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Kato-Noguchi, H. Invasive Mechanisms of Mimosa pigra. Encyclopedia. Available online: https://encyclopedia.pub/entry/44355 (accessed on 17 September 2024).
Kato-Noguchi H. Invasive Mechanisms of Mimosa pigra. Encyclopedia. Available at: https://encyclopedia.pub/entry/44355. Accessed September 17, 2024.
Kato-Noguchi, Hisashi. "Invasive Mechanisms of Mimosa pigra" Encyclopedia, https://encyclopedia.pub/entry/44355 (accessed September 17, 2024).
Kato-Noguchi, H. (2023, May 16). Invasive Mechanisms of Mimosa pigra. In Encyclopedia. https://encyclopedia.pub/entry/44355
Kato-Noguchi, Hisashi. "Invasive Mechanisms of Mimosa pigra." Encyclopedia. Web. 16 May, 2023.
Invasive Mechanisms of Mimosa pigra
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Mimosa pigra is native to Tropical America, and it has naturalized in many other countries especially in Australia, Eastern and Southern Africa and South Asia. The species is listed in the top 100 of the world’s worst invasive alien species and is listed as Least Concern in the IUCN Red List of Threatened Species. M. pigra forms very large monospecific stands in a wet–dry tropical climate with conditions such as floodplains, riverbanks, grasslands, forests and agricultural fields.

allelopathy biological control monospecific stand mutualism

1. Reproduction and Growth

M. pigra is a fast-growing species, and it is capable of reaching reproductive maturity within 6–8 months [1][2][3][4][5]. Round flower heads (1–2 cm in diameter; mauve or pink) arise from actively growing young shoots, which contain approximately 100 flowers. Each flower head generates 1–30 seed pods. Pods are 3–8 cm in length and are covered with dense stiff hair (Figure 1). Each pod contains oblong-shaped 8–20 seeds (4–5 mm long, 2 mm wide) [1][2][5]. The species flowers throughout the year in Sri Lanka and Queensland, Australia, and during spring to autumn in the Northern Territory of Australia, which may be dependent on climate conditions [2][3][4]. Flowers are pollinated by mostly self-fertilization and sometimes by bee or wind [1]. The seeds take about five to nine weeks for the maturation after the flower-bud formation [2][5] (Figure 1).
Figure 1. Mimosa pigra flowers and pods.
Annual seed production was estimated to be up to 220,000 seeds per plant [5][6], and 9000–12,000 per m2 [7]. Top soil under the canopy contained 2000 to 45,000 seeds per m2 [3][7][8]. The wind dispersion of the seeds occurs a relatively short distance from the plants. The long-distance dispersion of the seeds occurs through the adhesion of the pod’s stiff hair onto animals and agricultural vehicles and through the floating of the pods on water streams and flooded waters [8].
The seeds germinate when they are first wetted, and the rate of the germination is 75–94% [9]. The half-life of viable seeds in seed banks in field conditions is 9–99 weeks, which is dependent on the soil types and conditions [7][10]. The seed coats are very hard and impermeable and some of seeds have remained dormant in the soil for up to 26 years [5][11]. Ten years after the complete clearance of 250 ha of a M. pigra stand, its 109 seedlings per m2 still remained to emerge from the seed banks [11]. Sand scarification of the seeds increased the germination [3], indicating that the movements of the seeds by water stream and flooding may stimulate the germination.
The species grows at a rate of 1.1 cm in height per day during the first 90 days after germination and grows ca. 2.5 cm and ca. 7.5 cm in the stem diameter in the first year and the second year, respectively [1][2][12][13]. The species forms impenetrable dense monospecific stands (3–6 m in high) and the stands expand 76 m per year in wetlands [8]. It was recorded that the infested areas of the active stands doubled in 1 year and on average every 6 years in the Northern Territory of Australia [5][8]. The coverage of M. pigra in the monospecific stands was 96.3% and the biomass was estimated to be 35–45 tons dry weight per ha in the Adelaide River floodplain and the Finniss River catchment in Australia [14][15].
The species also regenerates from the remaining trumps after clearance of the above-ground parts of the trees [9]. Substantial numbers of the plants regrow from the base of stems after fire burning and the fire stimulates its germination in the seed banks [16]. The regrowth from the young stubble can reach 2.5 m in height and can cover 6.3 m2 within 12 weeks [13].
The characteristics of life history such as the high reproduction and high growth rate are important for the invasiveness and naturalization of invasive plants [17][18][19][20]. The observations described in this section suggest that M. pigra has the ability of rapid growth through its vegetative phase to flowering, self-compatibility, high seed output, high rate of germination, great longevity of seeds and regrowth from the stubbles (Table 1). These characteristics may contribute the invasion and naturalization of the species in invasive ranges.

