(a) .

Species description

Capsella bursa-pastoris is a small summer or winter annual herb. It has adapted to a wide range of environments and is also phenotypically plastic contributing to wide variation in size and life history traits. It has a dominant white taproot with few lateral fine roots (Hitchcock and Cronquist 1973; Aksoy et al. 1998; Defelice 2001). A solitary or several erect stems, simple or branched, grow from the same root, generally from 10–60 cm tall but occasionally as high as 90 cm (Fig 1A). It forms a basal rosette with the first leaves at the ground surface, consisting of petiolate oblong leaves that narrow to the stalk and are usually hairy, varying from almost entire to shallowly or deeply toothed, 3–15 cm long and 4 cm wide, but occasionally longer with rosette diameters occasionally exceeding 40 cm (Neuffer and Hurka 1986b). The stem leaves are smaller than the rosette leaves, stalkless, alternate one per node, are roughly linear entire to shallowly toothed to lanceolate on upper stem, basal leaves sagittate (arrow shaped), amplexicaul (leaf grasping stem) or auriclate (ear-shaped) and densely to sparsely covered with fine star-shaped hairs or sometimes hairless (Hitchcock and Cronquist 1973; Schultze-Motel 1986; Frankton and Mulligan 1987; Alex 1992; Stace 1997; Defelice 2001; Damgaard et al. 2008; Al-Shehbaz 2012). Flowers are small (2.5–8 mm across), initially in rounded clusters at the ends of stems and branches (Fig. 1B). Sepals are green or reddish (1.5–2 × 0.7–1 mm). Petals are white, rounded, and larger than the sepals, generally 2–4 × 1–1.5 mm (occasionally slightly narrower or wider, ranging to 5 mm). Stamens number six, with tetradynamous filaments (1–2 mm) and with a shorter style (< 0.8 mm). Flowers are present on a short, glabrous terminal raceme and pedicels, generally 0.5–1.5 cm long at maturity (Defelice 2001; Damgaard et al. 2008). Fruits (silicles) 2-valved, up to 3× as long as wide (4–10 × 3.4–8 mm), flattened at right angle to the stem, triangular to heart-shaped, with straight to slightly convex sides, base cuneate, apex emarginate or truncate, notched at the top, valves each with subparallel lateral veins, divided by a narrow septum (membranous partition) (Fig. 1C). Seeds numerous, up to about 32 per fruit, oblong, 0.8–1 mm long, orange-yellow to light brown, surface dull and punctured (Fig. 1C) (Schultze-Motel 1986; Frankton and Mulligan 1987; Hurka and Neuffer 1991; Alex 1992; Stace 1997; Al-Shehbaz 2012). Mucilage layer visible on seed surface when wetted (Swarbrick, 1971). Pollen grains are small (< 25 mm polar axis), isopolar, tricolpate, prolate spheroidal to prolate and are distinct from other genera in the Camelineae in having interruptions in the tectum that create the appearance of dimples on the pollen surface (Sagun and Auer 2017).

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.

(b) .

Distinguishing features

Capsella species are distinguished from other plants in the mustard family by their triangular or heart-shaped seed pods that have a narrow septum, or separating membrane, between the halves of the pod (Alex 1992). Refer to Hitchcock and Cronquist (1973) for a diagnostic key.

(c) .

Intraspecific variation

Capsella bursa-pastoris has been observed to have high intraspecific genetic, morphological, and phenological variability (Hurka and Neuffer 1991; Neuffer and Eschner 1995; Hurka and Neuffer 1997; Neuffer and Meyer-Walf 1996; Hawes et al. 2005; Neuffer et al. 2011; Wesse et al. 2021). However, no particular genetic, cytological, morphological, or phenological variants have been described within Canadian populations, although Wesse et al. (2021) incorporated Canadian accessions in their global analysis of variation in C. bursa-pastoris.

In Canada, a chromosome count of 2n = 32 is based on cytological specimens from Ontario, Saskatchewan, and British Columbia (Mulligan 1957, 1984; Taylor and Mulligan 1968) and 2n = 32 is given as the standard count in North America (Al-Shehbaz 2012) and Europe (Neuffer 1990; Slotte et al.2007). While counts of 2n = 16 have occasionally been reported, these counts most likely represent counts for Capsella rubella Reuter, which has extremely similar morphology (Neuffer 1990; Slotte et al.2007). However, C. rubella has not yet been documented as occurring in North America.

