Bocconia frutescens
(plume poppy)

Pictures

Picture	Title	Caption	Copyright
Title Habit Caption Bocconia frutescens (parrot-weed, plume poppy, tree celandine); invading dry forest at Kanaio Natural Area Reserve. Maui, Hawaiian Islands, USA. January, 2003. Copyright ©Charles G. Chimera-2003	Habit	Bocconia frutescens (parrot-weed, plume poppy, tree celandine); invading dry forest at Kanaio Natural Area Reserve. Maui, Hawaiian Islands, USA. January, 2003.	©Charles G. Chimera-2003
Title Habit Caption Bocconia frutescens (parrot-weed; plume poppy; tree celandine); invading dry forest, with a native tree (Pleomele auwahiensis) in left foreground. Kanaio Natural Area Reserve, Maui, Hawaiian Islands, USA. Copyright ©Charles G. Chimera-2013	Habit	Bocconia frutescens (parrot-weed; plume poppy; tree celandine); invading dry forest, with a native tree (Pleomele auwahiensis) in left foreground. Kanaio Natural Area Reserve, Maui, Hawaiian Islands, USA.	©Charles G. Chimera-2013
Title Habit Caption Bocconia frutescens (parrot-weed, plume poppy, tree celandine); invading a lava flow and shrubland. Kanaio Natural Area Reserve, Maui, Hawaiian Islands. January, 2003. Copyright ©Charles G. Chimera-2003	Habit	Bocconia frutescens (parrot-weed, plume poppy, tree celandine); invading a lava flow and shrubland. Kanaio Natural Area Reserve, Maui, Hawaiian Islands. January, 2003.	©Charles G. Chimera-2003
Title Habit Caption Bocconia frutescens (parrot-weed, plume poppy, tree celandine); invading a lava flow and shrubland. Kanaio Natural Area Reserve, Maui, Hawaiian Islands. January, 2003. Copyright ©Charles G. Chimera-2003	Habit	Bocconia frutescens (parrot-weed, plume poppy, tree celandine); invading a lava flow and shrubland. Kanaio Natural Area Reserve, Maui, Hawaiian Islands. January, 2003.	©Charles G. Chimera-2003
Title Habit Caption Bocconia frutescens (parrot-weed, plume poppy, tree celandine); invading dry forest, with a native tree (Pleomele auwahiensis) in the background. Kanaio Natural Area Reserve, Maui, Hawaiian Islands, USA. January, 2003. Copyright ©Charles G. Chimera	Habit	Bocconia frutescens (parrot-weed, plume poppy, tree celandine); invading dry forest, with a native tree (Pleomele auwahiensis) in the background. Kanaio Natural Area Reserve, Maui, Hawaiian Islands, USA. January, 2003.	©Charles G. Chimera
Title Flowering habit Caption Bocconia frutescens (parrot-weed, plume poppy, tree celandine); flowering tree, with multi-branched habit. Kanaio Natural Area Reserve, Maui, Hawaiian Islands, USA. December, 2002. Copyright ©Charles G. Chimera-2002	Flowering habit	Bocconia frutescens (parrot-weed, plume poppy, tree celandine); flowering tree, with multi-branched habit. Kanaio Natural Area Reserve, Maui, Hawaiian Islands, USA. December, 2002.	©Charles G. Chimera-2002
Title Mature panicle Caption Bocconia frutescens (parrot-weed, plume poppy, tree celandine); mature panicle, before dehiscence. Auwahi dry forest, Maui, Hawaiian Islands, USA. December, 2002. Copyright ©Charles G. Chimera-2002	Mature panicle	Bocconia frutescens (parrot-weed, plume poppy, tree celandine); mature panicle, before dehiscence. Auwahi dry forest, Maui, Hawaiian Islands, USA. December, 2002.	©Charles G. Chimera-2002
Title Inflorescence Caption Bocconia frutescens (parrot-weed, plume poppy, tree celandine); inflorescence. Kanaio Natural Area Reserve, Maui, Hawaiian Islands, USA. December, 2002. Copyright ©Charles G. Chimera-2002	Inflorescence	Bocconia frutescens (parrot-weed, plume poppy, tree celandine); inflorescence. Kanaio Natural Area Reserve, Maui, Hawaiian Islands, USA. December, 2002.	©Charles G. Chimera-2002
Title Fruiting panicle Caption Bocconia frutescens (parrot-weed, plume poppy, tree celandine); fruiting panicle, with dehisced capsules and arillate seeds. June, 2003. Copyright ©Charles G. Chimera-2003	Fruiting panicle	Bocconia frutescens (parrot-weed, plume poppy, tree celandine); fruiting panicle, with dehisced capsules and arillate seeds. June, 2003.	©Charles G. Chimera-2003
Title Seed Caption Bocconia frutescens (parrot-weed, plume poppy, tree celandine); close-up of seed, with aril inside dehisced capsule. Copyright ©Charles G. Chimera-2013	Seed	Bocconia frutescens (parrot-weed, plume poppy, tree celandine); close-up of seed, with aril inside dehisced capsule.	©Charles G. Chimera-2013
Title Seed Caption Bocconia frutescens (parrot-weed, plume poppy, tree celandine); close-up of seed, with aril inside dehisced capsule. June, 2003. Copyright ©Charles G. Chimera-2003	Seed	Bocconia frutescens (parrot-weed, plume poppy, tree celandine); close-up of seed, with aril inside dehisced capsule. June, 2003.	©Charles G. Chimera-2003
Title Seedlings Caption Bocconia frutescens (parrot-weed, plume poppy, tree celandine); seedlings with cotyledons. March, 2004. Copyright ©Charles G. Chimera-2004	Seedlings	Bocconia frutescens (parrot-weed, plume poppy, tree celandine); seedlings with cotyledons. March, 2004.	©Charles G. Chimera-2004
Title Seedling recruitment Caption Bocconia frutescens (parrot-weed, plume poppy, tree celandine); seedling recruitment in the understory of the Auwahi dry forest restoration site. Maui, Hawaiian Islands, USA. January, 2003. Copyright ©Charles G. Chimera-2003	Seedling recruitment	Bocconia frutescens (parrot-weed, plume poppy, tree celandine); seedling recruitment in the understory of the Auwahi dry forest restoration site. Maui, Hawaiian Islands, USA. January, 2003.	©Charles G. Chimera-2003
Title Seedling recruitment Caption Bocconia frutescens (parrot-weed, plume poppy, tree celandine) seedling recruitment in the understory of the Auwahi dry forest restoration site. Maui, Hawaiian Islands, USA. January, 2003. Copyright ©Charles G. Chimera-2003	Seedling recruitment	Bocconia frutescens (parrot-weed, plume poppy, tree celandine) seedling recruitment in the understory of the Auwahi dry forest restoration site. Maui, Hawaiian Islands, USA. January, 2003.	©Charles G. Chimera-2003
Title Seedling carpet Caption Bocconia frutescens (parrot-weed, plume poppy, tree celandine); seedling carpet in the understory of the Kanaio Natural Area Reserve. Maui, Hawaiian Islands, USA. Copyright ©Charles G. Chimera-2013	Seedling carpet	Bocconia frutescens (parrot-weed, plume poppy, tree celandine); seedling carpet in the understory of the Kanaio Natural Area Reserve. Maui, Hawaiian Islands, USA.	©Charles G. Chimera-2013
Title Resprouting stump Caption Bocconia frutescens (plume poppy, parrot-weed, tree celandine); resprouting, after a cut stump treatment with no herbicide application. Kanaio Natural Area Reserve, Maui, Hawaiian Islands, USA. Copyright ©Charles G. Chimera-2013	Resprouting stump	Bocconia frutescens (plume poppy, parrot-weed, tree celandine); resprouting, after a cut stump treatment with no herbicide application. Kanaio Natural Area Reserve, Maui, Hawaiian Islands, USA.	©Charles G. Chimera-2013

