Diversity of Phyllanthaceae Plants

Abstract

Euphorbiaceae, one of the major components of tropical flora worldwide, has long been considered a heterogeneous group (Webster 1994; Radcliffe-Smith 2001). Recent molecular phylogenetic analyses have clearly shown that Euphorbiaceae is nonmonophyletic, and consequently, Pandaceae, Phyllanthaceae, Picrodendraceae, Putranjivaceae, Peraceae, and Centroplacaceae have been removed from it, although these families all belong to the order Malpighiales together with the updated Euphorbiaceae (Euphorbiaceae s. str.; Angiosperm Phylogeny Group III 2009). Thus, the small unisexual flowers and trilocular capsule that characterize the plants of the former Euphorbiaceae are plesiomorphic or convergent characters. For example, Rafflesiaceae, the family with the world’s largest, unisexual but unilocular flowers, is embedded in the former Euphorbiaceae (Davis et al. 2007); the clade sister to Rafflesiaceae is now Euphorbiaceae s. str., and the lineage sister to (Rafflesiaceae + Euphorbiaceae s. str.) is split as Peraceae (Fig. 4.1). Of the seven former Euphorbiaceae families, Euphorbiaceae s. str. and Phyllanthaceae are by far the largest, with the former containing about 300 genera and about 7500 species, and the latter 54 genera and about 2000 species (Table 4.1). Webster (1994) noted an important morphological feature of Phyllanthaceae that clearly distinguishes them from Euphorbiaceae s. str.; the former has two ovules per locule whereas the latter only has one ovule per locule.

1 Taxonomy of Phyllanthaceae

Euphorbiaceae , one of the major components of tropical flora worldwide, has long been considered a heterogeneous group (Webster 1994; Radcliffe-Smith 2001). Recent molecular phylogenetic analyses have clearly shown that Euphorbiaceae is nonmonophyletic, and consequently, Pandaceae , Phyllanthaceae, Picrodendraceae , Putranjivaceae , Peraceae , and Centroplacaceae have been removed from it, although these families all belong to the order Malpighiales together with the updated Euphorbiaceae (Euphorbiaceae s. str.; Angiosperm Phylogeny Group III 2009). Thus, the small unisexual flowers and trilocular capsule that characterize the plants of the former Euphorbiaceae are plesiomorphic or convergent characters. For example, Rafflesiaceae , the family with the world’s largest, unisexual but unilocular flowers, is embedded in the former Euphorbiaceae (Davis et al. 2007); the clade sister to Rafflesiaceae is now Euphorbiaceae s. str., and the lineage sister to (Rafflesiaceae + Euphorbiaceae s. str.) is split as Peraceae (Fig. 4.1). Of the seven former Euphorbiaceae families, Euphorbiaceae s. str. and Phyllanthaceae are by far the largest, with the former containing about 300 genera and about 7500 species, and the latter 54 genera and about 2000 species (Table 4.1). Webster (1994) noted an important morphological feature of Phyllanthaceae that clearly distinguishes them from Euphorbiaceae s. str.; the former has two ovules per locule whereas the latter only has one ovule per locule.

Fig. 4.1

Phylogenies of Malpighiales (left) and Phyllanthaceae (right). Former Euphorbiaceae families on the Malpighiales phylogeny are indicated in bold. Phyllanthaceae is divided into two subfamilies, Antidesmatoideae and Phyllanthoideae, the latter of which includes the tribe Phyllantheae. Phylogenetic relationships are based on Davis et al. (2005) for Malpighiales and Kathriarachchi et al. (2006) for Phyllanthaceae

Table 4.1 Families traditionally classified in Euphorbiaceae and tribal classification of Phyllanthaceae

Phyllanthaceae is a predominantly tropical family of shrubs and treelets and rarely of herbs and trees. Depending on the author, the family contains 54–60 genera, grouped into 2 monophyletic subfamilies and 10 well-defined, monophyletic tribes (Table 4.1). Of these, association with Epicephala moths is limited to Phyllantheae, which has more than half the species in the family (>1200 species) and contains Glochidion, Breynia, and Phyllanthus. Therefore, this chapter focuses entirely on the tribe Phyllantheae and reviews its diversity, phylogeny, and natural history. Recent molecular phylogenetic studies have greatly advanced our understanding of Phyllantheae classification, setting a cornerstone of evolutionary analysis on obligate pollination mutualism.

2 Genera of Phyllantheae

The generic classification of Phyllantheae is still contentious (Hoffmann et al. 2006; Kathriarachchi et al. 2006; Hoffmann 2008; van Welzen et al. 2014), and the number of genera is likely to change as additional progress is made. In this book, we use the following nine genus names to refer to the plants of Phyllantheae, acknowledging the fact that some are unnatural (paraphyletic) groups and should be redefined: Margaritaria, Plagiocladus, Lingelsheimia, Heterosavia (formerly a section of Savia ), Flueggea (including former Richeriella), Phyllanthus (including former Reverchonia), Sauropus, Breynia, and Glochidion (Table 4.2). Of these, the last three genera (Sauropus, Breynia, and Glochidion) are clearly embedded within Phyllanthus (Kathriarachchi et al. 2005, 2006). Breynia is further nested within Sauropus (Pruesapan et al. 2008, 2012).

Table 4.2 The genera of Phyllantheae used in this book

Hoffmann et al. (2006) proposed inclusion of Sauropus , Breynia , and Glochidion in Phyllanthus to avoid paraphyletic construction of the latter. By including the three embedded genera, Phyllanthus becomes a giant genus of >1200 species. A number of taxonomic and nomenclatural changes have been made for regional flora (Chakrabarty and Balakrishnan 2009; Wagner and Lorence 2011), but many more new combinations are necessary to accommodate fully the >400 species of Sauropus, Breynia, and Glochidion in Phyllanthus. Alternatively, van Welzen et al. (2014) proposed dividing Phyllanthus into >20 smaller genera because there is no morphological characteristic that defines the expanded Phyllanthus. In fact, the flowers, fruits, and growth forms of Phyllanthus are unusually diverse for a single genus, particularly if the genus is expanded to include Sauropus, Breynia, and Glochidion. Because the most recent molecular phylogenetic study of Phyllantheae only included approximately 10% of the constituent species (Kathriarachchi et al. 2006), an improved taxon sampling may group the species of Phyllanthus into many monophyletic, morphologically recognizable clades that can be recognized at generic rank. However, in the absence of a firm consensus at present, we adopt the traditional use of Phyllanthus, Sauropus, Breynia, and Glochidion in this book (Webster 1994; Radcliffe-Smith 2001; but see Chap. 12 for alternative names of Polynesian Glochidion species).