Shull (1909, 1929) examined and measured variations in leaf morphology and segregated them into two species and ten subspecies. Similarly, Almquist (1923, 1929) divided C. bursa-pastoris taxa into some 200 microspecies based mostly on small variations in fruit structure (Neuffer and Hurka 1986b; Aksoy et al. 1999). In the British Isles approximately 25 segregates have been recognized showing variations in leaf and fruit shape (Stace 1997). An analysis by Iannetta et al. (2007) of populations in the United Kingdom (UK) concluded leaf-shape was not associated with geographical distribution and only loosely with life-history traits but studies in other regions such as the Swiss Alps have shown stronger associations (e.g., Neuffer and Bartelheim 1989; Neuffer 1990). Analysis of the genetic structure of these UK accessions using inter simple sequence repeat (ISSR) markers showed a surprisingly large amount, almost 60%, of the genetic variation was attributed to individuals within an accession (Begg et al. 2012); this result is similar to more recent work by Wesse et al (2021) where 79% of the variation was found within populations in a regional analysis. Begg et al. (2012) also found three genetically differentiated clusters, the most defined of which was associated with the southern region, earlier flowering and increased seed production and reduced secondary dormancy, but not intensive cropping (Begg et al. 2012). Given the key role of rosette morphology in life history, Neuffer et al. (2018) examined the geographical distribution of four distinct rosette leaf types across the globe and their association with morphological, anatomical and physiological characteristics under different conditions. This revealed a complex pattern suggesting local adaptation of rosette characteristics overlaid with other factors such as genetic background.

Numerous studies have examined intraspecific variation in phenology in C. bursa-pastoris plants and its genetic basis. In general, researchers have found that there are ecotypes with differentiated flowering times that occur in areas with different temperature regimes whether as a result of latitude or elevation. For example, temperature-dependent variations in time to flowering and phenotypic plasticity were observed in wild populations along a transect from northern to southern Europe (Neuffer and Hurka 1986a). In the Swiss Alps, variations in such features as germination, flowering time and vegetative growth forms were correlated with altitude. Later flowering genotypes replaced earlier-flowering forms as elevation increased resulting in later flowering winter annual forms at high altitudes (Neuffer and Bartelheim 1989; Neuffer 1990). Similarly, California populations with early-flowering seem to have arisen from ancestral Spanish populations, while later-flowering populations in temperate North America have arisen from cooler, wetter northern European gene pools (Neuffer and Hurka 1999). Karley et al. (2008) also found the two flowering time variants in UK material and noted a strong, but negative correlation between flowering time and seed production, but none between seed production and reproductive duration. Therefore, Karley et al. (2008) concluded short flowering time combined with greater resource allocation to reproduction was the reason behind high fecundity (seed output). The genetic pathways that lead to these two flowering time variants were investigated in early flowering types obtained from Taiwan and late flowering types obtained from Sweden by Slotte et al. (2007). They found that the expression of two circadian genes, CCA1 and TOC1, and the modified function of the circadian clock function likely caused variation in flowering time, resulting in two extreme (early and late) flowering types. Linde et al. (2001) identified three quantitative trait loci (QTL) responsible for the onset of flowering. Given the likely linkage between flowering, rosette leaf development, and other factors (Linde et al. 2001), flowering induction is complex and more research is needed to elucidate the genetic pathway of flowering in C. bursa-pastoris. Overall the presence of both high dormancy/later flowering and low dormancy/earlier flowering appears to indicate a hedge betting strategy useful in variable environments.

An unusual heritable variant in floral morphology, first observed two centuries ago in Europe and described as Capsella apetala Opiz (Opiz 1821), is the recently rediscovered “decandric” or spermatogenesis-defective (spe) phenotype, in which all of the petals have been transformed into additional stamens (reviewed by Hintz et al. 2006; Hameister et al. 2009, 2013; Ziermann et al. 2009). A comparative study found that the flowers of the spe phenotype matured two weeks later in Germany, allowing stable coexistence with the wild type (Neuffer et al. 2020).

(d) .

Illustrations

The morphology of a mature C. bursa-pastoris plant, its basal and stem leaves, flower, seed pod and seed are shown in Fig. 1. Numerous photographic images are available online including:  http://ucjeps.berkeley.edu/eflora/eflora_display.php?tid=17109;  http://linnet.geog.ubc.ca/Atlas/Atlas.aspx?sciname=Capsella%20bursa-pastoris;  http://www.efloras.org/florataxon.aspx?flora_id=5&taxon_id=200009292;  https://www.brc.ac.uk/plantatlas/plant/capsella-bursa-pastoris;  https://www.calflora.org/cgi-bin/species_query.cgi?where-calrecnum=1472.

(a) .

Detrimental

Capsella bursa-pastoris was the 20th most abundant weed in residual weed surveys in western Canada during the 2000s (Leeson et al. 2005). It was found in 9.2% of fields, in densities as high as 140 plants·m⁻². It was most abundant in the Peace Lowland, Boreal Transition, Aspen Parkland and Fescue Grasslands ecoregions, and found in lower abundance in Interlake Plain, Moist Mixed Grassland and least in Mixed Grasslands and Lake Manitoba Plain. Globally, it is considered one of the most widespread plants on earth (Coquillat 1951; Zhou et al. 2001) and inevitably interferes with crop production, infesting winter cereals, horticultural crops, orchards, and forages (Aksoy et al. 1998).