2. Adaptivity and Plasticity

The species is found in tropical regions where annual rainfall level is between 750 mm and 2200 mm. It can grow around water bodies even when the annual rainfall is less than 750 mm [2]. M. pigra grows well in soil ranging from black cracking clays, sandy clays and siliceous river sand, although the species can grow in any type of soil [1][6]. It is found at an altitude of ca. 500 m above sea levels [12]. M. pigra has shown phenotypic plasticity in response to abiotic and biotic stress conditions such as available water level and intraspecific competition [21]. The genetic variation and structure of the M. pigra population in Thailand is high [22]. The characteristics of phenotypic plasticity of the plants are important for the naturalization of invasive plants into non-native ranges [17][18][19][20][21]. However, information is limited to discuss the phenotypic plasticity of M. pigra in different environmental conditions.

3. Natural Enemy

Long-term investigations from 1979 in the native ranges of M. pigra such as in Central and South America and in Mexico have shown that over 400 phytophagous insects, consisting of 61 families in 5 orders, are the natural enemies of M. pigra. The largest family is Coleoptera (59%), followed by Hemiptera (23%) and Lepidoptera (17%) [23][24]. Among them, for example, a stem-boring moth Carmenta mimosa Eichilin and Passoa (Lepidoptera) caused a 90% reduction in the seed production of M. pigra, and a weevil Coelocephalapion pigrae Kissinger (Coleoptera) rapidly colonized the M. pigra stands and fed on their leaves [25][26].
Pathogenic fungi: Mycosphaerella mimosae-pigrae H. C. Evans, G. Carrión and Ruiz-Belin; Sphaerulina mimosae-pigrae H. C. Evans and G. Carrión; Diabole cubensis Arthur and J. R. Johnst.; and Microstroma ruizii-belinii H. C. Evans, G. Carrión and Ruiz-Belin were found to infect M. pigra along the Pacific Coast of Mexico, and Sphaerulina mimosae-pigrae and Diabole cubensis occurred along the Caribbean Coast [27][28]. Phloeospora momosa-pigrae H. C. Evans and G. Carrión and Diabole cubensis selectively infected M. pigra in Mexico [5][27]. Some of those natural enemies were selected as the biological control agents for M. pigra, which were described in Section 3.3.
The interactions of the invasive plants with natural enemies are very critical for the naturalization of the invasive plants [17][18][19][20][21]. A great number of herbivore insects and fungal pathogens have been identified in M. pigra stands in the native ranges described above. However, very few natural enemies were found in Australia [29]. Having few natural enemies may contribute to the superior growth rate and naturalization of M. pigra in invasive ranges (Table 1).