Identity

Preferred Scientific Name

• Bocconia frutescens L.

Preferred Common Name

• plume poppy

Other Scientific Names

• Bocconia glauca Salisb.
• Bocconia pearcei Hutch.
• Bocconia quercifolia Moench
• Bocconia sinuatifolia Stokes
• Bocconia subtomentosa L'Hér. ex Stahl

International Common Names

• English: bocconia; parrotweed; parrot-weed; plume poppy; sea oxeye daisy; tree celandine; tree poppy
• Spanish: chilacolote blanco; jocote de fraile; palo de toro; pan cimarrón
• French: bocconie frutescente; bois codine; grande chelidoine

Local Common Names

• : grande chelidoine
• Argentina: sancho amargo
• Colombia: curarador; mata-chande; sarcillejo; sarno; trompeto
• Costa Rica: guacamaya; sangrillo; tabaquillo
• Cuba: palo amargo; palo amarillo
• Dominican Republic: yagrumo macho
• Germany: Federmohn, Strauchiger
• Guatemala: sangre de toro
• Jamaica: John Crow bush
• Mexico: calderón; cuatlataya; gordolobo; llora-sangre
• Panama: sangrillo; tabaquillo
• Puerto Rico: pan cimarrón; panapén cimarrón; panilla
• Uruguay: sancho amargo

EPPO code

• BOCFR (Bocconia frutescens)

Summary of Invasiveness

B. frutescens, is a short-statured Neotropical tree native to much of Central and South America and the West Indies, described as a fast growing, weedy pioneer that thrives in disturbed sites. It is naturalized in dry and mesic forests on the islands of Maui and Hawaii, where it is capable of forming dense stands that exclude the establishment of native species. It can reach reproductive maturity within four to six years, and produces tremendous numbers of seeds with fleshy arils that facilitate its dispersal by frugivorous birds. It also forms a long-lived seed bank, is able to resprout after repeated cutting and requires herbicide applications for effective control. It tolerates a broad range of environmental conditions along a large elevation gradient within its native range suggesting that it may further encroach upon additional native and non-native habitats within the Hawaiian Islands and could become invasive in similar tropical ecosystems worldwide. B. frutescens is listed as a noxious weed in Hawaii and affects a number of endangered species, including the rare flowering plant Melicope adscendens. PIER (2015) list it as high risk with a risk assessment scoring of 18.  

Taxonomic Tree

• Domain: Eukaryota
•     Kingdom: Plantae
•         Phylum: Spermatophyta
•             Subphylum: Angiospermae
•                 Class: Dicotyledonae
•                     Order: Papaverales
•                         Family: Papaveraceae
•                             Genus: Bocconia
•                                 Species: Bocconia frutescens

Notes on Taxonomy and Nomenclature

The Papaveraceae, or Poppy family, comprises about 25 genera and 200 species, which occur predominantly in temperate and tropical regions of the Northern Hemisphere (Wagner et al., 1999). In 1737, Linnaeus named the genus Bocconia for Paola Boccone, an Italian botanist and the grand duke of Tuscany (Wagner et al., 1999), with B. frutescens being the type species (Hutchinson, 1920). Macleaya, an Old World genus from China and Japan, was formerly included in the New World Bocconia genus, but the two are now recognized as distinct genera (Grey-Wilson, 2000). Bocconia, a genus of approximately 9 species of Central and South America and the West Indies (Kubitzki et al., 1993) may be distinguished from other members of the family by its woody, shrub to small tree-like, versus herbaceous, habit (Wagner et al., 1999) and may be considered atypical due to the apetalous flowers and a 1-seeded fruit (Allen, 1948).

Several varieties are recognized including Bocconia frutescens var. cernua, B. frutescens var. glaucescens and B. frutescens var. subtomentosa (e.g. The Plant List, 2015).   

Description

The following is adapted from Wagner et al. (1999).