Despite its observed frequency, research quantifying economic yield losses for C. bursa-pastoris alone has rarely been conducted. While it can contribute to yield losses of field crops in the Canadian Prairies, it is relatively non-competitive compared with other weeds in spring crops including cereals and canola (Welbank 1963). Capsella bursa-pastoris can cause serious yield losses in cole crops such as cabbage, broccoli, cauliflower or Brussel sprouts and in other horticultural crops such as onions because herbicides which control the weed would also cause crop injury (Freyman et al. 1992; Bitterlich et al. 1996; Dillard et al. 2004; Sikkema et al. 2007). However, it was less competitive than cultivated radish in pot experiments (Perera and Ayres 1992) and cabbage grown in narrow rows and in both narrow and wide rows with 10 cm planting intervals were unaffected by C. bursa-pastoris (Freyman et al. 1992). Due to its winter annual life cycle, however, C. bursa-pastoris is common in Canadian winter wheat fields. In a meta-analysis of herbicide trials conducted in Sweden, Milberg and Hallgren (2004) reported that C. bursa-pastoris was more economically detrimental in winter crops based on yield loss in cereal crops investigated in 1691 trials. They concluded that C. bursa-pastoris was one of the two worst weeds for autumn-sown cereal crops. Widespread infestation was also seen in Great Britain, where 23% of 2359 winter cereal fields were infested with C. bursa-pastoris (Marshall et al. 2003). Population densities of C. bursa-pastoris determined from barley and wheat fields over three seasons in New Zealand indicated a strong presence and high degree of competition with crops in their early developmental stages within fields undergoing normal crop management practices, including postemergence herbicide treatments (Bourdöt et al. 1998). In Denmark, the observed weed frequency of C. bursa-pastoris increased for spring barley, spring rape, winter rye and winter wheat in 2001–2004 compared with 1978–1989, but decreased in the multispecies assemblies of grass leys (Andreasen and Stryhn 2008). Capsella bursa-pastoris is generally a component of the common broadleaf weed assemblage for which a wide range of herbicides are available (see Section 11. Response to Herbicides and Other Chemicals).

A suspected nitrite poisoning of pigs in South Africa was attributed to consumption of C. bursa-pastoris (Wiese and Joubert 2001) and cattle grazing on a mixture of 40% C. bursa-pastoris and 60% Sisymbrium irio L., another member of the Brassicaceae, died from polioencephalomalacia, a neurologic disease of ruminants, as a result of the sulfur content of the plants (McKenzie et al. 2009). 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 remedy for treating ailments in livestock (see Section 3(b) Beneficial).

Populations of C. bursa-pastoris can pose a risk to crop health, production, and quality as it is a host to insect, nematode, fungal, viral and bacterial pests, including spore-forming bacilli (Iannetta et al. 2010; see Section 13. Response to Herbivory, Disease and Higher Plant Parasites).

(b) .

Beneficial

Because of its widespread availability C. bursa-pastoris has a long tradition of use as a potherb (a plant used in seasoning of food prepared by boiling in a pot) and in folk medicine in the majority of cultures around the world (Bussmann et al. 2019). Young leaves were cooked as greens or eaten raw as salad; seed pods were used as a peppery seasoning, seeds were dried and ground into meal, and roots were used as a ginger substitute. In Japan, the plant was an ingredient in a ceremonial barley–rice gruel (Facciola 1990; Defelice 2001) and it is eaten frequently in Korea, where its leaves and roots are consumed as vegetables (Lee et al. 2016). As a food plant, the species contains significant vitamins and minerals (Zennie and Ogzewalla 1977; Choi et al. 2014). However, an analysis of heavy metal content in wild food plants collected in an industrialized zone of Turkey showed higher than average levels of cobalt, lead, manganese, and iron in C. bursa-pastoris, placing it among plants hazardous to health if eaten in large quantities (Pehlivan et al. 2013).

Numerous medicinal properties ranging from analgesic to vermifuge (anti-parasite) have traditionally been attributed to extracts from the plant both for humans and livestock (Duke 2002), but it has primarily been associated with reducing internal or external bleeding. It has been used to staunch bleeding and to heal infected and bleeding wounds (Gerard 1633), and to treat such conditions as dysentery, bleeding, menstrual disorders and stomach problems, or as a diuretic (Defelice 2001; Kozub et al. 2012; Choi et al. 2014). Hartwell (1982) cited popular European sources dating to the medieval period on the use of infusions of C. bursa-pastoris to treat ulcers and cancers, including those of the stomach and uterus. Millspaugh (1974) indicated that the plant was used to treat diarrhoea in calves in England and its use was reported as folk-remedy for livestock in Switzerland (Bischoff et al. 2016). Based on these traditional uses, several studies have investigated C. bursa-pastoris or its extracts 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, isothiocyanate sulforaphane extracted from crucifers was shown to inhibit antibiotic-resistant strains of the bacterium Helicobacter pylori, associated with gastric ulcers and stomach cancer in tissue culture (Fahey et al. 2002).

