene alcohols consisting of three unidentified and during the second or pistillate phase of anthesis, compounds and of taraxerol, b-amyrin, germanicol, a- the stigma branches diverge widely in such a way that amyrin, lupeol, cycloartenol and c-taraxasterol. Five automatic self-pollination is regularly effected if insect guaianolide glycosides were identified in extracts of the visitors have not removed the pollen during the first latex from young stems of L. communis: two previously phase of anthesis (Knuth 1908). Pollinators are attracted known sesquiterpene lactone glycosides, crepiside E by the nectar produced from the start of anthesis by and tectoroside, and three new compounds, lapsanoside collar-like nectaries around the base of the style and A, B, and C (Fontanel et al.1999). In Romania, on top of the inferior ovary (Wist and Davis 2006). FRANCIS ET AL. * LAPSANA COMMUNIS L. 561

The small capitula will remain open to pollinators somewhat higher at 1000 achenes per plant, with a during bright or sunny weather, but will close in late suggestion that in ruderal habitats the actual number of afternoon or altogether if the weather is unfavourable achenes produced can be much higher (Bond et al. (Knuth 1908). 2007). Achenes are relatively small, but size and number The ability to self-pollinate was confirmed in a recent may vary considerably, depending upon conditions as Russian study of achene formation under different noted by Berkefeld (1988) (see Section 2c). In a study of flowering regimes. There was no evidence of apomictic achenes collected from a variety of open and closed reproduction in L. communis following emasculation of habitats in the United Kingdom, Fenner (1983) found capitula, but non-emasculated capitula could produce an average weight of 1.07 mg, with an embryo weight of high seed set even when blooming in isolation, indicat- 0.6 mg. Guitia´ n and Garrido (2006) determined an ing that the species was among facultatively allogamous average weight of 0.44 mg for achenes collected from a species (Kashin et al. 2007). deciduous woodland in northwestern Spain; whereas The style projects 1.52 mm from the anther-cylinder, Jankowska-Blaszczuk and Daws (2007) determined a which in turn exceeds the corolla tube of the disc florets mean weight of 0.86 mg for achenes collected from a by 23mm (Knuth 1908). The anthers are tetraspor- deciduous forest in Poland. angiate, the mature pollen is 3-celled, and the pollen The absence of a bristly pappus ensures that achenes grains are yellow, polyhedral, and average 31 mmin of L. communis, although relatively small and light, will diameter (Knuth 1908; Jurukova-Grancharova 1995). not be carried long distances by wind, as is the case for Transmission and scanning electron microscopy of the many Asteraceae, such as dandelion, and there is no pollen grains has shown them to be echinolophate in evidence of dispersal by birds or mammals. As noted in structure, with sections including both ridge and lacunar Sections 3a and 6, dispersal of L. communis has been areas (Skvarla et al. 1977). very slow and gradual from forest margins and ruderal Although Mu¨ ller (1883) suggested that flowers of L. areas to neighbouring cultivated areas, although long- communis attracted few insect visitors and were primar- distance dispersal has occurred in the course of transfer ily self-pollinated, florets have a pollen-presentation of soil associated with sod and garden material. The mechanism involving stamens with sensitive (or ‘‘irrita- species has also been documented as a contaminant of ble’’) filaments, which contract in response to touch (of cereal and other grass seeds (see Section 3a). In a study filaments or anther tube) by flower visitors. A general of understorey plants in a managed temperate forest in description of the pollen-presentation mechanism in the Denmark (Svenning and Skov 2002), L. communis was family is given by Proctor and Yeo (1973). The present mainly in open areas with a minimal spread to mechanism, clearly an adaptation for insect pollination, neighbouring plots, and, like other poor dispersers, is seen in many (but not all) members of the Asteraceae showed a stronger tendency to clumping at the 100-m (Small 1917a, b). Small (1917a) described the touch scale compared with more effective dispersers.