Branched shrubs; stems 2-6 m long, pith white. Leaves often somewhat congested toward the tips of the branches, oblong-obovate to oblong-lanceolate, 10-45 cm long, 4-20 cm wide, pinnately cleft ca. 1/2 to midrib, upper surface sparsely strigillose, lower surface glaucous and puberulent, especially along veins. Panicles densely branched, 20-60 cm long, bracts lanceolate, 2-5 mm long, pedicels 3-10 mm long; sepals erect, elliptic, 8-10 mm long; stamens 8-10; filaments filiform; anthers linear, pendent by the filaments at anthesis. Capsules grayish at maturity, pulp pale yellow, ca. 12 mm long, stipe ca. 5 mm long. Seed 1, black, 6-7 mm long, the surface smooth and glossy, the lower 1/2-1/3 covered with a red, pulpy aril.

The internationally preferred common name, plume poppy, is indicative of the terminal inflorescences up to 60 cm long, with over 2000 small, petal-less, greenish-purple flowers per panicle (Graf, 1992). Another common name from Mexico, ’tears of blood’, refers to the bright red, pulpy aril attached to the shiny black seeds, 6-7 mm long (Gunn and Seldin, 1976). 

Plant Type

Distribution

B. frutescens has a broad native distribution from Central and South America to the West Indies (Wagner et al., 1999). It is naturalized in dry forests on the island of Maui, and in mesic forests on Hawaii, USA (Wagner et al., 1999). Tassin et al. (2006) list it among the woody non-indigenous plants to Réunion Island, and mark its status as "known as a colonizer in Réunion Island", but provide no information on date of introduction. USDA-ARS (2013a) lists B. frutescens as naturalized on the island of Mauritius, but includes Tassin et al. (2006) among the supporting references, suggesting that its naturalized status has been erroneously attributed to Mauritius. Grey-Wilson (2000) records it as present in a garden in New Zealand, and also reports that it has become naturalized in Java, with no other details on introduction or current distribution.

Distribution Table

The distribution in this summary table is based on all the information available. When several references are cited, they may give conflicting information on the status. Further details may be available for individual references in the Distribution Table Details section which can be selected by going to Generate Report.

History of Introduction and Spread

B. frutescens was first noted by the botanist Charles N. Forbes in the Kanaio area on the southern slopes of Haleakala on the island of Maui in 1920 (Wagner et al., 1999). During an extensive collecting trip throughout leeward East Maui, Forbes reported seeing only a single 8 ft. tall Bocconia plant growing on the roadside of the old government trail in Kanaio (Medeiros et al., 1993). Fosberg (1969) reported that B. frutescens was “at least precariously naturalized along the road south of Ulupalakua Ranch headquarters". On April 14, 1974, Fosberg and Sachet (1975) reported that many well-developed shrubs had spread some distance south along the road. A single seedling several decimeters tall was reported in Auwahi, in a fenced nature preserve above Ulupalakua Ranch, while a mature shrub was also reported in Kula, at about 1200 m elevation near the junction with Upper Kula Road and Haleakala Highway. Fosberg and Sachet (1975) still believed that it was possible to eradicate the weed at the time.

In the ensuing 90+ years following the collection of Forbes, Bocconia has spread on the island of Maui as far to the northwest as Kula at elevations of up to 1200 m and as far east as Manawainui Gulch in Kahikinui on Department of Hawaiian Homelands land up to as high as 1767 m. The heaviest concentration of plants, with the broadest elevational distribution and the largest numbers of reproductive sized individuals as well as recently germinated seedlings, occurs in the dry forests of Kanaio and Auwahi on the south slope of Haleakala, in the vicinity of the original 1920 observation. Medeiros et al. (1986) reported that B. frutescens was one of the characteristic introduced species of the upper dryland forest, from 915-1464 m, suggesting a certain ubiquity of this plant at the time but otherwise did not comment on its current or potential invasiveness. In 1992, however, Medeiros et al. (1993) found that the tree made up the sixth most common alien plant cover for non-native species in the Kanaio Natural Area Reserve, and recommended that it be opportunistically eliminated from areas of relatively intact native vegetation. It now occupies an area that extends from 488-1220 m to at least 1220 m.

The only other Hawaiian island on which Bocconia is naturalized is Hawaii, where it occurs in mesic forest at elevations of 550-920 m at disturbed sites, such as roadsides (Wagner et al., 1999), although the date of introduction is not known. The first collection on the island was documented in 1982 (Bishop Museum, 2013). In 2001, two specific Bocconia infestations were observed; one near Manuka Natural Area Reserve (scattered plants) and the other in Wood Valley (scattered individuals or small patches of plants over nearly 1200-1400 hectares) (Duane Nelson, US Forest Service, USA, personal communication, 2013). Benitez and Saulibio (2007) conducted an island wide survey in 2003, reporting that Bocconia was distributed over 1522 hectares in Wood Valley, 82 hectares in Honomolino, and 34 hectares in Manuka regions of Hawaii island.

Although not recorded as naturalized B. frutescens is also reported to be present on the Hawaiian Island of Oahu, where landowners are encouraged to control it on their property (HISC, 2013).

Elsewhere in the world, Tassin et al. (2006) list B. frutescens among the woody non-indigenous plants to Réunion Island, and mark its status as "known as a coloniser in Réunion Island", but provide no information on date of introduction. USDA-ARS (2013a) lists B. frutescens as naturalized on the island of Mauritius, but includes Tassin et al. (2006) among the supporting references, suggesting that its naturalized status has been erroneously attributed to Mauritius. Grey-Wilson (2000) also reports that it has become naturalized in Java, with no other details on date of introduction or current distribution.

Introductions

Risk of Introduction

Intentional introduction and cultivation of B. frutescens for ornamental or medicinal purposes is the most likely vector for movement of the species outside of its native range. Although Grey-Wilson (2000) suggests that the tropical distribution of the genus make Bocconia species unsuitable for temperate gardens, Riffle (1998) states that Bocconia is unexcelled for creating the tropical effect in sunny, well-drained sites.

It is valued for its bold tropical appearance, especially in the warmer parts of the USA, where it has been planted as an ornamental (Rzedowski, 1991; Everett, 1992). In Guacamayo, Costa Rica, the native B. frutescens is considered to be an economically important ornamental plant (Longhi, 1980).