Weeds such as C. bursa-pastoris play a role in maintaining biological diversity within crop fields (Storkey and Westbury 2007; Begg et al. 2012). For example, the species’ phenotypic and biochemical variability provides a heterogeneous resource for phloem-feeding aphids (Karley et al. 2008). Five insect families, 13 species, two of which are host specific, and three of which are pests, were associated with C. bursa-pastoris in winter cereal fields in Great Britain (Marshall et al. 2003). Capsella bursa-pastoris was also deemed important for 2–3 UK seed-feeding farmland birds and 11–25 invertebrates (Marshall et al. 2003). Andreasen and Stryhn (2008) suggest the increasing abundance of Brassicaceous weeds may improve food availability for birds and insects in arable lands.

Capsella bursa-pastoris extracts can be used as weed control against annual ryegrass and wild radish, though annual ryegrass is affected more (Seal et al. 2009). Extract concentrations of 5% or more were able to significantly inhibit growth for both aforementioned weeds, this includes root growth. A 400% concentrated extract was able to inhibit annual ryegrass shoot length and weight by more than 70% when grown in a tray filled with 50:50 sand:peat moss (Seal et al. 2009).

As an extremely abundant and widespread plant on the planet, C. bursa-pastoris is an important model organism for studies in a wide variety of areas including the evolutionary ecology of weeds (Nutt et al. 2006; Hintz et al. 2006; Choi et al. 2019; Žerdoner Čalasan et al. 2021) and genome evolution following hybridization and polyploidization (Hurka and Neuffer 1997; Slotte et al. 2007; Kasianov et al. 2017). Because it exhibits a wide range of genetic variation among populations, many studies have looked at patterns across its geographic range to examine the evolutionary mechanisms involved (Slotte et al. 2007; Neuffer 2011; Begg et al. 2012; Toorop et al. 2012).

(c) .

Legislation

In Canada, C. bursa-pastoris is not listed under either the federal Plant Protection Act or the Federal Weed Seeds Order 2016, under the Seed Act. After its removal from Alberta noxious weed legislation, Manitoba remains the only province that has continued to designate the species a noxious weed (Noxious Weeds Act, CCSM c. N110 2010). In the United States, C. bursa-pastoris is not listed on either federal or state noxious weeds lists; but has been reported as invasive in several states [Invasive Plant Atlas of the United States ( http://www.invasiveplantatlas.org/)].

(a) .

Climatic requirements

Capsella bursa-pastoris is adapted to a wide range of micro-climates around the world but is commonly found growing in cool and warm (subtropical) temperate regions, as indicated by its broad range in Canada where it grows in all provinces and territories (Aksoy et al. 1998; Defelice 2001; Fig. 2). However, the species is also well-adapted to drought conditions (see Section 7(a) Morphology). Its presence was recorded in the Nile valley where the average rainfall was 20 mm in spring and mean temperature near 27 °C in May. In Germany, it survives as a rosette over winter, when the temperature can be as low as −12 °C (Aksoy et al. 1998). Capsella bursa-pastoris is restricted to flat or gently sloped regions but is more common on south-facing slopes (Grime et al. 2014).

(b) .

Substratum

Capsella bursa-pastoris grows in various types of soils, however it grows predominantly on fertile-disturbed, clay to sandy loam soil (Aksoy et al. 1998; Defelice 2001; Grime et al. 2014). It can tolerate soil with pH 5–8 (Aksoy et al. 1998) but is absent from regions with a soil pH less than 5 (Grime et al. 2014). Aksoy et al. (1998) curated a list of soil types where C. bursa-pastoris has been recorded including: serpentine soils in southern Urals (Brooks 1987), loess soil in Lublin, Poland (Lipecki 1989), alkaline sandy loam soils found in the Nile Valley in Egypt (El-Habibi and Youssef 1981), calcium carbonate enriched sandy loam soil in Turkey (Aksoy and Gemici 1993) and wet humus-rich soil in Korea (Kang 1983). Capsella bursa-pastoris has also been recorded growing on soil contaminated by cadmium (Liu et al. 2015).

(c) .