4. Mutualism

Plant species belongs to Mimosa genus nodulate generally with the member of the Betaproteobacteria (β-rhizobia or β-proteobacteria), which includes the genera of Cupriavidus, Burkholderia, Paraburkholderia and Trinickia [30][31]. The species of Burkholderia was the main symbiosis rhizobia for M. pigra, followed by the species of Cupriavidus in South and Central America and in Taiwan [32][33][34]. Among 191 rhizobia isolated from the root nodules from three separated populations of M. pigra in Taiwan, 96% and 4% of rhizobia were members of Burkholderia and Cupriavidus, respectively [35].
Rhizobium nodulation enhances the host plant performance through the nitrogen and ammonium supply to host plants [36][37]. The nitrogen-fixing ability of Burkholderia species nodulated with M. pigra was also much greater than that of Cupriavidus species [35]. M. pigra nodulated vigorously even under flooded condition and fixed substantial quantities of nitrogen [38][39][40].
Rhizobium species, Burkholderia mimosarum sp. nov. was isolated from the root nodules of M. pigra population in Taiwan and Venezuela. However, the strains of Burkholderia mimosarum sp. nov. from Taiwan (invasive range of M. pigra) differed from the strain from Venezuela (native range of M. pigra) [33][35][41]. The strain LMG 23256T of Burkholderia mimosarum sp. nov., which was isolated from the root nodules of the M. pigra population in Taiwan, was highly effective for nitrogen fixing than the strains from Venezuela [42]. The Taiwan strains showed fast growing and fast colony-forming ability [43][44] and outcompeted other rhizobium species for nodulation with M. pigra under flooded conditions [34].
Ninety rhizobia isolated from the root nodules of M. pigra in an Australia population (i.e., an invasive range) were characterized as Burkholderia spp., which are also the main rhizobia in Tropical America (i.e., native ranges) [32][33][34]. The strains of Burkholderia in Australia showed divergent lineages, and all of them did not have a close relationship to the Burkholderia strains in the native ranges. Inoculation of M. pigra with the Australian Burkholderia strains showed equal or higher nodule nitrogenase activity than that of with the Tropical American Burkholderia strains, which resulted in its high plant growth rate. Therefore, the M. pigra population in Australia acquired more effective nitrogen-fixing symbionts compared to the M. pigra population in the native ranges [45].
A high level of arbuscular mycorrhizal fugus colonization was found in the flooded roots of M. pigra in wetlands [46][47]. The dominant mycorrhizal fungi in the M. pigra roots are the members of the Rhizophagus and Glomus genera, which belong to the Glomerales order and are considered to be generalist mycorrhizal fungi [48]. Arbuscular mycorrhizal fungi enhance their host plant performance through increasing water and nutrient acquisition, photosynthetic activity, and defense functions against the pathogen attacks and stress conditions [49][50][51]. Arbuscular mycorrhizal fungi also improve the host plant performance even in wetland conditions [52].
Those observations suggest that M. pigra associates actively with rhizobia and arbuscular mycorrhizal fungi even under flooded conditions. M. pigra in the invasive ranges may colonize with rhizobia, which possess high nitrogen-fixing activity compared to that of its native ranges (Table 1). The mutualism with rhizobia with high nitrogen-fixing activity in the invasive ranges may contribute to the invasiveness of the species.

5. Allelopathy

Many secondary metabolites in the invasive plants exhibit the function of allelopathy [53][54][55][56]. Allelopathy is the interaction between donor plants and their neighboring plants through certain secondary metabolites that are defined as allelochemicals [57][58][59][60]. The allelochemicals are released into the vicinity of the donor plants either by volatilization, rainfall leachates, root exudation and decomposition processes of donor plant residues, and they suppress the germination, growth and establishment of neighboring plants, as well as exhibiting mutualism with rhizobia and arbuscular mycorrhizal fungi [61][62][63][64][65][66][67]. Since allelochemicals are synthesized and stored in certain plant tissues until releasing into the vicinity of donor plants [57][58][59][60], several researchers determined the allelopathic activity in the residues of the leaves and extracts from different plant parts of M. pigra.
The leaf powder of M. pigra was mixed with soil and then the seeds of Ruellia tuberosa L. were sown into the mixture. The mixture suppressed the germination and growth of Ruellia tuberosa [68]. Ruellia tuberosa is also invasive species from Central and South America [69]. Aqueous extracts of M. pigra leaf powder inhibited the germination and growth of Vigna radiata (L.) R. Wilczek in an extract concentration-dependent manner [70]. The leaves and stems of M. pigra were soaked in boiling water for 10 min and the obtained solutions inhibited the root growth of Allium cepa L. and disturbed the cell division of its meristematic root cells, such as reducing the mitotic index and increasing chromosomal aberrations [71]. Methanol leaf extracts of M. pigra suppressed the root and shoot growth of Ruellia tuberosa, Echinochloa crus-galli (L.) P. Beauv. and Lactuca sativa L. The extracts showed the reduction of cell viability of their roots and also disturbed the mitosis of their root cells in a concentration-dependent manner. The extracts also increased lipid peroxidation in their roots and shoots [72][73].
Those observations suggest that the leaf residues and leaf and stem extracts of M. pigra exhibit allelopathic activity that influences the germination and growth of some plant species, as well as probably contains water and methanol extractable allelochemicals. Some of these allelochemicals would be liberated into the soil during their decomposition processes of the residues. Total annual litterfall of M. pigra was estimated to be 758 g m2 [74], and such a litterfall may be one of the sources of allelochemicals of the species. Allelochemicals of the invasive plant species suppressed the regeneration process of the native plant species in their invasive ranges [53][54][55][56][57][58][59][60][61][62][63][64][65][66][67]. Allelochemicals of M. pigra may also suppress the regeneration process of the native plant species through the inhibition of their germination and growth. Total concentrations of flavonoids, tannins and saponins were estimated in M. pigra leaves [73]. However, there has been no information available on the isolation and identification of the allelochemicals from M. pigra.
Mimosine (synonym; leucenol) was first isolated from Mimosa pudica L. [75] and found in some other species of the Mimosa and Leucaena genera [76][77][78]. Mimosine has shown a wide range of biological properties such as allelopathic, anti-tumor, apoptotic, anti-inflammation, anti-viral, and cell cycle blocking activity [79]. However, mimosine has not yet been identified in M. pigra.