Once introduced to a region, dispersal of the seeds by frugivorous birds (Wheelwright et al., 1984; Chimera, 2004; Chimera and Drake, 2010), and perhaps by movement of contaminated soil containing the long-lived seeds (Benitez and Saulibio, 2007; Veldman et al., 2007) is likely to contribute to the spread of this species. 

Habitat

B. frutescens is described as a fast growing, weedy pioneer (Francis, 2004; Condit et al., 2010), and has been found to thrive in disturbed sites (Tanner, 1982) such as those occurring along roadsides (Gentry, 1993; Young 1994; Wagner et al., 1999), riverbanks (Hutchinson, 1920), forest clearings (Adams, 1972), abandoned plantations (Cavelier and Santos, 1999), landslides (Myster and Sarmiento, 1998) and secondary woodlands and thickets (Liogier, 1985; Little et al., 1974; Holz and Gradstein, 2005). It occupies habitats that are sunny and well-drained and is found at low and mid elevations (Liogier, 1985). Rozema et al. (1997) describe B. frutescens as a weed of clearings and roadsides from 350-2200 m a.s.l. that prefers open habitats.

Williams-Linera and Ewel (1984) state that B. frutescens can rapidly colonize both disturbed and burned areas. Eventually, Bocconia may be overtopped and replaced by late successional species, such as in a Costa Rican upper montane Quercus forest, where it and other pioneer species gave way to large numbers of Quercus copeyensis and Q. costaricensis with heights >15 m (Kappelle et al., 1996).

Goodland and Healey (1997) identify B. frutescens as a gap demanding native species in Jamaica, a characteristic that would contribute to its invasiveness in the fragmented dry forests of the Hawaiian Islands. Tanner (1982) states that it is common in disturbed areas of the tropical montane forests of the Blue Mountains of Jamaica. This habitat is continually cloudy and often fog-shrouded forest, with light winds, high relative humidity (Tanner, 1982) and an annual precipitation of 2600-4270 mm (Tanner, 1977).

Francis (2004) reports that Bocconia can grow on a wide variety of soils and habitats, ranging from subtropical dry forests along streams to subtropical moist and wet forests of Puerto Rico. It is most commonly found along streams, road cuts, and landslides, but also occurs in abandoned pastures and secondary forest (Francis, 2004). In Nicaragua, it grows in cloud forest (Stevens et al., 2001) and in Costa Rica, it occurs in mesic to wet regions, in second growth and open sites as well as along roadsides (Gargiullo et al., 2008). In the Hawaiian Islands, it invades dry forest on the island of Maui and mesic forest on the island of Hawaii, and is also commonly found in disturbed sites and along roadsides (Wagner et al., 1999). Riffle (1998) states that Bocconia can be grown as a shrub in USDA plant hardiness zones 9b and 10a.

Habitat List

Hosts/Species Affected

B. frutescens is considered a major weed in small agricultural lots in the Wood Valley area of Hawaii, and has spread rapidly following the demise of the sugar cane industry (Motooka et al., 2003).

Biology and Ecology

Genetics

The chromosome number is 2n = 20 (Wagner et al., 1999).

Reproductive Biology

The small apetalous flowers are not very showy, yet are frequently visited by non-native syrphid flies and honeybees (Apis mellifera) within the introduced range on Maui, Hawaii. Tanner (1982) observed honeybees visiting the male flowers in the tropical montane rain forests of Jamaica. The structure of the flower, with anthers dangling from pendent filaments, also suggests adaptations for wind pollination. Blattner and Kadereit (1999) showed that morphological change in the Bocconia/Macleaya clade of Papaveraceae is related to the evolution of wind pollination from insect pollination in these two genera after a habitat shift. Tanner (1982) mentions that Bocconia is also successfully wind-pollinated.

Physiology and Phenology          

B. frutescens will first flower and fruit with a single panicle after approximately four to six years of growth (Chimera, 2004). Although May to August appear to be the peak fruiting period in the Hawaiian Islands (Chimera and Drake, 2010), in its native range it can flower and fruit sporadically throughout the year (Adams 1972; Little et al., 1974). In Jamaica, Bellingham et al. (1995) reported that following hurricane disturbance B. frutescens grew to 5 m tall and reached maturity in 3.5 years before dying.

As the tree grows in size and increases its number of stems and branches, it has the ability to produce a significant number of panicles and ultimately seeds. In Maui, a Bocconia tree approximately 4 m tall with three main trunks arising from the base (basal diameters: 34.5 cm; 14.4 cm; 9 cm) had 44 infrutescences with predominantly immature capsules and 109 infrutescences with predominantly mature capsules present (CG Chimera, University of Hawaii, Hawaii, USA, 1997, unpublished data). The 153 branched fruiting panicles, averaging 37.6 cm in length (n=25), had an average of 1962.8 capsules per panicle (n=11) and thus gave this tree the potential to produce up to 300,308 seeds in a single fruiting season. Nevertheless, there were also 94 old infrutescences present on the tree at the time of this survey, completely devoid of fruit, which appear to have persisted from the previous year and which could account for another 184,503 seeds produced by this tree. It is worthy of note that the tree sampled for the fruiting estimate (4 m) is approximately half as tall as the largest recorded individuals (Bailey and Bailey, 1976). A larger tree would presumably produce a much greater number of seeds during the fruiting seasons. Once the immature capsules (approximately12 mm long) change from a dull, greyish-blue colour to a pale yellow colour, they dehisce by two caducous valves from the base to reveal the single, shiny-black seed. The seed is approximately 6-7 mm long and is covered by a bright red to scarlet aril, which covers about 2-4 mm of its length.

B. frutescens is able to persist in the environment, and to exploit and rapidly colonize disturbed sites in part through the long-lived seeds and persistence of the seed bank. Bocconia seeds contain chemicals which defend them against soil pathogens and arthropod seed predators, allowing them to persist in the soil for decades or longer (Veldman et al., 2007). Despite these chemicals, however, vertebrate seed predators, including introduced rodents (Rattus spp.) in a tropical dry forest on the island of Maui, Hawaii (Chimera and Drake, 2011), as well as unspecified mammalian seed predators in Costa Rica (Jones et al., 2003) have been documented to remove and presumably consume the seeds.