The genus Sauropus and the embedded Breynia have recently been thoroughly reviewed based on morphology and molecular data (Pruesapan et al. 2008, 2012; van Welzen et al. 2014). Based on the results of well-sampled phylogenetic analysis, van Welzen et al. (2014) expanded Breynia to include the Southeast Asian species of Sauropus, and reinstated the Australian Synostemon , a section of Sauropus, to generic rank, making each genus monophyletic and morphologically definable. However, we did not reflect these changes here due to the lack of consensus on whether to expand or divide Phyllanthus, as discussed above. On the other hand, the inclusion of Richeriella in Flueggea (Hoffmann et al. 2006) and of Reverchonia in Phyllanthus (Webster 2007) is generally not contradicted, so we adopted these changes in this book. The name Phyllanthus is derived from the Latin phyll (leaf) and anthus (flower), and its common name is leafflower . This is because the leaves on the lateral, flower-bearing branches of most Phyllanthus are flatly arranged on a horizontal plane, resembling the leaflets of compound leaves, and giving an overall impression that flowers are borne on (compound) leaves. Thus, Phyllanthus plants are relatively easy to recognize in the field compared to plants of other Phyllanthaceae genera. Phyllanthoid branching is a distinguishing morphological characteristic shared among most, but not all Phyllanthus species including Sauropus, Breynia, and Glochidion (Webster 1956; Fig. 4.2). In species with phyllanthoid branching, the leaves on the main (vertical) axes are reduced to scales (called cataphylls ), and normal leaves are only developed on lateral, flower-bearing axes. This is another reason that the lateral axes of Phyllanthus look like compound leaves, particularly in species in which the branchlets are deciduous. Phyllanthoid branching was once gained at an early stage of Phyllanthus diversification, probably as an adaptation to herbaceous or shrubby habits in open forest habitats, and was independently lost in several derived lineages, some of which are arboreal. Figure 4.3 summarizes the most recent understanding of Phyllantheae phylogeny based on molecular data (Kathriarachchi et al. 2006; Kawakita and Kato 2009), incorporating the most recent subgeneric arrangements within Phyllanthus (Kathriarachchi et al. 2006; Ralimanana and Hoffmann 2011, 2014; Ralimanana et al. 2013). The genus Phyllanthus is subdivided into about 15 subgenera and numerous sections, some of which are still poorly defined and require revision. Note that there are many more species of Phyllanthus, the phylogenetic positions of which have not been determined; only half of the entire Phyllanthus diversity is represented in the figure. An important and rather unexpected finding of molecular phylogenetic analyses was the correspondence between clades and biogeographic boundaries. For example, in Phyllanthus, the Neotropical species are grouped into three well-supported clades (although additional clades may appear when additional species are sampled), therefore there were probably only three dispersals from the Old World to the New World and no dispersal in the reverse direction. Therefore, traditional sections or subgenera that spanned both sides of the Pacific are all artificial. The Sauropus–Breynia clade is divided into two subclades (corresponding to Breynia and Synostemon of van Welzen et al. 2014), each occurring exclusively in Australia and Southeast Asia (with the exception of Sauropus macranthus that occurs in both regions). In addition, there is a large monophyletic group of Phyllanthus species consisting entirely of species endemic to Madagascar . Thus, long-distance dispersals were probably much less frequent than inferred from traditional taxonomy.

Fig. 4.2

Phyllanthoid (a) and nonphyllantoid (b) branching. (a) Vertical axis of Breynia retusa lacks normal leaves (arrows), and thus the branching is phyllanthoid. (b) Vertical axis of Flueggea suffruticosa bears normal leaves and flowers (arrows), retaining the ancestral nonphyllanthoid branching

Fig. 4.3

Phylogeny of the tribe Phyllantheae. The tree is based on the most recent phylogenetic analyses of the tribe by Kathriarachchi et al. (2006) and Kawakita and Kato (2009). Species richness of each terminal clade, compiled from various sources, is provided as the area of the clade triangle. The five lineages containing Epicephala moth-pollinated plants are indicated by black shadows on group names. Phyllanthus clades that have secondarily lost phyllanthoid branching are indicated by brackets around group names

3 Global Distribution and Diversity Patterns

The overall distribution of the five basal genera (Margaritaria, Plagiocladus, Lingelsheimia, Heterosavia, and Flueggea) is highly relictual. For example, Flueggea is widespread in the Paleotropics but also has fragmentary distributions in the Iberian Peninsula , Turkey , Caribbean , Ecuador , and northeastern Brazil (Webster 1984; Gemici 1993), which are most likely relicts (there is a single apparent dispersal to Hawaii; Hayden 1987). Similarly, Plagiocladus, Lingelsheimia, and Heterosavia have highly restricted distributions in West Africa , Africa and Madagascar , and the Caribbean , respectively (Table 4.2; Govaerts et al. 2000; Radcliffe-Smith 2001; Lebrun and Stork 2006; Hoffmann 2008), suggestive of range contractions from once broader distributions. On the other hand, distributions of the more derived genera (Phyllanthus, Sauropus, Breynia, and Glochidion) are likely the result of more recent dispersals. For example, Glochidion includes more than 300 species and ranges throughout the tropical parts of Asia , Australia , and the Pacific , with species colonizing as far east as the Pitcairn Islands (Govaerts et al. 2000). The Southeast Asian tropics have the highest diversity of Phyllantheae plants at both species and genus levels (Fig. 4.4, Table 4.2), although there are also notable diversity centers in New Caledonia (>110 spp.), Madagascar (ca. 60 spp.), Cuba (ca. 50 spp.), and Venezuela (ca. 60 spp.). Phyllantheae plants are less common in dense rainforests and thus have low diversity in the Amazonian basin. Much of the current Southeast Asian diversity is attributable to recent diversification of a few derived genera (Sauropus, Breynia, and Glochidion) rather than richness of major Phyllantheae lineages. The relative abundance of basal lineages (Margaritaria, Plagiocladus, Lingelsheimia, and Flueggea) in Africa , Madagascar , and South America (Table 4.2) may suggest a Gondwanan origin for the tribe as a whole.

Fig. 4.4

Global distribution of Phyllantheae plants. (a) Number of Phyllantheae plants occurring at each geographic region, as defined by Hollis and Brummitt (1992). Data were taken from Govaerts et al. (2000). Note that the geographic regions differ in size, which affects species abundance. (b) Approximate distributions of the five Phyllantheae lineages with Epicephala-pollinated species

4 Growth Form and Habitat

The tribe Phyllantheae has remarkable diversity of vegetative form and habitat . The plants range from very small shrubs to canopy-layer trees and a number of Phyllanthus lineages have become herbaceous (annual or perennial), which is rare among the predominantly woody Phyllanthaceae. Herbaceous species include weeds that have become naturalized in many tropical regions of the world (e.g., P. amarus , P. urinaria , and P. tenellus ). One Neotropical species, P. fluitans , is a free-floating aquatic (Macbride 1951). There are also a number of rheophytes , including P. bourgeoisii in New Caledonia (Schmid 1991), P. rheophyticus in Hainan (Li et al. 2008), and Sauropus heteroblastus in Indochina (van Welzen 2003). P. microcarpus is a scandent shrub that ascends by clinging to the surrounding vegetation (Luo et al. 2011a). P. mirabilis is the only succulent species (Chantaranothai 2005).

Phyllantheae plants are most frequently found in open habitats such as forest margins, roadsides, savannas, swamp edges, riverbanks, or coastal scrublands. However, some Phyllanthus and Sauropus species occur in forest understory, whereas Margaritaria and Glochidion constitute the canopy of rainforests. Large numbers of species have clear associations with limestone or serpentine vegetation (Webster 1956, 1957, 1958; Schmid 1991; Radcliffe-Smith 1996; van Welzen 2003; Thulin 2003; Gilbert and Thulin 2008; Hoffmann 2008), indicating the propensity of these plants to survive adverse soil conditions. Major radiations of Phyllanthus subgenera Gomphidium and Xylophylla took place in New Caledonia and Cuba , respectively (Webster 1956, 1957, 1958; Schmid 1991), where the land is abundant in serpentine substrates and is barely forested. Some Phyllanthus and Sauropus species are specialized to limestone cliffs and calcareous rock crevices (Webster 1970; Thulin 2005; Gilbert and Thulin 2008). P. warnockii (formerly Reverchonia arenaria ; Webster 2007) occurs on sand dunes in arid regions of the southwestern United States (Webster and Miller 1963).

