Synopsis of Trichosanthes (Cucurbitaceae) based on recent molecular phylogenetic data.

The snake gourd genus, Trichosanthes, is the largest genus in the Cucurbitaceae family, with over 90 species. Recent molecular phylogenetic data have indicated that the genus Gymnopetalum is to be merged with Trichosanthes to maintain monophyly. A revised infrageneric classification of Trichosanthes including Gymnopetalum is proposed with two subgenera, (I) subg. Scotanthus comb. nov. and (II) subg. Trichosanthes, eleven sections, (i) sect. Asterospermae, (ii) sect. Cucumeroides, (iii) sect. Edulis, (iv) sect. Foliobracteola, (v) sect. Gymnopetalum, (vi) sect. Involucraria, (vii) sect. Pseudovariifera sect. nov., (viii) sect. Villosae stat. nov., (ix) sect. Trichosanthes, (x) sect. Tripodanthera, and (xi) sect. Truncata. A synopsis of Trichosanthes with the 91 species recognized here is presented, including four new combinations, Trichosanthes orientalis, Trichosanthes tubiflora, Trichosanthes scabra var. pectinata, Trichosanthes scabra var. penicaudii, and a clarified nomenclature of Trichosanthes costata and Trichosanthes scabra.

Introduction

Background

L. is the largest genus in the Cucurbitaceae family, with over 90 species. The genus has its center of diversity in Southeast Asia, but ranges from India throughout Asia east to Taiwan, the Philippines and Japan, and southeast to New Guinea, Australia, Fiji and Vanuatu (de Wilde and Duyfjes 2010). The snake gourd ( L.) is a popular vegetable in South and Southeast Asian cuisine and PageBreakcultivated in tropical and subtropical regions around the globe. Arn. includes four species (de Wilde and Duyfjes 2006) and ranges from India through China and Southeast Asia into the Malay archipelago, but does not occur in New Guinea and Australia (de Wilde and Duyfjes 2010).

Morphology and classification

are mostly stout perennial climbers, 3–30 m long, dioecious, less frequently monoecious, with branched tendrils, distinctly fringed petals, and often egg-sized brightly colored fruits. Dioecy, variation in vegetative morphology (esp. in juvenile plants), and incomplete herbarium collections, complicate taxonomical studies and have contributed to the description of nearly 300 taxa (de Wilde and Duyfjes 2010; IPNI 2011).

No full taxonomic treatment of the genus exists, but in recent years regional revisions have been published for most of its distribution: India (Chakravarty 1959; Jeffrey 1980a; Jeffrey 1982), China (Lu et al. 2011; Yueh and Cheng 1974; Yueh and Cheng 1980), Thailand (Duyfjes and Pruesapan 2004), Cambodia, Laos and Vietnam (Keraudren-Aymonin 1975), Malaysia, Indonesia, the Philippines and Papua New Guinea (Rugayah and de Wilde 1997; Rugayah and de Wilde 1999; de Wilde and Duyfjes 2004; de Wilde and Duyfjes 2010), Australia (Telford 1982; Cooper and de Boer 2011) and Japan (Ohba 1984).

Infrageneric classifications of the genus have been proposed by various authors (Yueh and Cheng 1974; Jeffrey 1980b; Chen 1985; Huang et al. 1997; Rugayah and de Wilde 1999; de Wilde and Duyfjes 2004). The most recent classifications of the genus (Rugayah and de Wilde 1999; de Wilde and Duyfjes 2004) propose six sections: (i) sect. , (ii) sect. (Gaertn.) Kitam. including subsect. (Gaertn.) Kitam. and subsect. (C.Y.Cheng & Yueh) Rugayah, (iii) sect. Rugayah, (iv) sect. C.Y.Cheng & Yueh, (v) sect. (Ser.) Wight including subsect. C.Jeffrey ex S.K.Chen and subsect. (C.Y.Cheng & Yueh) C.Jeffrey ex S.K.Chen, and (vi) sect. W.J.de Wilde & Duyfjes. However, both Rugayah and de Wilde (1999) and de Wilde and Duyfjes (2004; 2010) are reserved in their infrageneric classifications, and mention a need for further investigation.