Longevity

Bellingham et al. (1995) described it as a short-lived pioneer tree, and reported that plants which germinated underneath hurricane-defoliated canopies and gaps in Jamaican montane forests grew to 5 m tall, flowered and fruited, and died within 3.5 years.

Associations

In Costa Rica, Williams-Linera and Ewel (1984) reported that the mycorrhizal status of Bocconia is unknown, but that no mycorrhizal fungi have been observed on the root preparations they examined. This factor could contribute to the success of B. frutescens in colonizing disturbed areas in which the mycorrhizal flora is damaged or absent.

Environmental Requirements

Tanner (1982) states that it is common in disturbed areas of the tropical montane forests of the Blue Mountains of Jamaica. This habitat is “continually cloudy and often fog-shrouded forest, where winds are light and relative humidity is always high” (Tanner 1982) and has an annual precipitation of 2600-4270 mm (Tanner 1977). B. frutescens is reported to grow in the tierra templada of Colombia, a region from 600-1300 m elevation, with a warm and temperate climate (17-22°C) (Hobbs, 2007). In Puerto Rico, Francis (2004) found that it grows in subtropical dry forest along streams (750-1000 mm/year precipitation), in subtropical moist forest (1000-2000 mm/year precipitation), and in subtropical wet forests (2000-3000 mm/year precipitation). Riffle (1998) states that Bocconia can be grown as a shrub in USDA plant hardiness zones 9b and 10a. Zone 9b has average annual minimum temperatures ranging from -1.2 to –3.8°C and Zone 10a has average annual minimum temperatures ranging from -1.1 to 1.6°C. Riffle (1998) also states that it can be grown as a tree in hardiness zones 10b and 11, with average annual minimum temperatures ranging from 1.7 to 4.4°C and above 4.5°C respectively. Zone 9 is characterised by mild winters, long growing seasons and almost no winter freezes. Zone 10 includes subtropical regions in Hawaii and Florida and is characterised by year-round growing seasons and ocean regulated climates. Zone 11 is a tropical region that occurs in Hawaii and the lowermost Florida keys and also has mild temperatures and a year-round growing season.

B. frutescens has become invasive in dry forests in Auwahi and in the Kanaio Natural Area Reserve, on the leeward side of East Maui, Hawaii, at an elevation between 750-850 m (Chimera, 2004; Medeiros et al., In press). The climate in Kanaio is hot and dry, with annual temperatures between 20-30°C and with mean annual rainfall of approximately 750 mm, mostly falling between the months of October to April (Giambelluca et al., 2013). In Auwahi, mean annual precipitation is ca. 730 mm with a pronounced dry season from April to September (Giambelluca et al., 2013) and with mean monthly temperatures between 13.9°C and 18.3°C (Scholl et al., 2007).

Francis (2004) reports that B. frutescens trees can grow on a wide variety of soil types, implying that they are not limited by soil nutrient levels. In a study on forest succession in Jamaica, McDonald and Healey (2000) reported that secondary forests, of which B. frutescens is a component, were similar to the functioning of undisturbed forest in terms of soil and nutrient cycling.

Climate

Air Temperature

Rainfall

Rainfall Regime

Soil Tolerances

Soil drainage

• free

Soil texture

• heavy
• light
• medium

Notes on Natural Enemies

Preliminary work, funded by the Hawaii Invasive Species Council, has begun to evaluate natural enemies of B. frutescens for their potential as biological control agents within the state of Hawaii. Johnson and Nishida (2008) stated that B. frutescens is an excellent candidate for classical biological control because the Hawaiian flora has only one native species of Papaveraceae, Argemone glauca, and non-target concerns are therefore minimal and easily addressed. In its native range in Costa Rica, Nishida and Johnson (2010) found 38 species of natural enemy but only recommended three for further study: “a gregarious leafminer Liriomyza sp. (Agromyzidae), a treehopper Ennya pacifica (Membracidae) which deposits egg masses on leaf veins, and a leaf tier moth (Tortricidae) whose larvae damage young leaves.” Nishida and Johnson (2010) cautioned that there may be serious constraints associated with these organisms, however, and suggested searching for natural enemies in other areas within the natural range of B. frutescens. However, further study in Costa Rica by Boucher and Nishida (2014) has identified two new species of Neotropical Liriomyza mining leaves of B. frutescens.   

Tupac et al. (2009) found that B. frutescens is a natural host for the root hemiparasitic plant Corynaea crassa.

Means of Movement and Dispersal

Natural Dispersal

Although Smith (1985) suggests that seeds are wind-dispersed, they possess no morphological adaptations for wind dispersal (Wagner et al; 1999). Those seeds that fall directly from the parent tree without consumption or transport by frugivorous birds would more accurately be described as dispersed by gravity (Chimera and Drake, 2010).

As B. frutescens is frequently found along streams and rivers (Hutchinson, 1920; Francis, 2004) the potential exists for movement of seeds by water. Within the invaded range on Hawaii, Benitez and Saulibio (2007) reported that Bocconia is common in streambeds and surmised that plants found in gulches below a heavy infestation likely established from seeds that were washed down during heavy rains.

Vector Transmission

The pulpy aril material of B. frutescens is attractive to birds and aids in the dispersal of the seeds (Gargiullo et al., 2008). Within its native range, bird species which have been documented to consume and disperse Bocconia seeds include Elaenia frantzii (the mountain elaenia) (Marini and Cavalcanti, 1998), Chiroxiphia linearis (long-tailed manakin) and Vireo flavoviridis (yellow-green vireo) (Wheelwright et al., 1984).

Within its introduced range on the Hawaiian island of Maui, numerous non-native birds have been documented to consume and disperse the seeds. In describing its spread on Maui, Fosberg and Sachet (1975) reported that the fleshy aril or caruncle probably assures its wide distribution by mynahs and other introduced frugivorous birds.