Unlike supra-annual flowering of canopy trees in Asian tropical rain forests, the shrubby/herbaceous growth form and open habitat of Phyllanthus plants resulted in periodical or continuous flowering, which must have been a prerequisite for the association with pollinator moth partners, because the moths must reproduce periodically and synchronously with their host plants.

5 Floral Biology

The flowers of Phyllantheae plants are small (usually <1 cm in diameter) and unisexual. The basal lineages (Margaritaria, Plagiocladus, Lingelsheimia, and Flueggea) primarily consist of dioecious plants (although monoecious conditions occur in Lingelsheimia and Flueggea; Webster 1984; Radcliffe-Smith 2001), whereas the derived genera (Phyllanthus, Sauropus, Breynia, and Glochidion) are almost entirely monoecious . Flowers are usually borne singly or in clusters on leaf axils but rarely on the elongate inflorescence axis (e.g., Flueggea gracilis , P. acidus ). Cauliflory occurs in several Phyllanthus, Sauropus, and Glochidion species (Takeuchi 1999, 2003; van Welzen 2003; Thin 2007). Flowers lack petals (except in Heterosavia ; Hoffmann 2008), as is common to many groups within the family (Webster 1994; Radcliffe-Smith 2001; Hoffmann et al. 2006). Tepals are predominantly greenish regardless of the pollination system, although some non-Epicephala-pollinated plants have red-purple or white tepals. Thus, Phyllantheae flowers exhibit relatively poor floral display, and although flowers of Epicephala-pollinated plants are hardly conspicuous, inconspicuousness itself is not necessarily their exclusive feature. Nectar production has been confirmed in many taxa (Kawakita and Kato 2004a, 2009), although many, but not all Epicephala-pollinated plants are nonnectariferous (Kato et al. 2003). Flowering phenology has not been well studied, but both flowering and fruiting appear to be continuous throughout the year in most species. Clear seasonality occurs in some temperate taxa (e.g., P. flexuosus ). The most distinctive floral features associated with pollination mode are the structures of the pistils and stamens (Kawakita and Kato 2009; Kawakita 2010). The styles are usually free and bifid at the apices in non-Epicephala-pollinated plants, but are reduced to entire tips and are medially fused in most Epicephala-pollinated species (Kawakita and Kato 2009; Kawakita 2010). Similarly, filaments and anthers are usually free in non-Epicephala-pollinated plants, but are variously fused in species with Epicephala pollination. These morphological characteristics are likely associated with the pollination behavior by Epicephala females (Chap. 3). In the majority of species, the ovary consists of three locules , each of which has two ovules (Webster 1994; Radcliffe-Smith 2001). Thus, a single fruit contains six seeds . Exceptions include some Glochidion and Phyllanthus species that have 6, or rarely, 12–15 locules and hence twice the number of seeds. Fruits are predominantly capsules and seeds are dispersed by explosive dehiscence . Fleshy fruits (berries and drupes ) occur in a number of groups, including Flueggea, Breynia, and Phyllanthus sections Anisonema, Cicca, and Emblica, which are adapted for bird dispersal . Fruits of Margaritaria, Glochidion, and some Sauropus and Breynia are tardily dehiscent, and the seeds are coated with fleshy sarcotesta , which is also consumed by birds (seeds of one New Guinean Glochidion are consumed by cassowaries; Takeuchi 2003).

6 Natural History of Each Group

To date, Epicephala pollination has been uncovered in five separate lineages within Phyllantheae (Kawakita and Kato 2009). In this section, we describe the natural history of each lineage of Phyllantheae along the phylogeny in Fig. 4.3, with a special focus on pollination biology and association with Epicephala moths. Overall, there is substantial variation among lineages in the pollination system and mode of association with Epicephala, which are both critically important in understanding the origin and evolutionary dynamics of obligate pollination mutualism in Phyllanthaceae.

6.1 Margaritaria, Plagiocladus, Lingelsheimia, and Heterosavia

One of the most surprising results of recent molecular phylogenetic studies of Phyllanthaceae is the inclusion of Lingelsheimia and Heterosavia in Phyllantheae. Lingelsheimia is a small genus of six species distributed in equatorial Africa (Gabon , Zaire , and Tanzania ) and Madagascar , and was traditionally placed in Putranjivaceae (near Drypetes) due to its unusually large number of stamens (15–35; Webster 1994), although this placement has been questioned. Heterosavia , a genus of five species endemic to the Caribbean , was formerly a section of the genus Savia , which was shown to be polyphyletic in recent molecular phylogenetic studies (Kathriarachchi et al. 2005) and now contains only two species in the tribe Bridelieae, with the remaining species transferred to Wielandieae (Hoffmann et al. 2006). Heterosavia is unique among Phyllantheae with petals (Hoffmann et al. 2006). Another Phyllantheae lineage that was recently recognized at generic rank is Plagiocladus . This genus consists of a single central African species Plagiocladus diandrus , which was formerly a Phyllanthus, but molecular phylogenetic studies clearly placed it as a sister to Margaritaria (Kathriarachchi et al. 2006). Plagiocladus, Lingelsheimia, and Heterosavia have never been observed in the field, thus it is still unknown how they are pollinated or whether they are associated with Epicephala moths.

Margaritaria (Fig. 4.5) consists of 14 species that are widely distributed in the tropics, with concentrations of species in the Caribbean (4 spp.) and Madagascar (4 spp.). The plants are usually dioecious, with flowers possessing distinct nectaries. Although studies on pollination of the genus have been limited due to their low abundance and canopy-reaching habit, observation of Margaritaria indica in Japan indicated that the greenish flowers are frequently visited by nectar-seeking flies (Kawakita and Kato 2009). Information on the fruit-feeding insect fauna is also limited, but gracillariid larvae were not found from fruit samples of Margaritaria discoidea collected in Guinea (Kawakita and Kato 2009). Further studies are clearly needed to search more broadly for gracillariid seed feeders in Margaritaria. The seeds of some species of Margaritaria have a spectacularly metallic blue-green, fleshy sarcotesta, which is likely involved in seed dispersal by birds. The cellular structure of Margaritaria nobilis seeds has recently inspired a new fiber material that changes color as it stretches (Kolle et al. 2013).