Pollen morphology has also been used for infrageneric classification in the genus (Khunwasi 1998; Pruesapan and Van Der Ham 2005; Huang et al. 1997), but as a character is very variable in Cucurbitaceae, and its taxonomic value is not clear (Schaefer and Renner 2011). Palynological studies (Pruesapan and Van Der Ham 2005) have indicated that a variety of pollen types exist in including 3(-4)-porate and 3(-4)-colporate pollen with psilate, perforate, verrucate, reticulate, and regulate ornamentation. Their study of pollen from 37 species distinguishes five pollen types, two of which are further divided into subtypes, and categorized these using exine ornamentation patterns for the major types and ectoaperture characters for the subtypes.

strongly resembles certain species, but lack thread-like fringes on the petals, and the overall shape of the folded petals in the mature bud is elongate (short and rounded in ) (de Wilde and Duyfjes 2006). A revision of the genus was published by de Wilde and Dufyjes (2006), with minor nomenclatural changes published later (de Wilde and Duyfjes 2008). Cogniaux (1881) divided into two sections, (i) sect. containing the type (Wight & Arn.) Cogn. from southern India and Sri Lanka, and (ii) sect. (M.Roem.) Cogn. containing the Southeast Asian and Malesian species. Later authors did not follow this classification (Jeffrey 1980a; Philcox 1997; de Wilde and Duyfjes 2006).

Recent molecular phylogenetic studies

The molecular phylogenetic study of by de Boer et al. (Submitted) shows that and are both non-monophyletic, but together form a clade with high support in the Bayesian tree and weak support in the ML tree (0.99/62). This indicates that should be merged with , and that a revised infrageneric classification is necessary. Some previously recognized sections in and are well supported, but others need to be described or redefined.

Results and discussion

Molecular phylogeny

The molecular phylogeny of and by de Boer et al. (Submitted) has nomenclatural implications for the species in and the infrageneric classification of . The species of are placed in different clades within , with the sect. , including the type , grouping in a well-supported clade (1.00/84) together with species of sect. and sect. . The sect. , consisting of the three other species in the genus, W.J.de Wilde & Duyfjes, (Lour.) Merr., and (Lour.) W.J.de Wilde & Duyfjes, forms a well-supported clade (1.00/86) together with the taxa in sect. .

Within the support for the two clades here defined as subgenera (1.00/94) and (1.00/97) is high. However,splitting the genus into two genera corresponding to subg. and subg. would not improve clarity, as both would consist of species with fringed and fringeless corollas. Maintaining a large is in accordance with the recent taxonomic revisions of the genus (de Wilde and Duyfjes 2010; Chakravarty 1959; Lu et al. 2011; Duyfjes and Pruesapan 2004; Keraudren-Aymonin 1975; Cooper and de Boer 2011; Ohba 1984), and is the alternative that best provides taxonomic stability.

Some proposed sections in and are well supported: (i) sect. (1.00/93), including subsect. (0.99/-) and subsect. (0.99/69), (ii) sect. (1.00/75), and (iii) sect. (1.00/100). The subsections of sect. are statistically supported, but subsect. consists solely of accessions of Lour. and species that have been reduced to its synonymy (Cooper and de Boer 2011). Sect. is only weakly supported (0.83/65), primarily due to the low support for inclusion of its type, (Ser.) Wight. The subsections of are not supported, and taxa belonging to subsect. are nested in different locations within subsect. . Sect. is not supported by the analysis, and could possibly form a grade at the base of sect. . However, morphological support for this section is strong as all taxa share characters of flower morphology, i.e. fringeless corollas. Sect. Cheng & Yueh, which in its original sense included the species related to Maxim. and Blume (Yueh and Cheng 1974; Rugayah and de Wilde 1999; de Wilde and Duyfjes 2004), is not supported. However, a clade consisting of Maxim., Hayata, Hayata, Hand.-Mazz., Harms, and Miq. is strongly supported (1.00/99). Section , in its original sense including C.B.Clarke, Craib, Hayata (Yueh and Cheng 1980), and C.Y.Wu (Jeffrey 1980b), is not supported, as the three latter species all end up elsewhere in the phylogenetic tree.