6. Secondary Metabolites

Pharmacological investigations showed that M. pigra contains several secondary metabolites, which have pharmacological activity such as analgesic, antipyretic, anti-inflammatory, anti-diabetic, anticancer and antioxidant activity [80][81][82]. The methanol extracts of M. pigra leaves showed antioxidant and anti-inflammatory actions in the Wister rat, and quercitrin (quercetin 3-O-rhamnoside) and myricitrin (myricetin 3-O-rhamnoside) were isolated from the extracts [80] (Figure 2). The methanol extracts of M. pigra leaves also showed anti-dermatophyte activity, and astragalin, luteolin and quercitrin were isolated from the extracts [81].
Figure 2. Possible allelochemicals of Mimosa pigra.
Several flavonol glycosides, quercetin (2″-O-galloyl)-3-O-α-L-rhamnopyranoside, quercetin-3-O-α-L-rhamnopyranoside, quercetin-3-O-α-L-arabinopyranoside, myricetin (2″-O-galloyl)-3-O-α-L-rhamnopyranoside and myricetin-3-O-α-L-rhamnopyranoside [83], and quercetin-3-O-α-L-rhamnopyranoside, quercetin-3-O-β-D-galactopyranoside, quercetin-3-O-α-L-arabinopyranoside, myricetin-3-O-α-L-rhamnopyranoside, kaempferol-3-O-α-L-rhamnopyranoside and kaempferol-3-O-α-L-rhamnopyranosyl-(1→2)-β-D-glucopyranoside, and a flavonoid; 3′,4′,5,7-tetrahydroxyflavone [84], were isolated and identified in the leaf extracts. Terpenoid saponin: machaerinic acid was isolated from stems of M. pigra [85]. A furanochromone, 6,8-dihydroxy-2-methyl-9H-furo(3,2-b)choromen-9-one, was isolated and identified in the leaf extracts of M. pigra [86]. Pharmacological active compounds identified in the plant species of Mimosa genus were also reviewed by Rizwan et al. [82].
Table 1. Possible mechanisms for the Mimosa pigra invasion.
Many flavonoids have shown anti-herbivore, anti-fungal and anti-bacterial activity [87][88][89]. In addition, quercitrin and myricitrin have also been isolated from Ludwigia hexapetala Hook. (i.e., water primrose), and they displayed allelopathic activity [90]. Ludwigia hexapetala is native to Central and South America, it is a noxious invasive species in Western Europe and the United States and it grows well in swampy lands such as the margins of lakes and streams [91]. Quercitrin was reported to work as an allelopathic agent for the other territorial plant kiwifruit (Actinidia deliciosa (A. Chev.) C. F. Liang et A. R. Ferguson), and it has inhibited the growth of several other plant species [92][93].
Although most of the identified compounds in M. pigra have not yet been related to the invasiveness of the plant species, some of them may be involved in allelopathy and defense functions against herbivores and pathogenic fungi. Therefore, these compounds may contribute to the invasiveness and naturalization of M. pigra in the invasive ranges.

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