Fig. 4.5

Genus Margaritaria. (a–c) M. indica. (d, e) M. discoidea. (a) Canopy of M. indica in subtropical forest of Okinawa Island, Japan. (b) Male flowers. (c) Female flowers. (d) M. discoidea in a grassland habitat in Guinea. (e) Fruiting branch. Photos (d, e) courtesy of Ryutaro Goto

6.2 Flueggea

Flueggea (Fig. 4.6) is another lineage of early branching Phyllantheae. The genus consists of 16 species, and as noted earlier (Section 4.4), their distribution is highly relictual. Some of these species are confined to the Iberian Peninsula , Turkey , Indochina , South Africa , the Caribbean , Ecuador , and northeastern Brazil , indicating substantial range contraction of a once more continuous distribution. There is one very widespread species ( Flueggea virosa ) that occurs throughout the tropics of Asia , Australia , and Africa , and another species (Flueggea suffruticosa) that occurs widely in the temperate regions of east Asia. F. virosa is one of three species in the genus that possess baccate fruits and is dispersed by birds (A. Kawakita, personal observation), which is probably responsible for its wide distribution. Flueggea neowawraea is one of the two Phyllantheae species that reached Hawaii (the other being P. distichus ), although it is unclear how they reached the islands because both plants have dry capsules and the seeds are dispersed by explosive dehiscence. F. gracilis , distributed in Southeast Asia , produces flowers in an elongated inflorescence axis, and the species was placed in another genus, Richeriella , based on this trait. The genus was subsumed to Flueggea after recent molecular phylogenetic studies (Hoffmann et al. 2006). Pollination biology and association with gracillariid moths have been well studied in the Japanese F. suffruticosa (Fig. 4.6). This species is dioecious as with most other species of the genus, and both male and female plants produce abundant nectar that is foraged by diurnal bees, flies, beetles, and butterflies (Kawakita and Kato 2009). Similar pollination biology was confirmed for F. virosa in Taiwan. Interestingly, F. suffruticosa is associated with a gracillariid moth, Conopomorpha flueggella , which visits female plants at night and lays eggs in the buds, flowers, or young fruits. The hatched larvae eat the developing seeds in the fruit, and each larva usually consumes all of the six seeds in its natal fruit to complete larval development. None of the moths collected on flowers possessed pollen on the proboscis or displayed pollination behavior on flowers, therefore they are pure seed parasites of Flueggea. The moth was initially identified as a species of Epicephala (Kawakita and Kato 2009), but subsequent taxonomic study described it under Conopomorpha , a genus that includes seed feeders of longan and lychee. However, the species is distantly related to the proper Conopomorpha (Kawakita et al. 2010) but is more closely related to Epicephala, thus it is best placed in a new genus (also see Chap. 5).

Fig. 4.6

Genus Flueggea. (a–e) F. suffruticosa: (a) flowering male individual in a temperate forest in Japan; (b) male flowers; (c) male flower showing nectariferous gland; (d) female flowers; (e) fruits. (f, g) F. virosa: (f) flowering male individual in tropical Taiwan; (g) fruiting branch. (h, i) F. jullienii: (h) male and female flowers of F. jullienii; (i) general habitat on a rocky riverbank in Laos. (j) F. acidoton in a spiny thicket developed on limestone soil in Jamaica

It is interesting to look further for gracillariid seed feeders in other species of Flueggea. To date, searches for larvae in F. virosa in Taiwan and Laos and Flueggea jullienii in Laos have yielded negative results, but examination of herbarium material suggests that the seeds of Ecuadorian Flueggea elliptica are infested by Epicephala-like larvae (see also Chap. 5). Whether the Ecuadorian moth is related to the Asian Conopomorpha flueggella, or is alternatively a product of more recent colonization of Flueggea by Epicephala associated with Neotropical Phyllanthus, remains to be determined.

6.3 Subgenus Isocladus and Sections Macraea and Ceramanthus

The subgenus Isocladus was proposed by Webster (1956) to group all of the Phyllanthus species with nonphyllanthoid branching . However, as shown by recent molecular phylogenetic analysis, phyllanthoid-branching taxa are not monophyletic, and consequently, the only species placed in this subgenus is the type species, P. maderaspatensis , an herbaceous plant that originally occurred in India but has since been introduced to many parts of the African, Asian, and Australian tropics. Molecular phylogenetic analysis placed P. maderaspatensis as sister to the clade including all of the other Phyllanthus species (Kathriarachchi et al. 2006). Sections Macraea and Ceramanthus (Fig. 4.7) are two of the four sections that were separated from former Isocladus. Of these, Macraea is a group of weedy herbs or subshrubs distributed in the Old World tropics, but some have colonized the Pacific islands, including P. chrysanthus , which is endemic to New Caledonia . P. myrtifolius , originally recorded from Sri Lanka, is planted as an ornamental bush in many tropical areas. The most abundant visitors to male and female flowers of P. ussuriensis in Japan and P. virgatus in Laos are ants that seek nectar in flowers and are likely the most effective pollinators (Kawakita and Kato 2009). Notably, the fruits of P. ussuriensis in Japan and P. chrysanthus in New Caledonia are infested by larvae of Epicephala moths. Although the behavior of adult moths has not been observed in the field, eggs are only found in developing fruits and not in pollination-stage flowers, suggesting that moths only visit young fruits to lay eggs and do not pollinate the plants. A single larva destroys all of the six seeds contained in a fruit. Ceramanthus is a Paleotropical section and consists of four species. The group contains P. cochinchinensis (Fig. 4.7), a forest understory shrub distributed in Indochina, the flowers of which are pollinated by Deltophora moths (Gelechiidae ) that are reported to consume Phyllanthus pollen by chemically breaking down sporopollenin on the surface of their proboscis (Luo et al. 2011b). The larvae feed on the leaves of P. cochinchinensis, therefore this is another form of reciprocally dependent mutualism. A similar mutualism was reported between P. rheophyticus and a different species of Deltophora, but the phylogenetic position of P. rheophyticus has yet to be determined. At present, ecological information is lacking for other members of the section Ceramanthus.

Fig. 4.7

Phyllanthus sections Macraea and Ceramanthus. (a–c) P. virgatus: (a) general habitat on disturbed land in Laos; (b) male flowers visited by the ant Solenopsis sp.; (c) mature fruits. (d, e) P. chrysanthus: (d) general habitat on forest edge of serpentine forest in New Caledonia; (e) male flowers. (f) P. myrtifolius used as hedge plant in Malaysia. (g) General habitat of P. cochinchinensis

6.4 Subgenus Kirganelia

The subgenus Kirganelia (Fig. 4.8) is a Paleotropical subgenus of about 15 species and is one of the five Phyllantheae lineages currently known to have mutualistic associations with Epicephala. The subgenus is most easily recognized by the baccate fruits , which is otherwise only known in Breynia within Phyllanthus s. lato. Pollination by host-specific Epicephala has been studied in P. reticulatus and P. microcarpus (both in section Anisonema ), which have particularly wide overlapping distributions from India and Sri Lanka to throughout Southeast Asia (Luo et al. 2011a; their presence in Africa remains to be verified). A detailed natural history of the obligate pollination mutualism is given in Chap. 11. The section Anisonema additionally contains four species endemic to Madagascar (Ralimanana and Hoffmann 2011). Although their pollination biology has not been studied, they share the fused style morphology with P. reticulatus and P. microcarpus, and herbarium specimens of the Madagascan species contained fruits infested by Epicephala larvae. Thus, obligate pollination mutualism is likely widespread within the section Anisonema.