was placed in sect. by Yueh and Cheng (1974), and later in subsect. by Jeffrey (1980b), but subsequently moved to sect. by Rugayah and de Wilde (1999). In the protologue of Duyfjes and Pruesapan (2004), the authors stated that the three species , and form a coherent, distinct group based on presence of white fruit pulp, male flowers with the stamens inserted low in the receptacle tube, and a pseudo-ovary. The molecular evidence shows that all accessions of these species in this study form a well-supported monophyletic group, confirming the observations by Duyfjes and Pruesapan (2004) and warranting placement of these taxa in a new section, sect. H.J.de Boer.

Cooper and Ford (2010) and Cooper and de Boer (2011) placed F.Muell. ex Cogn. in section as it has obovate seeds with an entire broad marginal band similar to those found in Malesian species of section . However, Huang et al (1997) proposed to place it in section subsect. based on it pollen morphology. The current phylogenetic data place the accessions of as sister (1.00/91) to a well-supported clade (1.00/84) consisting of sections , , and , and the species is here placed in a separate section, sect. (Yueh & L.Q.Huang) H.J.de Boer.

Pollen

Species with colporate ectoaperturate pollen form two monophyletic groups in subg. , one including sections , , , and , and the other including sect. , with (data from R. van der Ham 2011, pers. comm.). The latter clade is sister to the clade consisting of sections , and (1.00/84). The remaining sections in subg. have porate ectoapertures, and varying exine ornamentation including psilate, (micro-)reticulate, perforate, verrucate, and rugulate pollen (Huang et al. 1997; Pruesapan and Van Der Ham 2005). in sect. has 3-colporate, rugulate-reticulate pollen (Khunwasi 1998; van der Ham et al. 2010), whereas in in sect. the pollen is 3-porate and microreticulate (R. van der Ham 2010, pers. comm.).

The other genera in the tribe Sicyoeae have colpate-colporate pollen, similar to that in many other distantly related groups in Curcurbitaceae (Schaefer and Renner 2011). In the light of the molecular data and the phylogenetic analysis (de Boer et al. Submitted), a transition from colporate to porate apertures has taken place three times in the evolutionary history of , in the common ancestors of: 1) sect. ; 2) sect. ; and 3) sections , and .

Taxonomy and classification

A revision of the infrageneric classifications suggested by previous authors on the basis of morphological studies (Yueh and Cheng 1974; Jeffrey 1980b; Huang et al. 1997; Rugayah and de Wilde 1999; de Wilde and Duyfjes 2004) is here proposed on the basis of the molecular phylogenetic data (de Boer et al. Submitted). A synopsis is presented in which we attempt to assign all 91 species recognized here to sections using the clades recovered in the phylogenetic analysis as a framework, along with a plenitude of data from macromorphological studies of herbarium vouchers (Chakravarty 1959; Jeffrey 1980a; Jeffrey 1980b; Jeffrey 1982; Telford 1982; Ohba 1984; Rugayah and de Wilde 1997; Rugayah and de Wilde 1999; Duyfjes and Pruesapan 2004; de Wilde and Duyfjes 2004; de Wilde and Duyfjes 2006; Cooper and Ford 2010; de Wilde and Duyfjes 2010; Lu et al. 2011; Cooper and de Boer 2011) and palynological work (Huang et al. 1997; Pruesapan and Van Der Ham 2005; van der Ham et al. 2010). Synonyms are only included if these are new or relevant for this paper. Names that have been placed in synonymy by previous authors can be found in the above-cited morphological studies.

L. (1753) Sp. Pl. 2: 1008 – Type: L. [= L.]

(Kurz) H.J.de Boer, comb. nov. – subg. Kurz (1877) J. Asiat. Soc. Bengal, Pt. 2, Nat. Hist. 46: 99. – Lectotype, designated here: Lour. [ = Blume]

Naud., nom. illeg. (1862) Ann. Sci. Nat., Bot. sér. 4, 16: 172. – Type: Roxb. [ = Blume]

Rugayah (1999) Reinwardtia 11: 232. – Type: Ruguyah.

