Noxious Alien Plant Species Bidens pilosa: History
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Contributor:
Hisashi Kato-Noguchi
,
Denny Kurniadie

Bidens pilosa L., belonging to the Asteraceae family, is an annual (or biennial) herbaceous plant. The species grows 20–180 cm tall, and the stems are quadrangular with hairy straggling branches. It has alternate leaves with 3–5 pinnate leaflets, which are supported by a petiole (10–70 mm long). The leaflets are broadly ovate, serrate, and 30–70 mm long and 12–18 mm wide. Capitula occur at the end of the main stems and lateral branches and expand 5–12 mm in diameter. Capitula consist of 0–8 ray florets and 35–55 disk florets. The corollas of the ray florets are 7–15 mm long and white–yellow. The ray florets have poorly developed pistils and lack stamens. The disk florets have 3–5 mm long yellow corollas, five stamens, and well-developed 2–3 mm long pistils. Its fruits are black liner cypselae with 2–5 stiff awns of 2–4 mm long. The species often forms thick monospecific stands. 

  • adaptation
  • allelopathy
  • asynchronous germination
  • defense function
  • flowering phenology
  • heteromorphic seed
  • natural enemy

1. Impacts of B. pilosa

B. pilosa has the potential to rapidly grow and to form dense thickets. The species outcompetes crops in agricultural fields and eliminates indigenous plant species in introduced ranges by expanding the margins of its dense thickets [1][2][3][4][5][6]. B. pilosa was reported to replace the indigenous plant species of islands such as Panicum fauriei Hitcc. and Scaevola coriacea Nutt. on Hawaii [7], and Salvia pleberia R.Br. on Iriomote Island, Japan [8] (Figure 1).
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Figure 1. Monospecific stands of B. pilosa. The pictures were taken by the authors.
B. pilosa infestation suppressed the growth of sugarcane (Saccharum officinarum L.) by 40% on day 60 and 80% on day 120 after sugarcane planting under field conditions in Okinawa, Japan, and caused 80% of the final production losses [9]. The species infestation reduced the production of a bean (Phaseolus vulgaris L.) by 48% in Uganda and by 18–48% in Peru [1]. The growth of this bean showed a significant negative correlation with the density of B. pilosa [10][11]. The species, at a density of 1.85 plants per m2, caused the bean yield to reduce by 18%, while 10 plants per m2 caused a reduction by 48% [12]. When B. pilosa and soybean (Glycine max (L.) Merr.) were grown together under field conditions, B. pilosa showed a higher relative growth rate than soybean and suppressed soybean’s vegetative growth and seed production [13]. A density of one and four plants of B. pilosa per m2, respectively, caused a soybean yield loss of 9.4% and 28% [2]. The contamination of the cypselae of B. pilosa also spoiled the quality of the crop grains [2]. When B. pilosa was germinated and grown with 16 crop plant species under different fertilizer and disturbance gradients under field conditions, B. pilosa showed a high competitive ability against crop plants from the families of Poaceae, Begoniaceae, Solanaceae, Balsaminaceae, Caryophyllaceae, and Convolvulaceae [6]. The stiff awns of its cypselae also irritate people and livestock [1][2]. Observations suggest that the infestation of B. pilosa causes a reduction in crop production and quality.
B. pilosa is also involved in the transmission of pathogens to agricultural crop plants as a vector. Sonchus yellow net virus was transmitted from B. pilosa to Nicotiana glutinosa L., Nicotiana clevelandii A.Gray, Zinnia elegans Jacq., and lettuce (Lactuca sativa L.) through the medium of the aphid (Hyperomyzus lactuae L.) [14][15]. B. pilosa has the potential to serve as a vector for tomato spotted wilt virus, which causes the typical tospovirus symptoms of chlorotic ringspots and necrosis on both young and older leaves of tomato (Lycopersicon esculentum Mill.) [16]. However, the movement of the virus between B. pilosa and tomato remains unknown. The papaya mealybug Paracoccus marginatus Williams & Granara de Willink, which is native to tropical America, was detected in South Asia, and B. pilosa was a host plant of the mealybug and transmitted it to other plant species [17]. The involvement of B. pilosa in the transmission of pathogens and insects may reduce the agricultural crop production.
As described in this section, the impacts of B. pilosa infestation on agricultural crop production were documented in several publications. However, its impacts on native plants and indigenous ecosystem are limited.

2. Fast Growth

B. pilosa established dense stands 50–135 days after its germination. The species starts flowering four–eight weeks after germination and produces mature seeds two–four weeks after flowering [18][19]. Regarding the population of the species in its favorite conditions, B. pilosa flowers throughout the year and makes up to four generations annually [1][2][20]. B. pilosa showed a higher growth rate, leaf area, and biomass than two indigenous congeners, Bidens bripartit (Lour.) Merr. & Sherff and Bidens tripartita L., under field conditions in China [21]. B. pilosa also showed more efficient utilization of water, photosynthetic fixed carbon, and nitrogen than the indigenous Cirsium setosum (Willd.) M. Bieb [22]. B. pilosa was reported to regenerate from remaining stems after cutting the above-ground parts of the plants [8]. These observations suggest that B. pilosa rapidly grows, establishes dense stands soon after germination, and produces several generations in a year.