Fig. 4.8

Phyllanthus subgenus Kirganelia. (a–c) P. flexuosus: (a) flowering individual in the understory of Cryptomeria plantation in temperate Japan; (b) fruiting individual; (c) male (black arrows) and female (white arrow) flowers. (d) Male and female flowers of P. oligospermus. (e, f) P. deplanchei: (e) general habitat in a dry sclerophyllous forest in New Caledonia; (f) female flowers. (g–i) P. reticulatus: (g) general habitat in a disturbed roadside land in tropical Taiwan; (h) male flower; (i) female flower. (j) Fruiting individual of P. microcarpus in a forest edge in Laos

However, there are species in this subgenus that have conspicuously colored flowers and lack association with Epicephala. For example, P. flexuosus , which is distributed in Japan , has male flowers with red-purple tepal s, and female flowers with widespread style s. Flowers emit an unpleasant odor during the daytime and are visited by dipteran and coleopteran insects (Kawakita and Kato 2009). Epicephala moths have not been found in any population studied to date, indicating that this species is free of Epicephala. P. oligospermus , which occurs in southern Japan and Taiwan , also has an overall similar ecology.

6.5 Subgenus Eriococcus and Section Antipodanthus

Eriococcus (Fig. 4.9) is a group of approximately 30 shrub species with marked diversity in the Indochina region. They are easily distinguished from other Phyllanthus by usually having tetramerous male flowers with only two stamens and four distinctly lacerate tepal s. Tepals are also often red-purple in color as in P. flexuous, which may be an indication of a common pollination system. However, to date, observing flower visitors in Eriococcus has been difficult. In P. liukiuensis occurring in Japan , a few pollen-bearing gall midge s were collected on flowers (Kawakita and Kato 2009), so dipterans may pollinate these plants. Another group of species in this subgenus has flowers with long pedicels that are remarkably erect in female flowers. In such species, the tepals of male flowers are imbricate , so they may have a pollination system that is entirely different from species with lacerate and colored tepals. Because Epicephala has not been recorded from any Eriococcus species, the plants in this subgenus likely have an unknown specialized pollination system. In addition, some Eriococcus species have unique, distinctly swollen fruit s with a hollow space between the seeds and the endocarp . This is probably an adaptation to escape attack by seed-feeding braconid wasp s because their seeds are frequently infested by braconid larvae, and because adult wasps oviposit through the fruit wall using exceptionally long ovipositor s. Section Antipodanthus (Fig. 4.10) is an entirely Australian group of 13 species (Webster 2002). The plants are subshrubs and occur in fire-prone, open forests. They are notable for the lack of phyllanthoid branching . Both male and female flowers have clearly visible nectaries , and hoverflies were regularly observed visiting flowers to lick nectar during daytime.

Fig. 4.9

Phyllanthus subgenus Eriococcus. (a–c) P. liukiuensis: (a) habitat on a limestone outcrop in subtropical Japan; (b) male flower; (c) female flower. (d–g) P. pulcher: (d) general habitat on a forest floor along a river in lowland Laos; (e) male flower; (f) female flower; (g) fruits. (h, i) P. pulcheroides: (h) fruits; (i) longitudinal section of fruit with fully developed seeds and large internal airspace. (j–l) P. sp.: (j) habitat on forest floor of secondary forest in Vietnam; (k) male flowers; (l) female flowers

Fig. 4.10

Phyllanthus section Antipodanthus. (a–d) P. dallachyanus: (a) general habitat in understory of fire-prone forest in Queensland, Australia; (b) male flower; (c) female flower; (d) hoverfly nectaring on male flower

6.6 Subgenera Afroswartziani, Swartziani (Including Former Reverchonia), and Tenellanthus

The subgenera Afroswartziani , Swartziani , and Tenellanthus (Fig. 4.11) comprise a clade that traditionally contains many herbs or small shrubs placed in various sections and subgenera. Ralimanana and Hoffmann (2011) and Ralimanana et al. (2013) reorganized these species into the above three subgenera to reflect phylogenetic relationships. Afroswartziani contains shrubs, trees, and rarely herbs that mainly occur in Madagascar and Africa , but many Asian species not sampled in previous molecular phylogenetic studies may also belong to this subgenus. A Madagascan species, P. madagascariensis , has male and female flowers with five obovate whitish green tepal s and a nectariferous disk , and are visited by nectar-seeking insects such as long-proboscid crane flies . Some Madagascan species (e.g., P. lokohensis ) have female flowers, the tepals of which form a globe surrounding the pistil that may function to keep the ovary away from Epicephala oviposition because their fruits are infested by Epicephala larvae (probably nonpollinating species). P. debilis , a global weed , also belongs to this subgenus. The subgenus Swartziani was revised by Ralimanana et al. (2013) to only include three species native to the New World . These are P. amarus , P. abnormis , and P. warnockii (formerly Reverchonia arenaria ). P. amarus is now a globally distributed weed , and in its introduced populations in Laos their flowers are pollinated by ants , and their fruits are parasitized by nonpollinating species of Epicephala. P. abnormis , native to the southeastern United States , is also parasitized by an Epicephala moth, as demonstrated by the presence of pupae in herbarium specimens. P. warnockii is an unusual Phyllanthus that grows on sand dune s of the southwestern United States . The flowers are dark red and are visited by flies and small bee s in the daytime. Tenellanthus is a well-defined subgenus of four species occurring in Madagascar , the Comoro Islands , and Africa , with one species, P. tenellus , becoming a pantropical weed . To date association with Epicephala has not been found in this subgenus.

Fig. 4.11

Phyllanthus subgenera Tenellanthus, Swartziani, and Afroswartziani. (a) P. tenellus (Tenellanthus) on roadside in New Caledonia. (b) P. nummulariifolius (Tenellanthus) in rainforest understory in Madagascar. (c) P. amarus (Swartziani) on sandy riverbank in its introduced range in Laos. (d–g) P. warnockii (Swartziani): (d) habitat on sandy desert in New Mexico, USA; (e) general habitat on sandy dune; (f) flowers; (g) fruits. (h–j) P. lokohensis (Afroswartziani): (h) flowering branch; (i) male flowers; (j) section of female flower showing airspace between tepals and ovary. (k) P. deblis on roadside in its introduced range in Japan

6.7 Subgenus Gomphidium

The subgenus Gomphidium is distributed in tropical Australia , New Guinea , and the Pacific Islands as far east as Tonga , with the greatest concentration of species in New Caledonia . The subgenus consists of about 150 species of shrubs or trees, of which 106 species occur in New Caledonia, all of which are endemic except P. bourgeoisii (Schmid 1991). New Caledonia (Fig. 4.12) is located in the Pacific Ocean about 1200 km from Australia and consists of the main island (Grande Terre ) and a number of surrounding small islands, with a total area of 18,580 km². New Caledonia was part of the Gondwana supercontinent and was separated from Australia as early as 66 Ma, although a significant proportion of the land mass was once submerged under the sea around approximately 35 Ma and many of the plants are thought to be descendants of later colonizations (Grandcolas et al. 2008). New Caledonia is renowned for its unique flora ; the islands have five endemic angiosperm families (Amborellaceae , Oncothecaceae , Paracryphiaceae , Phellinaceae , and Strasburgeriaceae ) and more than 100 endemic genera with the proportion of endemic species exceeding 90%. The earliest branching angiosperm Amborellaceae is only known from New Caledonia, although its fossils are known from other parts of the world. The uniqueness of the flora is exacerbated by the prevalence of serpentine rocks, which cover roughly 40% of the total land area. Serpentine rocks are ultrabasic, and plants occurring on serpentine substrates require particular adaptation to tolerate adverse, magnesium-rich soil conditions, resulting in high endemicity. Many of the notoriously invasive plants, such as Leucaena leucocephala , Aleurites fordii , and Psidium littorale , do not occur on serpentine soil, although they are abundant on nonserpentine regions of New Caledonia. The New Caledonian species of Phyllanthus are remarkably diverse in their habitat s and vegetative form s, representing one of the most spectacular adaptive radiation s in the plant kingdom (Fig. 4.13). It is the largest plant genus in New Caledonia with 114 recorded species, of which 96% are endemic. The diversity is exceptional for an island that is smaller in size than the state of New Jersey (22,610 km²) or the island of Sicily (25,710 km²). Their habitats range from rainforest understory, dry sclerophyllous forest , calcareous forest , riverbank , and maquis (scrubland developed on serpentine soil) with the majority of species being very narrow endemics. P. bourgeoisii , P. loranthoides , and P. dracunculoides are rheophyte s with narrow lanceolate leaves. P. peltatus is unique with peltate leaves. The subgenus Gomphidium contains two large sections, Gomphidium and Adenoglochidion , and both sections occur in New Caledonia. Male flowers have imbricate folded tepal s with narrow apical openings and connate stamen s in Gomphidium, or spread tepals and free stamens in Adenoglochidion (Fig. 4.14). Female flowers have nonbifid styles that are either fused in the middle or spread, although species with bifid styles are known in other parts of the Pacific (Webster 1986). Epicephala pollination has been confirmed in two New Caledonian species, P. bourgeoisii and P. aeneus , belonging to Gomphidium and Adenoglochidion, respectively (Chap. 3).