For personal use only. response he observed in Lapsana communis as a marked lateral movement towards the touch accompanied by (c) Seed Banks, Seed Viability and Germination * There pollen being expressed at the top of the anther tube. are no published Canadian studies on L. communis In Europe, flowers have been observed to attract achene behaviour. All observations on the seed bank relatively small pollinators including the following: the and long-term viability of its achenes have come from syrphid flies Melanostoma mellinum L., Syritta pipiens Europe. The botanist Philip Miller (1752) noticed that L., Eristalis arbustorum L., E. nemorum L., E. sepulcralis the seed bank of L. communis was depleted after only 2 L. and Ascia podagrica Fabr. (Diptera: Syrphidae); 3yr of emergence in English gardens. A 5-yr study of house-flies (Diptera: Muscidae); butterflies (Lepidop- seedling emergence in the United Kingdom (Roberts terae); and several bees, Lasioglossum leucozonicum and Neilson 1981) confirmed that the majority of Schr., L. morio Fabr. and L. smeathmanellum (Kirby) achenes germinated in the first 23yr, although a small

Can. J. Plant Sci. Downloaded from pubs.aic.ca by Cornell University on 05/18/11 (Hymenoptera: Halictidae) (Knuth 1908; Drabble and percentage remained viable up to 5 yr. In France, Drabble 1927). A dagger fly, Empis pennipes L. changes in the soil seed bank were monitored over a (Diptera: Empididae), a cabbage butterfly Pieris rapae 4yr period on plots sown initially with L. communis and L. (Lepidoptera: Pieridae) and unidentified syrphid flies other weeds at known densities and with subsequent were photographed visiting flowers in Belgium (Lindsay shedding prevented (Chadoeuf et al. 1984). Lapsana 2005). communis was among species that disappeared rapidly The embryo develops according to the Asterad-type from the seed bank, the decrease being greatest in the (i.e., a blending of terminal and basal cells following first year. In a 5-yr study of weed seeds sown by hand in longitudinal division of the two initial embryonic cells) single-crop fields of winter wheat and spring barley (Jurukova-Grancharova 1995). (Barralis et al. 1988), L. communis showed a very high rate of annual decline in the seed bank, about 80% per (b) Seed Production and Dispersal * In Ontario, a plant year, with emergence representing an average of 15% of may produce from 400 to 800 achenes (Cowbrough the annual seed bank. In both French studies, viability 2005). In the United Kingdom, the figure given was of buried seeds remained relatively high. In Sweden, 562 CANADIAN JOURNAL OF PLANT SCIENCE

viability among buried seeds did not decrease signifi- plants, but moves into new areas after fire and other cantly over a 2-yr study period, although the long-term disturbances (Starr and Starr 2008; F. Starr, personal survival rate of L. communis was, at less than 5 yr, communication May 2010). the lowest among the species studied (Milberg and In untreated sample plots in 255 fields assessed in Andersson 1997). Finland, L. communis was among dicot weeds producing In the state of Massachusetts, USA, 99% of L. the highest biomass in spring cereals, ranking 7th with a communis achenes planted immediately post-harvest frequency of 55% and an average dry weight of 21 kg germinated within 7 d at 20308C in light and dark ha1 which comprised 67% of the total average weed conditions; with pre-chilling, however, achenes became biomass (Salonen and Ervio 1988). In a comparison of dormant (Lincoln 1983). In the United Kingdom, L. weed populations in hedges and field margins and at communis was among species exhibiting relatively rapid various distances into crop fields in the United King- germination after dry storage for 12 mo at 58C, dom, L. communis was among those plants found in although some achenes also germinated well immedi- both hedges and fields: higher percent cover occurred in ately after collection (Grime et al. 1981). Seed dormancy the hedges and on the margins than in the field, studies of L. communis from November 1994 to April suggesting a spread into fields via seed banks progres- 1997 in Sweden showed inconsistent dormancy changes: sively established at different distances (Marshall 1989). in 1995, germination was lowest during the first spring Wilson and Aebischer (1995) observed a similar pattern after planting, but, from July onwards, was complete in for L. communis in British cereal fields, and emphasized full light and almost so after short light exposure, but the progressive reduction in seed bank density further was almost nil in the dark (Milberg and Andersson from the edge of the field. In Poland, the species appears 1997). In Poland, L. communis was among 27 temperate to have spread from ruderal habitats to cultivated fields deciduous forest species investigated for the effect of the (Korniak and Kalwasinska 2001); and occurred in 35% red-far red light (R:FR) ratio on the percent germina- of cereal crop fields (Snarska 2004). A forest survey in tion of their seeds (Jankowska-Blaszczuk and Daws Denmark showed little response to microclimatic para- 2007). Lapsana communis was among the small-seeded meters such as orientation, soil type, drainage, altitude species with a moderately high light requirement achiev- or stand age; the species rarely spread beyond the open ing less than 20% germination at low R:FR, and 100% areas it occupied in the forest (Svenning and Skov 2002). at the highest R:FR level. The authors also found that In a study following the succession of plants in requirements of small-seeded species for light was abandoned agricultural fields in the United Kingdom, reflected in a greater persistence in the soil seed bank, L. communis was displaced by later successional species although this generalization is not consistent with the after several decades (Brenchley and Adam 1915). As above-cited results of studies elsewhere, perhaps because noted in Section 6, L. communis populations in Europe results were averaged over a number of species. have tended to remain in typical habitats of forest and