Communities

Apart 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 of ruderal and disturbed communities wherever it occurs. This includes waste fields, demolition plots, manure piles, compost heaps, roadsides, and gravel parking lots (Alex and Switzer 1976; Aksoy et al. 1998). In Canada, it has been found in gardens, orchards, vineyards, pastures, meadows, and beaches (Canadian herbarium records). In the United States, the species, along with other winter annuals such as chickweed (Stellaria media L.), field pennycress, and henbit (Lamium amplexicaule L.) have been moving into crop areas (Hill et al. 2014). Within the United Kingdom, the species has been dominant in several vegetation communities: the chickweed–Capsella and the chickweed– nettle (Urtica urens L.) communities, and in the plantain (Plantago major L.) and bindweed [Fallopia convolvulus (L.) Á. Löve] – speedwell (Polygonum aviculare Poir.) subcommunities; and is a minor component of other communities of herbs including other crucifers such as field pennycress (Thlaspi arvense L.) and grasses, including meadow grass (Poa annua L.) and rye-grass (Lolium perenne L.) (Pigott et al. 2000); while in other parts of Europe it is among plant communities dominated by members of the Chenopodioideae such as Amaranthus and Chenopodium spp., and among such communities in alpine pine-spruce stands and in vineyards (Aksoy et al. 1998; Konstantinović and Blagojević 2014). The species is ubiquitous in Germany, along with other species in the above-mentioned communities (Hanzlik and Gerowitt 2012).

(a) .

Morphology

Capsella bursa-pastoris, like other ruderal species, is characterized by phenotypic plasticity and genetic adaptability across a range of traits including height, rosette size, floral biology, and seed and fruit morphology (Hurka and Benneweg 1979; Neuffer and Hoffrogge 2000; Neuffer 2011; Neuffer and Paetsch 2013). Several common garden experiments have revealed variation in height is driven by both genetic differentiation and phenotypic plasticity (Neuffer and Hurka 1986b; Neuffer and Alberts 1996; Neuffer and Hoffrogge 2000). It forms a rosette, an adaptation for overwintering, and cold responsive (COR) genes have been shown to be promoted with rosette leaves in response to cold temperatures (Lin et al. 2016). Similarly, variation in petal size is strongly influenced by temperature, with warmer temperatures promoting larger petal growth (Neuffer and Paetsch 2013). Prolific seed production enables widespread dispersal of C. bursa-pastoris and seeds produce a mucilaginous sheath upon hydration (myxospermy), which can enhance water absorption, particularly in dry soil (Deng et al. 2015) and has likely played a major role in long-term dispersal success of the species (Neuffer et al. 2011). Its deep tap root (up to 33 cm) enables it to access water at considerable depth, also contributing to its ability to withstand drought conditions (Johnson et al. 2011).

(b) .

Perennation

Capsella bursa-pastoris is a summer or winter annual. It reproduces by seeds only (Neuffer 1990; Aksoy et al. 1998).

(c) .

Physiology and biochemistry

Capsella bursa-pastoris is a C₃, facultative winter annual that may overwinter as a rosette or emerge very early in spring. Cici and Van Acker (2011) investigated the freezing tolerance/recovery of several winter annual species and reported that C. bursa-pastoris, had lower cold tolerance than narrow-leaved hawksbeard, (Crepis tectorum L.), stinkweed/field pennycress (Thlaspi arvense L.), and field violet (Viola arvensis Murr.), but similar cold tolerance to downy brome (Bromus tectorum L.) and common chickweed [Stellaria media (L.) Vill.]. Specifically, C. bursa-pastoris plants showed 50% freezing damage at −14 °C with freezing tolerance mediated by a 21-fold increase in proline levels. Wani et al. (2018) analyzed cold stress responses of 30-day-old seedlings by exposing them to 10 °C and collecting plant tissues at 24, 48, 72, 96 and 120 h. Results indicated that cold stress reduced photosynthesis, but that turgor and osmotic pressure were maintained by increased levels of soluble sugars, saturated, and unsaturated fatty acids (Wani et al. 2018).

The performance of C. bursa-pastoris has been evaluated under light, water, and nutrient stress (Aksoy et al. 1998). The plant grows in both open and shaded areas, though leaf lengths were shorter under light flux reduction compared with full sun. Capsella bursa-pastoris had the highest total dry weight when it was watered for 4 consecutive days out of 14, compared with treatments with fewer or more (2, 6, 8, or 10) consecutive watering days. Nutrient requirements were tested in sand cultures over a 14 h day. Calcium treatments ranging from 5 to 200 μg·mL⁻¹ increased total dry weight while calcium levels between 5 and 15 μg·mL⁻¹ resulted in the rosette leaves to curl, indicating deficiency. Fertilization with phosphorus resulted in maximum root and shoot dry weight when supplied at 16 μg·mL⁻¹. Nitrogen supplied at various concentrations increased total dry weight until 81 μg·mL⁻¹ but declined significantly at 243 μg·mL⁻¹. Potassium supplied at various concentrations increased total dry weight until 32 μg·mL⁻¹, and then declined (Aksoy et al. 1998). Fertilization with ammonium nitrate may cause injury, with retention of the solution enhanced by trichomes on C. bursa-pastoris leaves (Bitterlich and Upadhyaya 1990).