Rugayah (1999) Reinwardtia 11: 252

Rugayah (1999) Reinwardtia 11: 253

Merr. & L.M.Perry (1949) J. Arnold Arbor. 30: 59

Rugayah (1999) Reinwardtia 11: 254

Harms (1925) Bot. Jahrb. Syst. 60: 160

C.Y.Cheng & Lu Q.Huang (1996) Bull. Bot. Res., Harbin 16: 503

W.E.Cooper & A.J.Ford (2010) Austrobaileya 8: 126

Harms (1925) Bot. Jahrb. Syst. 60: 160

Harms (1925) Bot. Jahrb. Syst. 60: 159

(Ser.) Wight (1840) Madras J. Lit. Sci. 12: 52. – Ser. (1825) Mém. Soc. Phys. Genève 3: 27, t. 5. – Type: Ser. [ = (Ser.) Wight]

Bedd. (1864) Madras J. Lit. Sci. III, 1: 47

Cogn. (1881) Monogr. Phan. [A.DC. & C.DC.] 3: 369

(Lam.) Voigt (1845) Hort. Suburb. Calcutt. 58

Cogn. (1881) Monogr. Phan. [A.DC. & C.DC.] 3: 385

Roxb. (1832) Fl. Ind. 3: 703

Blume (1826) Bijdr. Fl. Ned. Ind. 15: 935

Duyfjes & Pruesapan (2004) Thai Forest Bull., Bot. 32: 84

H. Lév. (1911) Repert. Spec. Nov. Regni Veg. 10: 148

Merr. (1918) Philipp. J. Sci., C 13: 332

Merr. (1929) Univ. Calif. Publ. Bot. 15: 299

Rugayah (1999) Reinwardtia 11: 258

Duyfjes & Pruesapan (2004) Thai Forest Bull., Bot. 32: 85

C.Y.Wu ex C.Y.Cheng & C.H.Yueh (1974) Acta Phytotax. Sin. 12: 438

Rugayah (1999) Reinwardtia 11: 260

Blume (1826) Bijdr. Fl. Ned. Ind. 15: 936

W.J.de Wilde & Duyfjes (2004) Sandakania 14: 19

Duyfjes & Pruesapan (2004) Thai Forest Bull., Bot. 32: 86

Kundu (1939) J. Bot. 77: 11

Rugayah (2000) Reinwardtia 11: 419

Duyfjes & Pruesapan (2004) Thai Forest Bull., Bot. 32: 89

Hayata (1911) J. Coll. Sci. Imp. Univ. Tokyo 30. Art. 1: 117

(Naud.) Cogn. (1881) Monogr. Phan. [A.DC. & C.DC.] 3: 377

Rugayah (1999) Reinwardtia 11: 265

Rugayah (1999) Reinwardtia 11: 266

Rugayah (1998) Reinwardtia 11: 218

W.E.Cooper (2011) Austrobaileya 8: 381

Rugayah (1999) Reinwardtia 11: 269

Duyfjes & Pruesapan (2004) Thai Forest Bull., Bot. 32: 90

F.M.Bailey (1900) Queensland Agric. J. 7: 349

Merr. & Chun (1934) Sunyatsenia 2: 20

F.Muell. in Benth. (1867) Fl. Austral. 3: 314

Rugayah (1999) Reinwardtia 11: 271

Rugayah (1999) Reinwardtia 11: 273

Blume (1826) Bijdr. Fl. Ned. Ind. 15: 936

A. Gray (1854) U.S. Expl. Exped., Phan. 15: 645

C.Y.Wu ex C.Y.Cheng & C.H.Yueh (1980) Acta Phytotax. Sin. 18: 351

C.H.Yueh (1996) Bull. Bot. Res., Harbin 10: 500

C.Y.Cheng & C.H.Yueh (1974) Acta Phytotax. Sin. 12: 440

Rugayah (1999) Reinwardtia 11: 275

C.Y.Cheng & C.H.Yueh (1980) Acta Phytotax. Sin. 18: 349

Lour. (1790) Fl. Cochinch. 2: 589

Rugayah (1999) Reinwardtia 11: 277

(Ser.) Wight (1840) Madras J. Lit. Sci. 12: 52

Cogn. (1881) Monogr. Phan. [A.DC. & C.DC.] 3: 384

(M.Roem.) H.J.de Boer, comb. nov. – M.Roem. (1846) Fam. Nat. Syn. Monogr. 2: 48. – sect. (M.Roem.) Cogn. (1881) Monogr. Phan. [A.DC. & C.DC.] 3: 390. – Type: Lour. [ = Blume]