For personal use only. field margins for centuries, rarely moving into or (d) Vegetative Reproduction * Lapsana communis does establishing within cleared fields until changes in field not reproduce vegetatively. management practices led to changes in population dynamics. 9. Hybrids No cases of inter-specific hybridization involving L. 11. Response to Herbicides and Other Chemicals communis were found. In southern Ontario, control of L. communis has been difficult, especially if plants were past the early seedling 10. Population Dynamics or rosette stage. However, based on single field trials in No published statistics on population spread or struc- corn and winter wheat, suggestions for control of this ture of L. communis in Canada were found. The species weed using post-emergent herbicides applied at recom-

Can. J. Plant Sci. Downloaded from pubs.aic.ca by Cornell University on 05/18/11 is still most widespread in the areas where it was first mended rates have been provided (Cowbrough 2005). reported in eastern Canada and British Columbia, with Applications of the following herbicides at the 12-leaf only a limited spread from ruderal habitats to crops (see stage or above provided 9499% control in field corn: Section 3a). In the United States, L. communis appears atrazine (10101490 g a.i. ha1), atrazine/2,4-D (936 to have spread only slowly from its original garden and 1404 g a.i. ha1; 1.5:1), bromoxynil atrazine (280 ruderal habitats, with occasional introductions to iso- 34010101490 g a.i. ha1), dicamba (600 g a.e. lated locations in new areas (see Sections 3a and 6). ha1), dicamba/atrazine (14801800 g a.i. ha1;1:2), However, in Michigan, an initially inconspicuous popu- and difluefenzopyr/dicamba (200 g a.i. ha1; 1:2.6); and lation began to increase dramatically in size in the 1970s 6083% control was provided by mesotrione (100 g a.i. into newly disturbed areas along trails and roads in ha1), primisulfuron/dicamba (166 g a.i. ha1;1:5.3), deciduous woods, in gardens, hedges and various waste and prosulfuron dicamba (10 g a.i. ha1140 g a.e. places (Voss 1996). In Hawaii, it populates mainly ha1) (Cowbrough 2005). In winter wheat, clopyralid higher elevations on Maui and Hawaii, and it is not (200 g a.e. ha1), dicamba/MCPA/mecoprop (400600 g always competitive in communities with more aggressive a.e. ha1; 1:4.4:1) and dichlorprop/2,4-D (1017 g a.i. FRANCIS ET AL. * LAPSANA COMMUNIS L. 563