The average lipid content of C. bursa-pastoris seed is reported to be 30%, though higher lipid contents are observed in plants from temperate regions compared with those from colder regions. The fatty acid profile has a relatively large proportion of very long-chain fatty acids (> C₁₈) as is characteristic of seeds from the Brassicaceae (Mukherjee et al. 1984). Specifically, the fatty acid profile of C. bursa-pastoris seed is dominated by 25%–40% linolenic acid (C18:3), 20% linoleic acid (C18:2) and has noteworthy levels of polyunsaturated fatty acids icosadienoic (C20:2; 10%–20%) and icosatrienoic acids (C20:3; 5%–15%), but has little erucic acid (C22:1), often a major component of brassicaceous seeds (Mukherjee et al. 1984; Moser and Vaughn 2012; Al-Snafi 2015). The roots and the aerial portions of the plants also contain these fatty acids (Al-Snafi 2015; Grosso et al. 2011). The levels of flavonoids, organic acids, and sterols among other chemicals have also been assessed, including their relationship to light and temperature at places of origin (Eschmann-Grupe et al. 1990; Grosso et al. 2011).

(d) .

Phenology

In 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 in Britain where seeds germinate primarily at the beginning of March, with a small germination event after August. The first rosette leaves are produced 12–14 d after germination. If germinated early, the rosette continues to grow until the beginning of June, while the first shoot appears by the beginning of May. Flower formation is initiated 3–4 d after shoot development starts, ripe seeds and fruits appear at the end of May with seeds released from June on (Aksoy et al. 1998). The time required before the onset of flowering has been reported to vary widely for European populations of C. bursa-pastoris (see section Intraspecific Variation). Iannetta et al. (2007) reported that early flowering variants required 70 d to flower, while other variants required >130 d.

(e) .

Mycorrhiza

Traditionally, plants of the Brassicaceae family, and C. bursa-pastoris in particular, were thought to be non-mycorrhizal (Gerdeman 1968; Medve 1983). Demars and Boerner (1994, 1995) observed vesicular-arbuscular mycorrhizal fungi colonization of C. bursa-pastoris in plants grown alone, and a greater level of colonization in plants grown in a grass matrix. However, this does not necessarily mean that C. bursa-pastoris is mycorrhizal, as it could mean that the mycorrhizae were attacking senescent roots. Alternatively, colonization did occur but only on a sporadic basis with the mycorrhizae mainly colonizing the grass species. Populations were sampled from both lawn and waste area habitats. Fungal colonization was significantly higher in lawn habitats, most likely due to the presence of strongly mycorrhizal plants. Internal hyphae, vesicles, chlamydospores and extramatrical hyphae were found from C. bursa-pastoris root segments investigated, but no arbuscles (Demars and Boerner 1994). Chawla et al. (2011) found arbuscules and extramatrical hyphae but no vesicular structures from populations in India and concluded C. bursa-pastoris may aid in maintaining mycorrhizal inoculum in the soil during winter.

(a) .

Floral biology

Capsella bursa-pastoris is self-compatible and primarily self-pollinating (autogamous), the extent to which varies with environmental conditions and other interactions. Nearly exclusive self-pollination occurs when the atmospheric humidity is high, temperature is over 15 °C and light intensity is low. Outcrossing is favoured under dry, sunny conditions (Hurka et al. 1976) with up to 10% outcrossing recorded under field conditions (Hurka et al. 1989). Sterile fruits are produced under extremely cold or hot conditions and this has been attributed to the failure of the anthers opening. Compared with self-incompatible Capsella species such as C. grandiflora, C. bursa-pastoris has smaller petals, lower pollen production, shorter styles and more rapid fertilization after pollination from compatible pollen (Hurka et al. 1976; Neuffer and Paetsch 2013). Examples of flower insect visitors included hoverflies (Syrphidae), bees (Apidae), beetles (Coleoptera) and thrips (Thysanoptera) for a population studied in Germany (Ziermann et al. 2009). The unique spe floral type where petals are replaced by stamens tends to attract hoverflies rather than bees as typical of the wild type (Neuffer et al. 2020). Homeotic mutants with stamenoid petals found close to Mainz, Germany exhibited half the number of insect visitations and no emission of volatile monoterpenes and benzenoids compared with wild type plants. Both the mutant and wild type plants attracted the same types of visitors (Ziermann et al. 2009). Day-length influences the onset of flowering time; C. bursa-pastoris behaves as a facultative long-day plant (Hurka et al. 1976).

(b) .