Fig. 4.12

Diverse habitats of New Caledonian Phyllanthus. (a) Araucaria-dominated scrubland on serpentine rock in Poro harboring P. pancherianus and P. bupleuroides. (b) Maquis vegetation near Prony in the southern part of Grande Terre. Note that the soil has the color of iron oxide and lacks introduced plants. (c) Rainforest along the valley of Troulala harboring P. serpentinus, P. buxoides, and P. pilifer. (d) Rainforest on the foot of Mt. Koghi harboring P. koghiensis and P. yaouhensis. (e) Maquis vegetation along the northwestern coast near Koumac harboring P. koumacensis, P. poumensis, and P. peltatus. (f) Humid rainforest of Massif du Panié on the northeastern coast harboring P. baladensis, P. valeriae, P. gneissicus, P. bourgeoisii, and P. loranthoides

Fig. 4.13

New Caledonian Phyllanthus (subgenus Gomphidium). (a) P. mouensis in montane forest of Mont Mou. (b) P. peltatus with peltate leaves in the understory of serpentine scrubland in Koumac. (c) P. poumensis on serpentine rock in Paagoumène. (d) P. serpentinus on the understory of serpentine scrub in Troulala. (e) P. valeriae on the understory of rainforest of Mont Panié. (f) P. mangenotii along stream in Cap Bocage. (g) P. aeneus on the understory of serpentine forest in Thio. (h) P. luciliae in coastal forest of Cap Bocage. (i) P. bourgeoisii on flood-prone habitat in Cascade de Bâ. (j) P. dracunculoides on flood-prone habitat in Tiwaka. (k) P. cf. montrouzieri on dry serpentinous scrubland in Kaala-Gomen. (l) P. koghiensis tree in rainforest habitat of Mont Koghi

Fig. 4.14

Flowers of New Caledonian Phyllanthus (subgenus Gomphidium). (a–h) Section Adenoglochidion (male and female flowers on upper and lower column, respectively): (a) P. peltatus; (b, f) P. serpentinus; (c) P. umbraecola; (d) P. pronyensis; (e) P. aeneus; (g) P. baladensis (photo courtesy of Eri Yamasaki) and (h) P. dorotheae. (i–p) Section Gomphidium (male and female flowers on upper and lower column, respectively): (i, m) P. poumensis; (j, n) P. kouaouaensis, (k, o) P. pilifer; (l, p) P. castus. An Epicephala egg is laid externally on the female flower in (n)

6.8 Madagascan Clade

There are seven Madagascan endemic Phyllanthus species that have until recently been considered members of Glochidion (Hoffmann and McPherson 2003; Fig. 4.15). This classification was based on their much reduced and entire style s, a characteristic most likely reflecting the shared Epicephala pollination syndrome . Indeed, these species are otherwise widely different from the true Glochidion in terms of floral and seed characters as well as growth form (Hoffmann and McPherson 2003). These plants are confined to the cloud forests in the northern part of Madagascar and are pollinated by Epicephala moths that feed on their seeds (Kawakita and Kato 2009).

Fig. 4.15

Madagascan Phyllanthus. (a) P. marojejiensis. (b) P. humbertii. (c) P. sambiranensis. (d) Cloud forest at approximately 2500 m a.s.l. of Mt. Marojeji, Madagascar where P. marojejiensis, P. humbertii, and P. sambiranensis occur in the understory. (e–g) P. marojejiensis: (e) male flower; (f) female flower; (g) fruit. (h, i) P. humbertii: (h) male flower; (i) female flower

Ralimanana and Hoffmann (2011) placed the above seven species and an additional three species in the subgenus Gomphidium , but molecular phylogenetic analysis suggests that they are distinct from Gomphidium known from New Caledonia and Australasia. Thus, the imbricate tepal s of male flowers and reduced styles used as the basis for their placement in Gomphidium is again a morphological convergence associated with Epicephala pollination. These Madagascan species are rather strongly united to subgenera Betsileani and Anisonemoides , both of which are also confined to Madagascar and contain 3 and 15 species, respectively. Collectively, these three lineages comprise a medium-sized clade that is entirely confined to Madagascar. Pollination biology is unknown for any of the species in Betsileani and Anisonemoides, but this information is critical to understanding the origin of Epicephala pollination in Madagascar. Epicephala pollination was studied in P. marojejiensis and P. humbertii at Mt. Marojeji in northeastern Madagascar. In both species, male flowers have imbricate tepals with either connate or free stamen s, and female flowers have very short and entire styles that lean inward (Fig. 4.15). Although flower visitation by Epicephala has not been directly observed, pollination by Epicephala is suggested by the following observations: (i) fruits of the two species were both infested by species-specific Epicephala larvae; (ii) an Epicephala female bearing pollen on the proboscis was collected on P. marojejiensis; and (iii) there was a near exclusive association between the pollinated status of female flowers and infestation by moth eggs, suggesting that ovipositing moths are the only pollinators (Kawakita and Kato 2009). Eggs are laid internally within the ovary, and a single larva destroys all of the six seeds in each fruit.