3. Reproduction

The species produces about 80 capitula on long peduncles arising from the apexes of the stems and the leaf axils. A single capitulum contains ray and disk florets, as explained in the Introduction. The ray florets are sterile but serve as a nectar guide for pollinators. A nectary gland is present at the base of the style of disk florets [20]. The fertilized disk florets produce single-seeded black cypselae within four weeks [1][2][3][23]. Each plant produces 2000–6000 cypselae during its life cycles [1][2][24]. The species produces two types of cypselae within the same capitulum: long cypselae (8–10 mm in length) and short cypselae (3–7 mm). The production rate of the long and short cypselae was 64% and 36%, respectively [20][25]. Relatively young plants produced more long cypselae, and senescent plants produced more short cypselae [25][26]. Both types of cypselae have 2–5 stiff awns 2–4 mm long and can be easily dispersed by the attachment of the awns to animals, birds, and human clothes or by wind and water [20][24]. The seeds in cypselae remain viable for 5–6 years [2] (Figure 2).
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Figure 2. Capitulum and cypselae of B. pilosa. The pictures were taken by the authors.
Long cypselae have thin seed coats compared with short cypselae. Long cypselae germinated soon after their dispersion under a wide range of conditions, while short cypselae showed dormancy and germinated only under favorable conditions, such as adequate moisture and temperature, for the subsequent growth of seedlings [20][26][27]. The germination of short cypselae was stimulated by red light and gibberellin application [27], which indicates phytochrome involvement in the germination. Long cypselae showed no light sensitivity and germinated in both light and dark conditions [26]. Long cypselae produced three–four generations in a year due to their quick germination after dispersion, while short cypselae germinated in subsequent years due to their dormancy [20]. Long cypselae contribute to the species by continuously increasing the population, while short cypselae contribute to the species by remaining in reserve for the population [20][28].
The B. pilosa population also shows two phenological types of flowering–fruiting events during the growing season. Less than 10% of the population of the species flower one–two months after germination (early type), and the others flower four months after germination (normal type). Normal-type plants grow larger than early-type plants, and early-type plants produce fewer and heavier seeds than normal-type plants. The seeds from early-type plants more quickly germinate than those of normal-type plants, and both seeds do not show dormancy. The different flowering phenology affects seed mass and production and germination. However, the seeds from both types of plants produce early-type and normal-type offspring. Therefore, the flowering–fruiting events of their offspring are not affected by the parental types [29]. Early-type plants may contribute to the species quickly expanding because of their quick growth and flowering–fruiting. Normal-type plants may contribute to the species by stably increasing the population and/or maintaining the population.
The germination behavior of plants affects plant fitness and persistence. Invasive plant species often show earlier and/or rapid germination and asynchronous germination. The production of different biotypes of seeds by a single plant is also one of the characteristics of invasive plant species [30][31][32][33]. Early-germinating species and rapidly germinating species may benefit from less competition with other plant species for resources and niches [34][35]. These species enable the suppression of the germination and establishment of later-germinating species [32][33][36]. However, early and rapid germination is a risky strategy under unpredictable environmental conditions, especially in the early growing season, and often increases seedling mortality in such conditions [32][37][38]. Asynchronous germination may be more beneficial to the rapid expansion of species under relatively stable conditions and to the persistence and survival of species under unpredictable environmental conditions, regarded as a significant characteristic of invasive species to expand their ecological niches and population [31][39].
B. pilosa produced a great number of cypselae during its life cycle, different biotypes of cypselae such as long cypselae and short cypselae [20][24][26][27], and different phenological types of flowering–fruiting events such as the early-type flower and normal-type flower [29]. The asynchronous germination of B. pilosa is a strategy in which one of the seeds’ subsets may successfully germinate and establish itself at different times and under different conditions, providing the chance to survive and colonize in new habitats. Therefore, B. pilosa may be able to survive as a widespread invasive species in different habitats and to expand its distribution in introduced ranges.
In addition, B. pilosa showed different breeding systems at a variety of levels within the species. B. pilosa var. minor and B. pilosa var. pilosa produced 89% and 74% of seeds, respectively, compared to the corresponding open-pollinated capitula, although 73% of the seeds were set in open-pollinated capitula [16][40]. This observation suggested that B. pilosa var. radiata is highly self-incompatible, whereas the other two are self-compatible. Therefore, B. pliosa showed different breeding systems at a variety of levels within the species. The invasiveness of B. pilosa var. radiata was observed to be higher than that of B. pilosa var. minor and var. pilosa. When solar irradiation is high, B. pilosa var. radiata allocates more biomass to axillary shoots than the other two varieties, contributing to the expansion of the varieties [41]. Xenogamy enables the species to increase its genetic diversity, which favors its establishment in heterogenous and variable environments [20].