ha1;1.1:1)provided6975% control, whereas thifen- In peas, aclonifen could be used alone or in tank sulfuron-methyl/tribenuron-methyl (15 g a.i. ha1;2:1), mixtures or sequential treatments with bentazon, and bromoxynil (280340 g a.i. ha1), dicamba (110139 g in potatoes, in tank mixtures or sequential treatments a.e. ha1), bromoxynil/MCPA (560 g a.e. ha1;1:1), with metribuzin. In Norway, greenhouse pot experi- MCPA (350850ga.e.ha1) and 2,4-D (350550ga.e. ments were carried out to study the effect of herbicide ha1) were progressively less effective, down to 0% doses and application times on the production of weed control for the latter, all applied at the nine-leaf stage or seeds in a reduced tillage system (Semb and Skuterud older (Cowbrough 2005). No field studies on the control 1996). The weeds were sprayed once with glyphosate at of this weed in soybeans have been published. 360 and 720 g ha1 and glufosinate at 200 and 400 g In Sweden, L. communis was among weeds that ha1 at the developmental stages of full flowering, and increased in frequency in spring cereals during 1951 at 10 d or 20 d later. The number of viable seeds of all 1990, suggesting that the herbicide mixture used to species studied was reduced by 90100% with applica- control weeds during this period (300 g L1 tions at full flowering, whereas later spraying had little dichlorprop130 g L1 MCPA58 g L1 ioxynil effect on the weight or number of viable seeds. The 38gL1 bromoxynil) had become less effective over greatest impact on the number of achenes of L. time (Hallgren 1996). In the United Kingdom, pyridate communis was obtained at the highest dose of glufosi- applied at post-emergence at rates of 1000 and 1500 g nate. Field experiments (19901991) in commercially a.i. ha1 was effective against a broad spectrum of grown cereal fields and fields sown with spring rape weeds in small grains and corn and selectively controlled were performed at the two- to four-leaf stage using a low L. communis in wheat and barley (Diskus et al. 1976). In dose spray mixture of ioxynil dichlorprop MCPA Germany, metsulfuron-methyl, a herbicide with low at rates of 53, 223 and 75 g a.i. ha1, respectively toxicity to wildlife and rapid absorption via the roots (Skuterud et al. 1998). Spraying took place at different and leaves of weeds, provided 100% control of L. times of the day. Lapsana communis was among the least communis in winter cereals at an application rate of 8 susceptible to this herbicide mixture when sprayed in the g a.i. ha1 (Drobny 1984). In Russia, L. communis was evening, when the number of plants and dry weight was among weeds treated at the two- to four-leaf stage that considered. Spraying reduced the weight of this species were controlled by application of either 1200 g lenacil more than the number of plants. It was suggested that 6 L phenmedipham ha1 by broadcasting, or 600 g the greater efficacy of applying herbicides in the lenacil3L phenmedipham ha 1 by banded placement morning might be attributed to a lower risk of rain (Kameneva et al. 1987). and strong wind during this time of day. In Finland, forage seed crops sprayed once with In Turkish hazelnut orchards, mechanical control bromoxynildichlorpropioxynilMCPA or with using either rotary hoeing or mowing combined with MCPAmecopropclopyralid in spring, or twice post-emergent herbicides glyphosate (2400 g a.i. ha1) 1

For personal use only. when the crop grass had 1 or 2 nodes, reduced the or paraquat (1000 g a.i. ha ) provided 100% control of numbers and weight of weeds, including L. communis, L. communis; rotary hoeing combined with pendimetha- but the effect was relatively small with the single lin at 1320 gfluazifop-p-butyl at 120 g a.i. ha1 application, and the meadow fescue crop required two provided 6065% control, less than control achieved applications of MCPAmecopropclopyralid for ef- by rotary hoeing alone; and mowing combined with fective weed control (Ervio 1982). The effectiveness of pendimethalin at 1320 g fluazifop-p-butyl at 120 g a.i. imidazolinones (IMIs), a group of herbicides inhibiting ha1 provided 70% control, slightly greater than mow- acetolactate synthase (ALS) activity in IMI-resistant ing alone (Mennan et al. 2006). canola, was tested at several locations, using imazamox (Haukkapa¨ a¨ et al. 2005). Imazamox was very effective 12. Response to Other Human Manipulation against the most troublesome weeds, but was largely Control of L. communis was achieved in the United

Can. J. Plant Sci. Downloaded from pubs.aic.ca by Cornell University on 05/18/11 ineffective against L. communis. In spring wheat fields Kingdom through prevention of achene dispersal and where L. communis had a moderately high frequency destruction of young plants by hoeing and tillage and biomass (see Section 10), control by MPCA sprayed (Morse and Palmer 1925). In Norway, Fiveland (1974) at 1200 g a.i. ha1 was poor (9%), confirming that this found that competition from L. communis and other species was among several that had become tolerant weeds in swede [Brassica napobrassica (L.) Mill.] and to MCPA, whereas dichlorpropMCPA provided 49% carrot crops could begin to affect yields after 28 d, and control and mecopropMCPA 90%, the MCPA to significantly affect yields after 42 d, but yields mixtures applied at an average rate of 25004000 g a.i. increased significantly after periods of hand-weeding ha1 (Salonen and Ervio 1988). every 14 d after planting up to 42 d, after which the In Denmark, the herbicide aclonifen, applied pre- or crops themselves provided effective weed control. In post-emergence on clay or sandy soils, or post-emer- Germany, the use of herbicides to control L. communis gence on organic soils was found to provide effective and other weeds in canola could be replaced by the control of L. communis and other weeds in a number of use of fast-growing cultivars and thorough seedbed vegetable garden crops (Brendstrup and Koster 1998). preparation, with rolling (to reduce the detrimental 564 CANADIAN JOURNAL OF PLANT SCIENCE