In a preliminary survey of frugivory and dispersal of B. frutescens by non-native birds, Chimera (CG Chimera, University of Hawaii, Hawaii, USA, 1998, unpublished data) observed large numbers of Japanese white-eyes (Zosterops japonicus) feeding on the mature fruits at 580 m elevation on the south slope of Haleakala just after sunrise. Northern mockingbirds (Mimus polyglottus) were also observed eating the ripe arils, and a northern cardinal (Cardinalis cardinalis) perched on a panicle but did not consume any seeds. Other birds recorded as present at the time but not observed to be feeding on the fruits included the common mynah (Acridotheres tristis), house finches (Carpodacus mexicanus) and several gamebirds, such as the black francolin (Francolinus francolinus), the gray francolin (F. pondicerianus), and the ring-necked pheasant (Phasianus colchicus). On 7/9/98, mist-nets were set up in a fruiting stand of Bocconia in the Auwahi dry forest of Maui at an elevation of 790 m. Four Japanese white-eyes (Z. japonicus) were caught and faecal samples collected after a 20-minute holding period. Two white-eyes had one seed present in each of their fecal samples, another had two seeds present, and the fourth had remains of the aril present without the seed. On 8/12/98, several Japanese white-eyes were also observed consuming seeds of Bocconia growing along the road in Kula, Maui, at an elevation of approximately 1220 m. In addition, seeds have been collected in the droppings of a larger bird, possibly a turkey or a peacock, in the dry forest of Kanaio.

In an analysis of seed dispersal within the tropical dry forest of Kanaio Natural Area Reserve, Maui, Chimera and Drake (2010) reported that B.frutescens seeds were the most abundant in the bird-dispersed seed rain, and observed the non-native Japanese white-eyes, northern cardinals and northern mockingbirds swallowing and presumably dispersing the seeds. Johnson and Nishida (2008) found that seeds were dispersed by Japanese white eyes and Red-billed leiothrix (Leiothrix lutea) for distances of apparently >1km. Chimera and Drake (2011) also reported that cleaned and intact (i.e. with arils attached) seeds were removed from ground sites under parent trees, and suggested that these seeds were depredated by non-native rodents due to the presence of husks and seed fragments. Because intact seeds were removed at high rates, Chimera and Drake (2011) speculated that rodents or game birds may also be providing some secondary dispersal of Bocconia seeds that fall directly under parent trees.

Accidental Introduction

As the seeds of B. frutescens are relatively large (6-7 mm length; Wagner et al., 1999), they are unlikely to be inadvertently dispersed into a new region as a seed contaminant of produce or other agricultural products. Once established within an area, however, the persistence of the seeds in the soil could allow for inadvertent dispersal through movement of contaminated soil from within the invaded area (Veldman et al., 2007). Benitez and Saulibio (2007) express concerns about the possibility of unintentional movement of seeds on Hawaii and provide recommendations such as decontamination of heavy machinery and prevention of soil movement from within invaded areas.

Intentional Introduction

B. frutescens was first collected on Maui, Hawaii in 1920 (Wagner et al., 1999), but the reasons for introduction, whether intentional or inadvertent, are unknown.

Intentional introduction and cultivation of B. frutescens for ornamental or medicinal purposes is the most likely vector for movement of Bocconia outside its native range, and it continues to be promoted as an ornamental plant in horticultural books and websites (Riffle, 1998; Dave's Garden, 2013). 

Pathway Causes

Pathway Vectors

Vectors and Intermediate Hosts

Impact Summary

Economic Impact

Although there are no cost estimates, Medeiros et al. (In press) report that weed control in a dry forest restoration area on Maui is predominantly focused on B. frutescens, incurring costs in both labour and herbicide usage.

Environmental Impact

Impact on Habitats

Tropical dry forests are one of the most endangered natural communities in the Hawaiian Islands and have been reduced to approximately 10% of their former cover (Bruegman, 1996). As it is capable of forming dense stands in dry habitats, Smith (1985) listed B. frutescens as one of the 86 worst weeds that have become serious pests of dry forests and other native ecosystems. The most significant infestations of Bocconia on Maui now occur from 485-1225 m in the dry forests of Auwahi and Kanaio, and during the 1992 survey of the now Kanaio Natural Area Reserve, Bocconia was found to comprise the sixth highest percentage cover of alien species along five monitoring transects (Medeiros et al., 1993). However, of the ten most common weeds by cover, it was the only woody species that could achieve the stature and dimensions of a dry forest tree. With its multiple-trunked, bushy growth habit, a single tree can occupy a fairly substantial amount of area close to the ground, which appears to prevent the establishment of other plants beneath it. For these reasons, it was identified as one of the seven most aggressive alien plant species that are a primary threat to native ecosystems of the Kanaio Natural Area Reserve (Medeiros et al., 1993).

In the mid to late 1990s, B. frutescens expanded its density and range throughout the Auwahi and Kanaio regions of Maui, with heavier concentrations of seedlings appearing with increasing frequency, especially in bare areas recently exposed by kikuyu grass (Pennisetumclandestinum) dieback. This appeared to be related to the effects of the yellow sugarcane aphid (Sipha flava) and drought (CG Chimera, University of Hawaii, Hawaii, USA, 1998, unpublished data). Combined with the ever-maturing population of reproductive sized individuals, the current B. frutescens infestation has continued to increase. In addition, the timing of the peak fruiting period provides a conspicuous food resource for birds in the area, especially during the beginning of the hot and dry summer months when other food resources become increasingly scarce (Chimera, 2004; Chimera and Drake, 2010). This phenomenon is contributing to the expansion of B. frutescens, with seedlings germinating away from the parent plant and beneath both native and nonnative trees. Under these trees, seedlings can form dense carpets and exclude the rarely reproducing native dry forest species (Chimera, 2004).