4. Adaptation

B. pilosa grows best in areas with full sunlight, a mean annual temperature between 25 °C and 38 °C, and annual rainfall between 500 mm and 3500 mm. It can grow in a wide range of soil types including sand and lime soil with a pH ranging from 4 to 9 and salinity up to 100 mM NaCl. The species tolerates frost, and the regeneration of its roots occurs after temperatures as low as −15 °C [1][2]. The species benefits from disturbances such as fire and soil tillage and quickly infests after a disturbance [4][42].
Under resource-limiting conditions, some invasive plant species can outcompete indigenous plant species either by efficient resource uptaking or by a lower resource requirement, called the resource conservative strategy [43]. The carbon (C), nitrogen (N), and phosphorus (P) contents in plant tissues and their ratios such as N:P and C:P reflect the use and adjustment of the available nutrients and the relative growth rate of the plants [44][45][46]. Lower N:P and C:P ratios in plant tissues indicate a higher P content in the whole plants and the stimulation of protein synthesis, resulting in higher growth and reproductive output [44]. A higher C:N ratio indicates higher C assimilation and lower nutrient requirements [46]. B. pilosa under low-nutrient conditions showed a higher C:N ratio in the roots, indicating a lower nutrient requirement and higher C assimilation, adapting a resource conservative strategy. B. pilosa under high-nutrient conditions showed lower N:P and C:P ratios in the roots, indicating higher protein synthesis, growth, and reproductive output [47]. When maize (Zea mays, L.) and B. pilosa grew together under field conditions, the C:N, C:P, C:K, N:P, and N:P ratios in B. pilosa significantly increased, while those ratios in maize changed a little, which indicates that B. pilosa has a distinct survival strategy under nutrient-competitive conditions, and is able to more efficiently use nutrients [48]. Therefore, B. pilosa may apply a competitive strategy in nutrient-rich environments and a resource conservative strategy in resource-poor environments.
B. pilosa showed a similar plant height as the indigenous plant species B. biternata (Lour.) Merr. & Sherff and B. tripartita L. under unfavorable light and moisture conditions. However, B. pilosa showed a greater plant height, biomass, and growth rate than both indigenous species under favorable light and moisture conditions. B. pilosa allocated more resources to the root biomass under a high-light condition and to the leaf biomass under a low-light condition [21]. When B. pilosa and Bidens biternata were grown in the conditions of different light intensities (40% and 10% sunlight) for 64 days, B. pilosa showed a higher leaf mass, a higher total leaf area, and increased photosynthesis than B. biternata [49]. These observations suggest that B. pilosa has a higher adaptative ability and a higher phenotypic plasticity than B. biternata and B. tripartita under low-light and low-moisture conditions, which may contribute to the invasiveness of B. pilosa.
Extreme precipitation often causes short-term waterlogging conditions for terrestrial plants, which cause hypoxia and serious damage to the plants’ root systems [50][51]. Short-term waterlogging stimulated adventitious root generation and higher dehydrogenase activity in the roots of B. pilosa [52][53], which is the adaptive response to the hypoxic condition [50][51]. The reduction in the photosynthesis and growth rate of B. pilosa under waterlogging conditions was significantly less than that of an indigenous species, B. biternata [53]. Therefore, B. pilosa may tolerate waterlogging conditions better than the indigenous species B. biternata.
The seeds of B. pilosa were collected from three different locations in China. Those seeds germinated at a temperature between 10 °C and 30 °C. The seeds lost viability after 8 days of continuous heating at 40 °C or 30 min heating at 50 °C. However, the intraspecific variation for high-temperature tolerance was found among seeds from different collection sites [54]. The germination requirements for temperature and water also significantly differed among seeds from different collection sites [55]. Seeds obtained from nine locations in Brazil showed 20–97% germination rates at a temperature of 10 °C–35 °C. The seed weight and the rates of germination and dormant seeds significantly varied among collection locations [56]. The germination rate of B. pilosa was higher with seeds buried in shallow soil than deep soil, and the seed dormancy was greater with deeper soil than shallow soil [57][58]. Therefore, the population of B. pilosa from different locations showed different tolerance and requirements for germination such as temperature and water and the different ratios of dormant seeds. The variation in the water requirement, temperature tolerance, and dormancy among seeds from different locations may be involved in the adaptation of B. pilosa to local conditions.
These observations suggest that the acclimation ability of B. pilosa to various environmental conditions such as soil fertility, temperature, and solar radiation is high. It also adapts to waterlogging conditions.

This entry is adapted from the peer-reviewed paper 10.3390/plants13030356

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