Blume (1826) Bijdr. Fl. Ned. Ind. 15: 933. — Type: Blume s.n. barcode L0589632, (lectotype L, designated by de Wilde and Duyfjes (2006); 2 isotypes L), Java, Indonesia. Heterotypic synonyms: Lour. (1790) Fl. Cochinch. 1: 156. – (Lour.) Merr. (1919) Philipp. J. Sci. 15: 256 – Type: †. Lour. (1790) Fl. Cochinch. 1: 595. – (Lour.) Kurz (1871) J. Asiat. Soc. Bengal, Pt. 2, Nat. Hist. 40: 57 –Type: Loureiro s.n. (BM), Vietnam. Roxb. (1832) Fl. Ind. 3: 711 – Type: Wallich Cat. 6749 (holotype? K-W), Dacca, Bangladesh. Note: The existence of Ser. (1828) Prodr. [A.P. de Candolle] 3: 315 blocks the transfer of , based on the basionym , to . The second name in line of priority would be , based on the basionym . However, the combination M.Roem. (1846) Fam. Nat. Syn. Monogr. 2: 96, based on Lour. PageBreak(1790) 722 (non L.), blocks the transfer. The third name in line of priority is Blume (1826) Bijdr. Fl. Ned. Ind. 15: 933, and this name is available for .

Lour. (1790) Fl. Cochinch. 2: 589. – (Lour.) W.J.de Wilde & Duyfjes (2008) Reinwardtia 12: 268. – Type: Poilane 11322 (neotype P; isoneotype L, designated by de Wilde and Duyfjes (2008)), Annam. Heterotypic synonym: (‘integrifolia’) Roxb. (1832) Fl. Ind. 3: 724. – (Roxb.) Kurz (1871) J. Asiat. Soc. Bengal, Pt. 2, Nat. Hist. 40: 58. –Type: Wallich Cat. 6730 (holotype? K-W), Burma.

var. scabra

var. (W.J.de Wilde & Duyfjes) H.J.de Boer, comb. nov. – (Lour.) W.J.de Wilde & Duyfjes var. pectinatum (W.J. de Wilde & Duyfjes) W.J.de Wilde & Duyfjes (2008) Reinwardtia 12: 268 – (Roxb.) Kurz var. pectinatum W.J.de Wilde & Duyfjes (2006), Blumea 51: 287. – Type: W.J. de Wilde and Duyfjes 21692 (holotype L), Java, Indonesia.

var. (Gagnep.) H.J.de Boer, comb. nov. – Gagnep. (1918) Bull. Mus. Natl. Hist. Nat. 24: 374. – (Lour.) W.J.de Wilde & Duyfjes var. penicaudii (Gagnep.) W.J.de Wilde & Duyfjes (2008) Reinwardtia 12: 268 – Type: Pénicaud 43 (lectotype P), Hainan, China.

(W.J.de Wilde & Duyfjes) H.J.de Boer, comb. nov. – W.J.de Wilde & Duyfjes (2006) Blumea 51: 290. – Type: De Wilde and Duyfjes 21937 (holotype L), Lombok, Indonesia.

Unresolved placement within this subgenus:

C.Y.Wu ex S.K.Chen (1985) Bull. Bot. Res., Harbin 5(2): 114

C.Y.Wu ex C.H.Yueh & C.Y.Cheng (1980) Acta Phytotax. Sin. 18: 347

W.J.de Wilde & Duyfjes (2004) Sandakania 14: 6. – Type: W.J.de Wilde & Duyfjes.