6.9 The New World Clade

This large clade of entirely New World species consists of the subgenus Xylophylla , section Nothoclema of subgenus Conami , and various Neotropical herb , subshrub , and aquatic species traditionally placed in divergent taxonomic groups. Of these, Xylophylla (Fig. 4.16) is a morphologically well-characterized and species-rich group with the center of diversity in the Caribbean Islands . The largest island in the Caribbean is Cuba , which has the greatest concentration of Xylophylla species. Its landmass is a mosaic of soil types, including serpentine and limestone ; thus, the radiation of Phyllanthus in Cuba is reminiscent of Phyllanthus diversification in New Caledonia. Many Xylophylla species possess flowers with fused tepal s and fused style s, and their seeds are infested by Epicephala larvae, suggesting that at least some species are pollinated by Epicephala moths. However, there are species with well-developed, showy tepals and distinct nectaries (Fig. 4.16), which are probably pollinated by diurnal bee s and flies . Two species in section Cauliflori have cauline inflorescences. Species of the section Xylophylla are characterized by flattened photosynthetic branches (phylloclade s) and an associated reduction of leaves (Fig. 4.16). They often occupy exposed habitats on limestone or coastal cliffs but are surprisingly robust to hurricane winds. Thus, the loss of leaves and substitution of photosynthesis by branches may be an adaptation to hurricane turbulence. P. arbuscula , a species with phylloclades, has bright red flowers, indicative of another unusual pollination system. Xylophylla is perhaps the most diverse lineage of Phyllanthus in terms of floral and vegetative adaptation, and further studies of the ecology of these plants are required. Section Nothoclema is another well-defined group of 11 tree species occurring widely from Mexico to Peru (Webster 2003). They can be easily distinguished from other Phyllanthus by their nonphyllanthoid branching , which is otherwise unknown in tree Phyllanthus. Epicephala moths are frequently found in the herbarium specimens of Nothoclema species, but the details of the association are still unknown. The clade sister to Nothoclema contains many herbs and subshrubs native to the New World with little known natural history. P. fluitans is a floating aquatic native to the Amazon but has also spread commercially as a water plant worldwide. P. niruri is used as a medicine to cure bladder stones. The members of the New World clade provide ample opportunity to study Phyllanthus–Epicephala association in the New World. The relationship likely varies from obligate pollination mutualism to pure parasitism, the latter involving nonpollinating moth species.

Fig. 4.16

Phyllanthus subgenus Xylophylla. (a) A flowering P. chamaecrystoides individual along stream in serpentine forest of Cuba. (b–d) P. williamioides: (b) flowering individual in serpentine scrubland in Cuba; (c) male flower; (d) female flower. (e–g) P. orbicularis: (e) flowering plant with brightly white flowers in serpentine scrubland in Cuba; (f) male flowers; (g) female flower. (h, i) P. cauliflorus: (h) cauline inflorescences in limestone forest of Jamaica; (i) female flower. (j–l) P. angustifolius: (j) habitat on limestone cliff in Jamaica; (k) individual bearing male and female flowers on phylloclades; (l) fruits. (m) P. arbuscula bearing male and female flowers on phylloclades. (n–p) P. nutans: (n) branch bearing erect male flowers; (o) branch with female flowers and fruits; (p) fruits (one on the lower right has exit hole excavated by Epicephala larva)

6.10 Sections Cicca, Aporosella, and Chorisandra

Sections Cicca , Aporosella , and Chorisandra each contain only one or two species and collectively form a monophyletic group of four species. Production of cauline inflorescences unites the four species morphologically. P. acidus (Fig. 4.17) is native to South America but is now widely cultivated in tropical parts of the world, particularly in tropical Asia. It is the most common fruit tree to be planted at home by the Lao people. The plant produces edible yellow drupe s, which are eaten fresh or candied in sugar or pickled in salt. P. acidus produces abundant fruits under cultivation apparently in the absence of Epicephala, although the pollinator of the species is yet unknown. Ecological information is unavailable for species of Aporosella and Chorisandra.

Fig. 4.17

Phyllanthus section Cicca. (a–c) P. acidus: (a) fruiting tree in a village of Laos; (b) cauline inflorescences; (c) inflorescence with male flowers and young fruits

6.11 Subgenus Emblica

The subgenus Emblica (Fig. 4.18) was traditionally confined to a few Asian shrub species, but Ralimanana et al. (2013) expanded the subgenus to include the herbaceous section Urinaria , which has clear phylogenetic affinity to the species traditionally included in Emblica. One such herbaceous species is P. lepidocarpus , the flowers of which produce abundant nectar and are effectively pollinated by nectar-seeking ant s. The plants are self-compatible and commonly attain 100% fruit even when non-ant visitors are experimentally excluded from flowers. The fruits of P. lepidocarpus are infested by Epicephala parasitica , which lacks the pollination behavior and oviposits in young fruits (Kawakita and Kato 2016). The resulting larvae destroy all of the seeds contained in each fruit. P. emblica , known as Indian gooseberry , is widely distributed in Southeast Asia and is common along the edges of seasonally dry tropical forest s. The plant produces numerous male flowers among which female flowers are embedded, and is visited by honey bee s in its native range in China . The plants produce near- spherical drupe s about 2 cm in diameter, which is an exceptionally large nondehiscent fruit otherwise unknown in Phyllanthus. As with P. acidus, the edible fruits are very sour and popularly eaten in many parts of tropical Asia, but the natural consumer of the fruit is unknown, and thus no information is available on the mechanism of seed dispersal . Other members of the subgenus Emblica are still poorly known. Because nectaries are well developed in flowers of Emblica, they are most likely pollinated by unspecialized, nectar-seeking insects as in P. lepidocarpus and P. emblica.

Fig. 4.18

Phyllanthus subgenus Emblica. (a–c) P. lepidocarpus: (a) weedy habitat on roadside pebbles in Japan; (b) flowering and fruiting branch; (c) male flower; (d) female flower; (e) the ant Tetramorium sp. nectaring on male flower. (f–h) P. emblica: (f) flowering branch in Guangzhou, China; (g) male flowers; (h) fruits sold at market in Vientiane, Laos. (i–l): P. sp.: (i) habitat on limestone forest in northern Laos; (j) flowering branch; (k) male flowers; (l) male flowers with nectar in flower

6.12 Sauropus

The genus Sauropus as traditionally circumscribed is clearly a paraphyletic group with respect to the embedded Breynia (Pruesapan et al. 2008, 2012). Within the Sauropus–Breynia clade, the Australian species of Sauropus forms a monophyletic group and is the earliest branching lineage. Earlier taxonomists placed Australian Sauropus in a separate genus, Synostemon , and van Welzen et al. (2014) reinstated Synostemon to the generic rank to refer to this Australian clade. The remaining Southeast Asian Sauropus and Breynia were grouped by van Welzen et al. (2014) in the expanded Breynia. The expanded Breynia is divided into the subgenera Sauropus and Breynia, the latter of which is further divided into sections Cryptogynum and Breynia. However, because Sauropus and Breynia are deeply embedded in Phyllanthus, whether to adopt the generic changes proposed by van Welzen et al. (2014) is tightly linked to the issue of whether to subsume Sauropus, Breynia, and Glochidion in an expanded Phyllanthus. Due to a lack of consensus at present, we followed the traditional circumscription of Sauropus and Breynia, while acknowledging that the former is a paraphyletic group. Sauropus (Fig. 4.19) produces flowers that are among the most unusual of all Phyllantheae. In most Southeast Asian species, the tepal s of both male and female flowers are spread flat on a horizontal plane, and as a result, the flowers are more or less disclike. In male flowers, the tepals are further inflexed toward the androecium, and together with the short, horizontally spread androecium , form three small cavities on the surface of the disc-shaped flower. As the anthers are held toward the cavities, pollen can only be picked up from inside these small cavities. The bifid style s of female flowers are also spread horizontally, and the stigmatic surface faces outward. Thus, as in male flowers, female flowers can only pick up pollen from flower visitors that approach or hold on to the flower in a particular manner. Several Sauropus species produce cauline inflorescences (e.g., S. racemosus ) or are even geoflorous ( S. discocalyx ). Species that produce flowers in forest understory habitats tend to possess red-purple-colored tepals. Despite these interesting floral morphological characteristics, the pollination system of Sauropus is still unknown. None of the Sauropus species studied to date host Epicephala larvae in the fruit, therefore the moths are not involved in the pollination of Sauropus. Their pollination system holds the key to understanding the evolution of Epicephala moth pollination in Breynia. The ecology of Australian Sauropus is much less well known. Most species are rare and have very limited distributions, and new species continue to be found (Telford and Naaykens 2015). One Southeast Asian Sauropus species ( Sauropus androgynus ) is cultivated as a leaf vegetable in many parts of tropical Asia.