herbivory from snails), early sowing, and cultivation to nutritious pasture plants such as red clover, red fescue control volunteer cereals (Klischowski and Beyer 1989). or timothy (Pettersson 1984; Aamisepp 1982, 1984; In Turkey, cover crops of Italian ryegrass, hairy vetch Nortoft 1985; Bond et al. 2007). However, there is no (Vicia villosa Roth) and red clover combined with suggestion that the weeds themselves were not eaten or mechanical control methods (rotary hoeing and mow- were harmful to animals. ing) were tested in hazelnut orchards for their weed control efficacy (Mennan et al. 2006). Residues from all (ii) Birds and other vertebrates * No information three cover crops suppressed L. communis, reducing the located. weed biomass significantly at 20 d after desiccation of the cover crops. The level of weed control by mechanical (iii) Insects * An absence of reports of insect herbivory means alone was inadequate, with at least double the of L. communis in North America suggests that this plant density and several times the residual dry weight species may not be particularly vulnerable to insect compared with combinations including various herbi- attack, as is the case in New Zealand where it has cides (see Section 11). In a comparative study in winter suffered virtually no herbivory compared with the native rye plots in Poland (Kraska and Pays 2007), where plants (Bossdorf et al. 2005). A survey of pre-dispersal herbicides were seldom used because the dense canopy predation in herbaceous Asteraceae in the United of rye plants was expected to suppress weed growth, Kingdom and New Zealand found no L. communis both conventional tillage involving stubble cultivation capitula infested by insects (Fenner and Lee 2001). In (810 cm depth) plus pre-plant ploughing (1820 cm Quebec, where this introduced plant has been known for depth), and conservation tillage involving rigid-tine longer than elsewhere in Canada, no evidence of cultivation (18 cm depth) were tested for effectiveness significant chemical defence compounds was found in in control of weeds over a period of 6 yr. Whereas L. local populations of the species (Almeida-Cortez et al. communis and several other species were completely 1999; Almeida-Cortez and Shipley 2002). The lettuce suppressed, and other weed species were suppressed by root aphid, Pemphigus bursarius (L.) (Homoptera: 5088% under the conventional tillage regime, weed Aphididae), which attacks roots of L. communis in density and biomass were found to be almost double Europe, has been reported on lettuce and other plants under the conservation tillage regime. in Quebec, but L. communis was not reported on the list In a study of biodiversity of arable weeds in Finland, of host plants compiled by Alleyne and Morrison L. communis was among the majority of weeds that (1977). increased in frequency of occurrence between the 1960s In the United Kingdom, the lettuce root aphid (when intensive cropping measures, including herbicide overwinters in the egg stage on black poplar (Populus use and frequent ploughing, had been applied) and the nigra L.), and colonizes hosts among the Asteraceae in 1990s (when many fields had been converted to organic the following summer. Large colonies have been found

For personal use only. production characterized by omission of herbicides and on the roots of L. communis reflecting its status as a mineral fertilizers, reduced tillage, and more diverse highly susceptible host; among 64 plants examined crop rotations). For example, Lapsana communis in- between July 1956 and February 1957, 43.7% of roots creased in frequency from 41.6 to 57.3% (Hyvo¨ nen were infested by a total of 617 aphids, or 22 aphids per 2007). The density of most weeds in the study decreased infested plant (Dunn 1959). It was subsequently found (that of L. communis from 18 to 15.5 plants m2), that a proportion of the aphid species that alternate attributed by Hyvo¨ nen (2007) in part to the greater between host plants had lost the sexual phase of the life- plant diversity and number of total individuals in a cycle. These remained in the soil and overwintered as given area. Comparing production systems in Finland, asexual apterae after the aestival host plant had died in the relative abundance of L. communis in organic fields the autumn, and L. communis was among the host was considerably lower (1.5% in MayJune, 1.8% in species likely to be colonized in the spring (Phillips et al.