On Hawaii, Benitez and Saulibio (2007) surveyed multiple B. frutescens populations, recording densities ranging from under 10 individuals/ha to a heavily invaded 29ha parcel containing 5224 individuals/ha within a young Eucalyptus plantation, and less than 100 individuals/ha within former cane fields. Although size classes were not recorded, all populations within this area included fertile individuals. Therefore, B. frutescens is reported as a severe pest on Hawaii, forming dense stands, primarily within Eucalyptus plantations and former sugar cane lands, but is generally not found under native, closed-canopy Metrosideros polymorpha and Acacia koa forests in the adjacent Ka`u Forest Reserve. However, B. frutescens has begun to invade native forests in the Honomolino region of Hawaii and infestations near Hawaii Volcanoes National Park are reported as one of the greatest threats to native plant communities because of their vicinity and dispersal mechanisms (Benitez and Saulibio, 2007).   

Within the remnant dry forest of Auwahi, Maui, upslope of the Kanaio NAR, Medeiros et al. (2003) reported that large Bocconia trees were completely removed from a 4ha restoration site in the late 1990s but that Bocconia seedlings continued to emerge and were present in 100% (n=10) of monitoring plots evaluated in a 2002 survey. A 15 year analysis of vegetation changes in the same restoration site found that despite control efforts on reproductively mature trees within and in the vicinity of the exclosure, Bocconia seedlings were recruiting at significantly greater numbers than at the start of the restoration project, and were one of the six most common seedlings recorded in the site (Medeiros et al., In press).

Impact on Biodiversity

The US Fish and Wildlife Service lists B. frutescens as one of the major threats to the survival of Melicope adscendens (Fish and Wildlife Service, 2000). This sprawling shrub is endemic to the dry forests of Kanaio and Auwahi, East Maui, areas in which Bocconia is proliferating. Other endangered plants occurring in the area that could also be negatively affected by competition with B. frutescens include Alectryon macrococcus (Sapindaceae), Bonamia menziesii (Convolvulaceae), the only known Maui population of Cenchrus agrimonioides (Poaceae), Fluggea neowawraea (Euphorbiaceae), Melicope knudsenii (Rutaceae), and Santalum freycinetianum var. lanaiense [S. haleakalae var. lanaiense] (Santalaceae) (Medeiros et al.,1993; Fish and Wildlife Service, 2000). The Fish and Wildlife Service also states that Bocconia threatens Nothocestrum latifolium (Solanaceae), the host plant of the endangered Blackburn’s sphinx moth (Manduca blackburni), through displacement and shading of immature plants (Fish and Wildlife Service, 1997).

PIER (2015) list it as high risk with a risk assessment scoring of 18 and on Hawaii it is listed as a noxious weed. On the island of Maui, Hawaii, Medeiros et al. (In press) report that B. frutescens is the most common non-native plant recruiting within dry forest restoration exclosures of Auwahi, and that weed control efforts are primarily focused on its control. Medeiros and von Allmen (2006) documented five endangered plant species within the area, including Zanthoxylum hawaiiense, Melicope knudsenii, M. adscendens, Alectryon macrococcus var. auwahiensis, and Santalum haleakalae var. lanaiense, as well as Nothocestrum latifolium, the primary native host plant for the endangered Blackburn’s sphinx moth (Manduca blackburni). Medeiros et al. (In press) suggest that, without control efforts, B. frutescens would likely increase and dominate portions of the restoration area and threaten the habitat of these endangered species.

Johnnson and Nishida (2008) found B. frutescens to be spreading and progressively dominating fern-filled gulches of Acacia koa forests of the Kahikinui district of leeward East Maui. This area has been identified as a key site targeted for A. koa restoration and as the prime release site of the endangered Maui parrotbill (Pseudonestor xanthophrys).

Threatened Species

Social Impact

The Auwahi dry forest on Maui, USA, is threatened by the invasion of B. frutescens. This forest is valued by native Hawaiians as a rich source of ethnobotanical materials, particularly durable hardwoods used for tools and weapons, and species with utilitarian, medicinal or religious significance (Medeiros et al., 1998). 

Risk and Impact Factors

• Proved invasive outside its native range
• Has a broad native range
• Abundant in its native range
• Highly adaptable to different environments
• Is a habitat generalist
• Tolerates, or benefits from, cultivation, browsing pressure, mutilation, fire etc
• Pioneering in disturbed areas
• Tolerant of shade
• Fast growing
• Has high reproductive potential
• Has propagules that can remain viable for more than one year

• Altered trophic level
• Damaged ecosystem services
• Ecosystem change/ habitat alteration
• Host damage
• Modification of successional patterns
• Monoculture formation
• Negatively impacts agriculture
• Reduced amenity values
• Reduced native biodiversity
• Threat to/ loss of endangered species
• Threat to/ loss of native species

• Competition - monopolizing resources
• Competition - shading
• Competition (unspecified)
• Interaction with other invasive species
• Rapid growth

• Difficult/costly to control

Uses

Economic Value

B. frutescens may provide economic benefits to those who are cultivating it for commercial sale and it has been widely planted as an ornamental (Rzedowski, 1979). It is valued for its bold, tropical looking foliage, especially in warmer parts of the USA (Everett, 1992). In Guacamayo, Costa Rica, the native B.frutescens is considered to be an economically important ornamental plant (Montiel, 1991).

In its native range it is used as a dye and the sap, roots and leaves are used in home medicines (Little et al., 1974; Duke, 2008). Martinez (1969) mentions that injections of an extract of the tree can produce a local anesthetic effect but with an irritant side effect. In Veracruz, Mexico, the orange sap has been used in the treatment of ulcers and skin eruptions, to alleviate bronchitis and as a local anesthetic, whereas the leaves have been heated and applied to wounds (Ojeda, 1982).    

Environmental Services  

Within its native range, B. frutescens reportedly contributes to biodiversity, helps protect the soil and furnishes food and cover for wildlife (Francis, 2004). It is also being evaluated as a species for restoration of disturbed sites.

Uses List

Environmental

• Revegetation
• Soil conservation
• Wildlife habitat

Medicinal, pharmaceutical

• Source of medicine/pharmaceutical
• Traditional/folklore

Ornamental

• Potted plant

Detection and Inspection

B. frutescens has been identified as an early detection species targeted for eradication and control on those Hawaiian Islands where it is yet to become established (HISC, 2013).