Seed production and dispersal

Capsella bursa-pastoris is a prolific seed producer, but production per plant is highly variable. Hurka and Neuffer (1991) reported seed production from individuals from seven European populations ranging from 100 to 91 000 seeds plant⁻¹. Hill et al. (2014) reported seed production from naturally occurring stands at 800 to 40 000 seed m⁻² from 40 to 230 plants·m⁻². Individual plant seed production ranged from a minimum of 5000 to a maximum of 90 000 seeds in a German study (Hurka and Haase 1982). Seed production per plant was increased by fertilization, and linked to increased branching (Yang 2018). The seed is 1 mm long and weighs approximately 0.1 mg on average but is highly variable. Seed weights reported for a variety of environments are relatively consistent. Mukherjee et al. (1984) reported seed weights from 0.093–0.156 g per 1000 seeds for material collected from a variety of elevations (10 to 2400 m) and latitudes (36 to 69 °N). Similarly, Werle et al. (2014) reported weights of 0.0110 ± 0.0001 and 0.0108 ± 0.0002 g per 100 seeds in two different years (2010 and 2011) from a farm field in Nebraska, USA, and Benvenuti (2007) reported 0.092 ± 0.071 per 1000 seeds from farm fields in Asciano, Italy. Seed size affects the germination rate and hypocotyl length of seedlings, with hypocotyl length longer in seedlings from larger seeds (Hurka and Benneweg 1979). Seed count varies from 10 to 40 seeds per fruit. Seeds are dormant at the time of dispersal. When the seed pod is ripe, it opens along its septa, but the seeds are not released immediately, lengthening the time over which seeds disperse and seedlings emerge (Hurka and Haase 1982). The small spherical, smooth seeds disperse unassisted within 50 cm of the parent plant (Aksoy et al. 1998), while for wind-aided dispersal, 80% of seed fell within 50 cm but 20% was scattered between 50 and 105 cm. The size and shape of the seed increases the probability of seed burial, even in the absence of tillage (Benvenuti 2007). It was observed the seeds were equally distributed in the first 10 cm of the soil, after which the frequency declined. No seeds were observed at 40 cm soil depth; this was attributed to the soil conditions at the field station (Hurka and Haase 1982). The mucilaginous sheath around the seed may enable long-distance dispersal by facilitating attachment to animals, vehicles, and people. Earthworms (Lumbricus terrestris L.) ingest the seeds and release them in their casts. This contributes to short-distance vertical dispersion and germination (Hurka and Haase 1982).

(c) .

Seed banks, seed viability and germination

Capsella bursa-pastoris has a persistent seed bank that can vary in size. Hurka and Neuffer (1991) reported a broad range of seed banks, from 500 to 300 000 seed m⁻² in various German environments. Sanderson et al. (2014) reported seed banks (as determined by germinable seeds) in organic dairy hay, permanent and recently established pastures at between 11 to 8580 seed·m⁻². In cotton–tomato rotations in California, seed banks ranged between 8 and 1220 seed·m⁻², with the highest seed bank exhibited in conservation tillage treatments with cover crops (Shrestha et al. 2015). Larger seed banks may be favored by a lack of soil disturbance, as viable seeds survive longer in undisturbed soil than in cultivated soil. In experiments conducted in the United Kingdom, C. bursa-pastoris seed was buried in disturbed and undisturbed soil and seed emergence and viability monitored over 6 years (Roberts and Feast 1973). In cultivated soil, they recorded 18% and 12% emergence in the first and second years, with a total of 46% emergence over the 6 years of the study and 4% of the seeds remaining viable in the soil. In uncultivated soil the emergence rates were lower, 5% and 1% in the first and second years and 12% total emergence over the 6 years, however 23% of the seeds remained viable in the seed bank. Similarly, Kivilaan and Bandurski (1981) reported that C. bursa-pastoris remained viable in Dr. Beal’s Alaska seed viability experiment for >35 yr, while Conn and Deck (1995) reported that seed germination declined from an initial 48% germination rate to 42, 42, 30, 9 and <1% after 2.7, 3.7, 4.7, 6.7 and 9.7 years, respectively. However, after this initial sharp decline in germination rate, seeds showed long-term persistence with viability remaining at a constant low level to 24.7 years. Specifically, viability for C. bursa-pastoris was 1.3% at 19.7 yr and 2.8% at 24.7 yr and further, unlike the majority of species tested, over a third of the seed still exhibited dormancy after 24.7 yr (Conn and Werdin-Pfisterer 2010). Baskin and Baskin (2006) combined data from the Duvel experiment, which lasted 39 yr and the Beal experiment which lasted 120 yr and suggested C. bursa-pastoris seeds can remain viable in the soil after 39–40 yr. However, the seed half-life according to Roberts and Feast (1973) is 5 yr which is further reduced to 1 yr if the soil is annually disturbed through cultivation (Aksoy et al. 1998). This suggests that in the absence of seed bank replacement, seed banks decrease more rapidly in cultivated soils, while C. bursa-pastoris can persist longer in wastelands, rights-of-way, and perennial crops.