Can. J. Plant Sci. Downloaded from pubs.aic.ca by Cornell University on 05/18/11 JulyAugust) than in conventional cereal (3.2%, 5.2%) 1999). When clones of P. bursarius were cultured first on and dairy farms (7.9%, 8.6%) where traditional man- L. communis as a ‘‘home’’ host and subsequently on two agement practices were used, suggesting that it differ- ‘‘away’’ hosts, Lactuca and Matricaria, no clones entially benefited within the weed flora from herbicide survived on Lactuca and only a few on Matricaria, use and high nitrogen input (Hyvo¨ nen et al. 2003). and populations of this aphid on L. communis appeared to be a mixture of cyclical and obligate parthenogens 13. Response to Herbivory, Disease and Higher and were more genetically heterogenous than popula- Plant Parasites tions on other hosts (Miller et al. 2005). In Sweden, L. (a) Herbivory communis is among summer hosts of the lettuce root (i) Mammals, including both domestic and wild animals * aphid (Ramert 1977). Lapsana communis is said to be eaten by all domestic A number of phytophagous insects have also been animals except goats (Fogelfors 1984). In reports of reported on L. communis in the United Kingdom weed contamination of pasture seed crops, the weeds, including the leaf miners Chromatomyia syngenesiae including L. communis, reduced the percentage of more Hardy, Ophiomya cunctata Hendel, and Phytomyza FRANCIS ET AL. * LAPSANA COMMUNIS L. 565

marginella Falle´ n (Diptera: Agromyzidae); the aphid curators of the following Canadian herbaria for making Hyperomyzus lampsanae Bo¨ rner (Homoptera: Aphidi- specimens available for study: ACAD, ALTA, CAN, dae) on leaves and shoots; and the moth Phalonidia DAO, HAM, LKHD, MAN, MT, NSPM, OAC, QFA, gilvicomana Zeller (Lepidoptera: Tortricidae) on QK, QUE, SASK, TRTE, UAC, UBC, UNB, UWO, V achenes (Filter and Peat 1994). and WAT. A British study showed a relationship between small capitulum size and reduced pre-dispersal achene preda- Aamisepp, A. 1982. Weed control in pasture seed crops. tion among species of Asteraceae (Fenner et al. 2002). Engfroavl. 1982: 211219. Among the 20 species examined L. communis had the Aamisepp, A. 1984. Weed control in grassland seed crops. smallest capitula and showed no insect predation. Svensk Frotidning 53:3,3132, 42. Alleyne, E. H. and Morrison, F. O. 1977. The lettuce root (iv) Other invertebrates * Lapsana communis was found aphid, Pemphigus bursarius (L.) (Homoptera: Aphidoidea) in to have a high degree of palatabililty to slugs in Quebec, Canada. Ann. Entomol. Soc. Que. 22: 171180. Washington State (Cates and Orians 1975). The authors Almeida-Cortez, J. S. and Shipley, W. 2002. No significant found both Ariolimax columbianus Gould and Aarion relationship exists between seedling relative growth rate under ater L., a European slug, feeding on L. communis. nutrient limitation and potential tissue toxicity. Funct. Ecol. 16: 122127. Almeida-Cortez, J. S., Shipley, W. and Arnason, J. T. 1999. Do (b) Diseases plant species with high relative growth rates have poorer (i) Fungi * In Canada, the rust fungus Puccinia chemical defences? Funct. Ecol. 13: 819827. lapsanae Fuckel has been reported on L. communis in Baagøe, J. 1977. Microcharacters in the ligules of the British Columbia and Ontario, and the leaf spot fungus Compositae. Pages 120138 in V. H. Heywood, J. B. Har- Ramularia lapsanae (Desm.) Sacc. in British Columbia borne, and B. L. Turner, eds. The biology and chemistry of (Conners 1967; Ginns 1986). The rust fungus has been the Compositae, Vol. 1., Academic Press, London, UK. reported from three states in the USA, Minnesota Barralis, G., Chadoeuf, R. and Longchamp, J. P. 1988. (McCain et al. 1990), Oregon, and Wisconsin (Farr Longevite´ des semences de mauvaises herbes annuelles dans and Rossman 2010). The only fungi reported on L. un sol cultive´ . Weed Res. 28: 407418. communis in New Zealand are P. lapsanae and R. Berge, T. W., Aastveit, A. H. and Fykse, H. 2008. Evaluation lapsanae, and the former has also been reported from of an algorithm for automatic detection of broad-leaved weeds Chile (Farr and Rossman 2010), suggesting that these in spring cereals. Precis. Agric. 9:391405. monophagous pathogens were introduced along with Berkefeld, K. 1988. Investigations about ecotype formation in the host species. The above and numerous other fungal Galium aparine L. (Rubiaceae) and Lapsana communis L. pathogens have been reported from various parts of (Compositae). Flora (Jena) 181: 111130. [in German, English Europe (Fitter and Peat 1994; Farr and Rossman 2010), abstract]. Blamey, M. and Grey-Wilson, C. 1989. The illustrated flora of