Similarities to Other Species/Conditions

The Spanish common name from Puerto Rico, ’pan cimarron’, may be derived from the slight resemblance of the leaves to those of breadfruit (Little et al.; 1974).

In Panama and Costa Rica, Condit et al. (2010) state that B. frutescens may appear similar to weedy Asteraceae with lobed leaves, but that it may be distinguished by its growth habit as a little tree. 

Prevention and Control

Due to the variable regulations around (de)registration of pesticides, your national list of registered pesticides or relevant authority should be consulted to determine which products are legally allowed for use in your country when considering chemical control. Pesticides should always be used in a lawful manner, consistent with the product's label.

Prevention and Control

As of June 1992, the Hawaii Department of Agriculture designated B. frutescens as a noxious weed to be targeted for eradication and/or control (USDA-ARS, 2013b).

Early Warning Systems

Identified as an early detection species, it is especially targeted for eradication and control on those Hawaiian Islands where it is yet to become established (HISC, 2013).

Public Awareness

B. frutescens has been the subject of education and outreach programmes by the Big Island Invasive Species Committee, based on the island of Hawaii, and the Kauai Invasive Species Committee, on the island of Kauai (HISC, 2013). In both cases, it has been the subject of early detection fliers and weed identification booklets in an effort to educate the public on the identification and impacts of B. frutescens on the respective islands, and the outreach materials request that members of the public report plant locations when encountered.                  

Physical/Mechanical Control

Some localized small scale pulling of B. frutescens seedlings and saplings has been carried out inside various exclosures of the Native Hawaiian Plant Society in the Auwahi dryland forest on the south slope of Haleakala (Nakagawa, 1994; 1995), but no large-scale mechanical or herbicidal treatments have been performed to date. Nevertheless, Medeiros et al. (1993), identified the tree as one of seven alien plant species that is aggressive and a primary threat to the native ecosystems of the Kanaio Natural Area Reserve and therefore recommended that some form of control be performed in areas of the most intact native vegetation. In an exclosure managed by the USGS-Biological Resources Division, the primary means of control involves the initial removal of all fruiting trees and the sporadic removal of the seed bank recruits. Simple mechanical control of plants involving cutting of the branches or trunks will result in the plant’s regrowth (CG Chimera, University of Hawaii, Hawaii, USA, 1998, unpublished data).

Containment/Zoning

The Big Island Invasive Species Committee (BIISC), in conjunction with private landowners, is performing mechanical and chemical control of B. frutescens outliers in an attempt to contain the spread of a 3500 acre (1416.4-ha) infestation in the Wood Valley, Ka’u district of Hawaii , and particularly, to exclude it from high conservation value lands. BIISC has requested that members of the public contact a regional pest hotline to report sightings of B. frutescens, especially those occurring outside the known areas of infestation (HISC, 2013).

Biological Control

Preliminary work has begun to evaluate natural enemies of B. frutescens for their potential as biological control agents within the state of Hawaii. Johnson and Nishida (2008) stated that B. frutescens is a promising candidate for classical biological control because the Hawaiian flora has only one native species of Papaveraceae, Argemone glauca, and non-target concerns are therefore minimal and easily addressed. Nishida and Johnson (2010) found that of 38 species of natural enemies, the following three merit further study: a gregarious leafminer Liriomyza sp. (Agromyzidae), a treehopper Ennya pacifica (Membracidae) which deposits egg masses on leaf veins, and a leaf tier moth (Tortricidae) whose larvae damage young leaves. Nishida and Johnson (2010) advised however, that there may be serious constraints associated with these organisms, and that further research for natural enemies in other areas within the natural range is needed.

Chemical Control

Herbicide trials involving thin line basal application of a chemical such as Garlon 4 in a diesel carrier have been suggested for the control of the tree. This method would probably only be practical for smaller diameter trees with single trunks. For larger trees with multiple trunks arising from the base, a cut-stump treatment would probably be more effective.

The aerial delivery of a foliar herbicide, such as Garlon 3A, from a long-line ball sprayer attached to a helicopter has also been suggested to help reduce the ubiquitous seed source of B. frutescens. This strategy, similar to the method employed in Miconia calvescens control efforts on the windward side of Maui (Medeiros et al., 1998), would target the larger, fruiting trees and dense stands of plants. Motooka et al. (2003) also reported that good control was achieved with 2,4-D and fair control with triclopyr applied using the basal bark application method.

Gaps in Knowledge/Research Needs

Although Nishida and Johnson (2010) reported 38 natural enemy species within its natural range of Costa Rica, they advised that there may be serious constraints with the utility of these organisms and recommend that the search for other biological control agents be expanded to incorporate a broader range of its natural distribution. 

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Distribution References

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Sherman R E, Martin P H, Fahey T J, 2005. Vegetation-environment relationships in forest ecosystems of the Cordillera Central, Dominican Republic. Journal of the Torrey Botanical Society. 132 (2), 293-310. DOI:10.3159/1095-5674(2005)132[293:VRIFEO]2.0.CO;2

Tassin J, Rivière J N, Cazanove M, Bruzzese E, 2006. Ranking of invasive woody plant species for management on Réunion Island. Weed Research (Oxford). 46 (5), 388-403. http://www.blackwell-synergy.com/servlet/useragent?func=showIssues&code=wre DOI:10.1111/j.1365-3180.2006.00522.x

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Links to Websites

Organizations

Hawaii: Big Island Invasive Species Committee - BIISC, 23 E. Kawili St. Hilo,, HI 96720, http://www.hawaiiinvasivespecies.org/iscs/biisc/

Hawaii: Leeward Haleakala Watershed Restoration Partnership - LHWRP, P.O. Box 652, Makawao, HI 96768, http://www.lhwrp.org/

Hawaii: Natural Area Reserve System - NARS, 1151 Punchbowl Street, Room 325 Honolulu,, HI 96813, http://hawaii.gov/dlnr/dofaw/nars

Contributors

31/07/2013 Original text by:

Charles G. Chimera, Pacific Cooperative Studies Unit, University of Hawaii, PO Box 983, Makawao, Hawaii, USA 96768

Distribution Maps