Temperature alters germination success with low temperatures inhibiting germination and growth (Wani et al. 2018). Seed germination of populations from Scandinavia, the European Alps and the Middle East was tested in growth chambers and greenhouses under five to seven different temperature treatments, showing a trend in greater germination with increased temperature (Neuffer and Hurka 1988). Neuffer and Hurka (1988) also observed that seed age influenced both germination capacity, the proportion of seed that germinated, and germination rate, the time taken for 50% of the seeds to germinate, with decreased germination with seed age. Seed dormancy level also influences germination timing (Neuffer and Hurka 1988; Toorop et al. 2012). Germination occurred from 10–30 °C, while soil pH ranged from 3 to 11 for seeds collected from a wheat field from Qarakheyl Crop Research Station, Iran (Rezvani et al. 2014). At 30 °C, the greatest germination rate was obtained under a 12/12-h light/dark treatment. In another study conducted in the Nile delta, the highest germination rates were obtained at 30–35 °C (Rayia et al. 2020).

Germination rates, seedling fresh mass, fresh root length and other traits indicative of germination and establishment were found to be higher when the plants were germinated in the presence of nematodes (Roberts et al. 2018).

In Canada, C. bursa-pastoris is a facultative winter annual with two distinct emergence peaks in late summer/fall and in spring. Cici and Van Acker (2009) reported that in Ontario, seeds from seedlings that emerged in August flowered in early spring (mid-April) and seeds from seedlings that emerged in spring flowered in May. In a Michigan study, seed maturity, expressed as 50% of seed release from the plant, occurred by 31 May and 28 May for 840 and 920 growing degree days (GDD), with a base temperature of 0 °C, in 2009 and 2010, respectively (Hill et al. 2014).

Dormancy triggers (release and re-entry) and germination triggers are an ecological adaptation mechanism that prevents germination under conditions unfavourable for survival of C. bursa-pastoris. Freshly harvested seed is almost completely dormant (primary dormancy) (Popay and Roberts 1970a; Baskin et al. 2004; Hill et al. 2014) and not all seed is released from dormancy in one year. After release from primary dormancy un-germinated seed may become conditionally dormant, depending on environmental conditions. Seed dormancy, both primary and (or) conditional, must be minimal to allow for seed germination. Baskin and Baskin (1989) reported that C. bursa-pastoris seed freshly harvested (dormant) in May became non-dormant (after-ripening) and capable of germinating after being exposed to high temperatures (25/15 to 35/20 °C day/night temperatures). Seeds that fail to germinate in fall or become conditionally dormant at 5 °C germinate in spring. Baskin et al. (2004) reported that seed collected from spring and fall germinated plants grown at high latitudes was dormant and neither was capable of germination in the fall, but rather it was only possible in spring the following year.

In the case of a small seeded species, depth of seed placement can be critical. Popay and Roberts (1970b) reported C. bursa-pastoris germination is influenced by light (red light stimulation), increased temperature, fluctuations between cool and warm temperatures, carbon dioxide (anoxia), soil nitrate and nitrite concentration, all of which could be influenced by depth of seed placement or by tillage. Under field conditions, Cici and Van Acker (2009) reported the primary microsite conditions; temperature, moisture and light were modified by CO₂, nitrate, and nitrite concentrations. Optimal soil depths are reported to be < 2 cm.

In agricultural systems C. bursa-pastoris co-evolved with crops and predictable periodic disturbance (by tillage and/or herbicide). Annuals respond to the environment via dormancy/release, germination, and phenotypic plasticity to avoid disturbance, and successfully produce seed. Predictable emergence patterns may be useful for guiding the timing of weed control (Cici and Van Acker 2009). Werle et al. (2014) planted seeds of C. bursa-pastoris in July at four sites over two years in Nebraska and measured emergence for one year. For C. bursa-pastoris 30% emerged in fall with a further 70% emerging in late winter and spring. Soil temperature was the most useful parameter in modeling emergence, although soil moisture was necessary for germination. The time of emergence of the maternal plant may affect the seed germination and morphology of the seed and plant. Van Acker and Cici (2012) reported that spring emerging plants produced seed that germinated faster, flowered earlier, and resulted in differential allocation of biomass to roots and reproductive tissue.

(d) .

Vegetative reproduction

This species does not reproduce vegetatively.

(a) .

Herbivory

(b) .

Diseases

(c) .

Higher plant parasites

Capsella bursa-pastoris is host of the field cow-wheat, Melampyrum arvense L., a hemi-parasite which attaches itself by haustoria to the roots of the host plant to obtain additional moisture and nutrients (Lechowski 1995). There are unconfirmed data from Bulgarian floras that Capsella is a host of the parasitic species Orobanche nana Noë (Stoyanov 2005). A greenhouse study done in Dijon, France showed that Phelipanche ramosa (L.) Pomel, a parasitic plant, had a low number of successful infections relative to other species in the study (Moreau et al. 2016).