For personal use only. among them the oligophagous Podosphaera fusca (Fr.) Britain and northern Europe. Hodder & Stoughton, London, U. Braun & Shishkoff, infecting leaves and stems with UK. 544 pp. powdery mildew, and Botrytis cinerea Pers., infecting Bogler, D. J. 2006. Lapsana Linnaeus. Page 257 in Flora of stems, leaves and achenes with grey rot or blight; but the North America north of Mexico. Vol. 19. Magnoliophyta: majority of the 56 species reported from the United Asteridae, part 6: Asteraceae, part 1. Oxford University Press, Kingdom are generalists and saprophytic on rotting or New York, NY. dead stems and leaves. In eastern Europe, L. communis Bond, W., Davies, G. and Turner, R. 2007. The biology and was among Asteraceae harbouring the lettuce downy non-chemical control of nipplewort (Lapsana communis mildew fungus, Bremia lactucae Regel, but there was no L.). Henry Doubleday Research Association, Ryton Organic interspecific transmissibility of B. lactucae isolates from Gardens, Coventry, UK. 3pp. [Online] Available: http:// the host species to Lactuca sativa cultivars (Lebeda and www.getsetgrow.org.uk/organicweeds/downloads/lapsana%20 communis.pdf [2010 May 13]. Can. J. Plant Sci. Downloaded from pubs.aic.ca by Cornell University on 05/18/11 Syrovatko 1988). Lindsay (2005) photographed infec- tion by Podosphaera fusca and Puccinia lapsanae on Bossdorf, O., Auge, H., Lafuma, L., Rogers, W. E., Siemann, E. leaves of L. communis in Belgium and Prati, D. 2005. Phenotypic and genetic differentiation between native and introduced plant populations. Oecologia (ii) Bacteria * No information located. 144:111. Brenchley, W. E. and Adam, H. 1915. Recolonisation of (iii) Viruses * No information located. cultivated land allowed to revert to natural conditions. J. Ecol. 3: 193210. (c) Higher Plant Parasites * No information located. Brendstrup, I. and Koster, I. 1998. FENIX (aclonifen) a novel herbicide for use in potato, pea, carrot, parsnip, celery, parsley ACKNOWLEDGEMENTS root and set onions. DJF Rapport, Markbrug 2:133140. [in We thank Rob Nurse, weed scientist, AAFC, Harrow, Danish, English abstract]. ON for valuable assistance on weed control; Forest Britton, N. L. 1901. Manual of the flora of the northern Frost, plant biologist, Hawaii, for information on states and Canada. Henry Holt and Company, New York, Lapsana communis populations in Hawaii; and the NY. 1080 pp. 566 CANADIAN JOURNAL OF PLANT SCIENCE