Fig. 4.19

Genus Sauropus. (a–b) S. androgynus: (a) general habitat at forest edge on limestone in Laos; (b) fruits. (c) S. cf. quadrangularis in the understory of seasonal dipterocarp-dominated tropical forest in Laos. (d) S. macranthus in the understory of evergreen broad-leaved forest in mountainous region of Laos. (e–l) Flowers of Sauropus species (male and female flowers on upper and lower column, respectively): (e, l) S. cf. quadrangularis; (f, j) S. brevipes; (g, k) S. androgynus; (h, j) S. macranthus. Photographs of flowers are on the same scale

6.13 Breynia

Breynia (Fig. 4.20) contains 35 species distributed throughout the Australasian tropics extending far east to Fiji (Govaerts et al. 2000). Several continental species are very widely distributed, which is likely due to their bird-dispersed fruits. For example, the distribution of Breynia vitis-idaea extends from Pakistan in the west to Japan and the Philippines in the east (Chakrabarty and Gangopadhyay 1996). The flowers of most Breynia species resemble those of B. vitis-idaea, so Epicephala moth pollination is likely widespread in the genus. However, at least one species, Breynia retusa (Fig. 4.20), does not have an association with Epicephala (Kawakita and Kato 2009). The flowers of B. retusa are very different from those of B. vitis-idaea, suggesting that the plant has an alternative pollination mechanism. Fruit characteristics are also variable in the genus. Most species, including B. vitis-idaea, produce berries, whereas others produce dry capsules containing seeds with a fleshy sarcotesta (Fig. 4.20).

Fig. 4.20

Genus Breynia. (a–e) B. retusa: (a) general habitat on forest edge in Laos; (b) flowering branch; (c) male flowers; (d) female flowers; (e) fruiting individual. (f) Fruits and seeds of B. fruticosa. Note that the fruit is a capsule, and the seeds have an orange sarcotesta

B. disticha , a native of New Caledonia , has a horticultural variety that produces strongly variegated leaves, which is known as “Snow Bush ” and is popularly cultivated as an ornamental plant in tropical parts of the world.

6.14 Phyllanthodendron

Subgenus Phyllanthodendron (Fig. 4.21) contains approximately 10 species occurring in Southeast Asia . Species of this subgenus have characteristic bell-shaped flowers that are unlike those of any other Phyllanthus. In addition, their growth form and leaf traits more resemble those of Glochidion than those of most Phyllanthus. Thus, the subgenus is often treated at generic rank (Li et al. 2008), and molecular phylogenetic analysis provided support for its unusual placement; Phyllanthodendron is sister to Glochidion and distantly related to all other Phyllanthus (Kathriarachchi et al. 2006).

Fig. 4.21

Phyllanthus subgenus Phyllanthodendron. (a, b) P. roseus: (a) flowering individual on forest edge of seasonal tropical forest in Laos; (b) flowers and fruit. (c–e) P. cf. caudatifolius: (c) general habitat on rocky riverbank in Laos; (d) branch with male flowers; (e) close-up of male flower showing the fused anthers

Pollination occurs during the daytime by numerous flies that visit flowers for nectar in P. roseus . None of the species studied to date has an association with Epicephala, although the seeds of P. roseus are consumed by braconid wasp larvae. The braconid wasp has a very long ovipositor that probably coevolved with the swollen fruit of P. roseus; its fruit has a large airspace between the fruit wall and ovule that likely distances the ovule from ovipositing wasps. The association between the Phyllanthus fruit and the braconid seed parasite reminds us of the evolutionary arms races between balloonlike fruit of a balloon vine ( Cardiospermum , Sapindaceae ) and its seed-sucking long-proboscid soapberry bug s (Carroll and Boyd 1992) and between the thick fruit pericarp of Japanese camellia and its seed-parasitic weevil s with long rostrums and long ovipositors (Toju 2009). P. mirabilis , native to Thailand , is the only Phyllanthus to be caudiciform , or with a succulent trunk. The species is cultivated as an ornamental plant.

6.15 Glochidion

Glochidion (Fig. 4.22) contains some of the tallest plants of all Phyllantheae. In the lowland rainforest of Malaysia , G. arborescens commonly exceeds 20 m, and others may reach the canopy layer. However, the majority of Glochidion species occur along forest edge s or roadside s and are typically small-sized tree s or treelet s. Few are forest understory shrub s. G. obovatum , endemic to Japan, occurs in habitat that is prone to deer browsing , and consequently, the stem apices of young plants are modified to thorn s. In areas with large deer populations, G. obovatum literally dominates the vegetation due to its effective defense against deer browsing provided by the thorns. All Glochidion species studied to date are pollinated by Epicephala and share the same basic pollination ecology as described in Chap. 3. As the specialized, fused style morphology is shared among all the members of the genus, it is unlikely that other pollination systems exist in the genus. There is considerable variation in the shape of female flowers among different Glochidion species (Fig. 4.23). Although the reason for this variation is unknown, morphological differences may partly facilitate host recognition by ovipositing Epicephala females. Even greater variation is found in the fruit size and the number of locule s per fruit, which should have major consequences on the proportion of seeds consumed by larvae. Some Glochidion species, such as G. littorale , have fruits exceeding 2 cm in diameter, each containing >20 seeds. There may be selection on Glochidion plants to produce larger fruits and more seeds per fruit to escape seed predation by Epicephala larvae. However, if Glochidion fruits evolve to become larger, the moths may adapt by laying more eggs per flower to consume a greater proportion of the seeds available. Therefore, it is interesting to examine whether such coevolutionary escalation is the cause of the large variation in fruit size among Glochidion species.

Fig. 4.22

Genus Glochidion. (a) G. sumatranum on forest edge of lowland rainforest in Malaysia. (b) Canopy-reaching tree of G. philippicum in Taiwan. (c) Forest floor shrub of G. sp. in lowland rainforest in Malaysia. (d) Thorny young plant of G. obovatum in temperate Japan

Fig. 4.23

Flowers and fruits of Glochidion. (a–h) female flowers: (a) G. lanceolatum (Japan); (b) G. philippicum (Taiwan); (c) G. sumatranum (Sarawak, Malaysia); (d) G. ferdinandii (Sydney, Australia); (e) G. sp. (Laos); (f) G. sp. (Laos); (g) G. sphaerogynum (Vietnam); (h) G. sp. (Laos). (i–m) fruits: (i) G. obscurum (Sarawak, Malaysia); (j) G. arborescens (Sarawak, Malaysia); (k) G. sericeum (Sarawak, Malaysia); (l) G. philippicum (Taiwan); (m) G. littorale (Sarawak, Malaysia). Photographs (i–m) are in approximately the same scale. (n) G. rubrum fruit (Japan) showing dehisced capsule and seeds with orange sarcotesta