Buttler, H. 1999. A first record of Lapsana communis L. Ervio, L. R. 1982. Repeated weed control in seed crops in subspecies intermedia (Bieb.) Hayek for Germany, with an spring. Engfroavl. 1982: 205210. overview of the genus. Florist. Rundbr. 33:37. Ervio, R., Hyvarinen, S., Ervio, L. R. and Salonen, J. 1994. Soil Carr, M. E. and Bagby, M. O. 1987. Tennessee plant species properties affecting weed distribution in spring cereal and screened for renewable energy sources. Econ. Bot. 41:7885. vegetable fields. Agric. Sci. Finl. 3: 497504. Cates, R. G. and Orians, G. H. 1975. Successional status and Farr, D. F. and Rossman, A. Y. 2010. Fungal databases, the palatability of plants to generalized herbivores. Ecology 56: Systematic Mycology and Microbiology Laboratory, ARS, 410418. USDA. [Online] Available: http://nt.ars-grin.gov/fungaldata- Catling, P. M., Erskine, D. S. and MacLaren, R. B. 1985. The bases/ [2010 May 13]. plants of Prince Edward Island with new records, nomencla- Fenner, M. 1983. Relationships between seed weight, ash tural changes and corrections and deletions. Research Branch, content and seedling growth in twenty-four species of Com- Agriculture Canada, Ottawa, ON. Publ. 1798, 272 pp. positae. New Phytol. 95: 697706. Chadoeuf, R., Barralis, G. and Lonchamp, J. P. 1984. Evolu- Fenner, M. and Lee, W. G. 2001. Lack of pre-dispersal seed tion du potentiel semencier de mauvaises herbes annuelles dans predators in introduced Asteraceae in New Zealand. N. Z. J. un sol cultive´ . VIIe` me Colloque International sur l’Ecologie, la Ecol. 25:9599. Biologie et la Syste´ matique des Mauvaises Herbes (Paris). pp. Fenner, M., Cresswell, J. E., Hurley, R. A. and Baldwin, T. 6370. 2002. Relationship between capitulum size and pre-dispersal Chytry, M. and Danihelka, J. 1993. Long-term changes in the seed predation by insect larvae in common Asteraceae. field layer of oak and oak-hornbeam forests under the impact Oecologia 130:7277. of deer and mouflon. Folia Geobot. Phytotax. Praha 28: 225 Fernandez, A. and Queiro´ s, M. 1971. Contribution a` la 245. connaisance cytotaxinomique des Spermatophyta du Portugal. Clapham, A. R., Tutin, T. G. and Moore, D. M. 1987. Flora of II. Compositae. Bol. Soc. Broteriana, se´ r. 2, 45:5121. the British Isles. 3rd ed. Cambridge University Press, Cam- Fitter, A. H. and Peat, H. J. 1994. The ecological flora bridge, UK. 688 pp. database. J. Ecol. 82: 415425. Lapsana communis. [Online] Conners, I. L. 1967. An annotated index of plant diseases in Available: http://www.ecoflora.co.uk [2010 Nov. 26]. Canada. Canada Dep.Agric. Res. Branch, Ottawa, ON. Publ. Fiveland, T. J. 1974. The competition between swedes or 1251, 381 pp. carrots and annual weeds. Meld. Nor. Landbrukshogsk 53: 21. Cowbrough, M. 2005. Nipplewort (Lapsana communis L.), 15 pp. Ontario Ministry of Agriculture, Food and Rural Affairs. Fogelfors, H. 1984. Useful weeds? Part 12. Lantmannen 105: [Online] Available: http://www.omafra.gov.on.ca/english/crops/ 14, 49. field/weeds/nipplewort.htm [2010 May 13]. Fontanel, D., Galtier, C., Debaouzy, J.-C., Gueiffier, A. and Darbyshire, S. J. 2003. Inventory of Canadian agricultural Viel, C. 1999. Sesquiterpene lactone glycosides from Lapsana weeds. Agriculture and Agri-Food Canada, Ottawa. [Online] communis L. subsp. communis. Phytochemistry 51: 9991004. Available: http://dsp-psd.pwgsc.gc.ca/Collection/A42-100-2003E. Fontanel, D., Galtier, C., Viel, C. and Gueiffier, A. 1998a. pdf [2010 May 13]. Caffeoyl quinic and tartaric acids and flavonoids from Darbyshire, S. J., Favreau, M. and Murray, M. 2000. Common Lapsana communis subsp. communis (Asteraceae). Zeitschr.

For personal use only. and scientific names of weeds in Canada/Noms populaires et Naturforsch. Sect. C, Biosc. 53: 10901092. scientifiques des plantes nuisibles du Canada. Agriculture and Fontanel, D., Kargol, M., Gueiffier, A. and Viel, C. 1998b. Agri-Food Canada/Agriculture et Agroalimentaire Canada, Triterpene alcohols and fatty acids in lipids and nonsaponifi- Ottawa, ON. Publ. 1397, 132 pp. able matter of Lapsana communis L. subspecies communis Diskus, A., Schonbeck, R., Auer, E. and Kloimstein, E. 1976. (Asteraceae). J. Am. Oil Chem. Soc. 75: 14571459. CL 11 344 a new selective herbicide for use in cereals and Froud-Williams, R. J. and Chancellor, R. J. 1987. A survey of maize. Proc. 1976 British Crop Protection Conference Weeds weeds of oilseed rape in central southern England. Weed Res. 2: 717722. (Oxford) 27: 187194. Douglas, G. W., Straley, G. B., Meidinger, D. and Pojar, J. Fuchs, M. A. 2001. Towards a recovery strategy for Garry oak (eds.) 1998. Illustrated flora of British Columbia. Vol. 1: and associated ecosystems in Canada: Ecological assessment Gymnosperms and dicotyledons (Aceraceae through Astera- and literature review. Environment Canada, Canadian Wild- ceae). British Columbia Ministry of Environment, Lands and life Service, Pacific and Yukon Region. Technical Report

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