Rugayah (1998) Reinwardtia 11: 216

W.J.de Wilde & Duyfjes (2004) Sandakania 14: 17

W.J.de Wilde & Duyfjes (2004) Sandakania 14: 26

Rugayah (1998) Reinwardtia 11: 223

(Gaertn.) Kitam. (1943) J. Jap. Bot. 19: 35. – Gaertn. (1791) Fruct. Sem. Pl. 2: 485, t. 180, t. 4. – Type: (Ser.) Maxim. [ = Lour.].

W.J.de Wilde & Duyfjes (2004) Sandakania 14: 11

Cogn. (1881) Monogr. Phan. [A.DC. & C.DC.] 3: 380

Rugayah (1999) Reinwardtia 11: 268

Rugayah (1998) Reinwardtia 11 (3): 219

Lour. (1790) Fl. Cochinch. 2: 588. Heterotypic synonyms according to Cooper and de Boer (2011): Gagnep. (1918) Bull. Mus. Natl. Hist. Nat. 24: 379; C.Y.Wu ex C.Y.Cheng & C.H.Yueh (1980) Acta Phytotax. Sin. 18: 340; F.Muell. (1886) Australas. Journ. Pharm. 1: 447.

Duyfjes & Pruesapan (2004) Thai Forest Bull., Bot. 32: 97

C.Y.Cheng & C.H.Yueh (1974) Acta Phytotax. Sin. 12: 425

C.Y.Cheng & C.H.Yueh (1974) Acta Phytotax. Sin. 12: 427. – Type: Maxim.

Hayata (1921) Icon. Pl. Formosan. 10: 8

Hand.-Mazz. (1936) Symb. Sin. Pt. 7: 1066

E.Walker (1971) J. Jap. Bot. 46: 71

C.H.Yueh (1980) Acta Phytotax. Sin. 18: 342

Maxim. (1859) Prim. Fl. Amur. 482

C.H.Yueh & R.G.Liao (1992) Bull. Bot. Res., Harbin 2: 115

Hayata (1921) Icon. Pl. Formosan. 10: 11

Miq. (1865) Ann. Mus. Bot. Lugd.-Bat. 2: 82

Harms (1901) Bot. Jahrb. Syst. 29: 603

(Arn.) H.J.de Boer, comb. et stat. nov. – Arn. (1840) Madras J. Lit. Sci. 12: 52. –Type: Wight & Arn. [ = (Wight & Arn.) H.J.de Boer].

(Wight & Arn.) H.J.de Boer, comb. nov. – Wight & Arn. (1834) Prodr. Fl. Ind. Orient. 1: 347. – (Wight & Arn.) Cogn. (1881) Monogr. Phan. [A.DC. & C.DC.] 3: 388 –Type: Rottler s.n. ex Herb. Klein in Herb. Wight Cat. 1118, February 1796 (holotype K; isotypes E, several duplicates), Trincomalee, Ceylon.

H.J.de Boer, sect. nov. Diagnosis: Similar to sect. , but male flowers with stamens inserted low in receptacle tube, with pseudo-ovary (a thick-walled basal part of the receptacle tube, without staminodes), and fruit with white pulp. Type: Blume.

Craib (1914) Bull. Misc. Inform. Kew: 7

Duyfjes & Pruesapan (2004) Thai Forest Bull., Bot. 32: 9

C.Y.Cheng & C.H.Yueh (1980) Acta Phytotax. Sin. 18: 346

Blume (1826) Bijdr. Fl. Ned. Ind. 15: 934

L. (1753) Sp. Pl.: 1008

N.G.Ye & S.J.Li (1989) Acta Phytotax. Sin. 27: 153

Roxb. (1832) Fl. Ind. 3: 701

Thwaites (1859) Enum. Pl. Zeyl. [Thwaites]: 127

Roxb. (1832) Fl. Ind. 3: 703. – Heterotypic synonyms: Cogn. (1881) Monogr. Phan. [A.DC. & C.DC.] 3: 362; Cogn. (1881) Monogr. Phan. [A.DC. & C.DC.] 3: 342

L. (1753) Sp. Pl.: 1008

C.Y.Cheng & C.H.Yueh (1974) Acta Phytotax. Sin. 12: 427. – Type: C.B.Clarke

C.B.Clarke (1879) Fl. Brit. India [J.D. Hooker] 2: 608. – Heterotypic synonym: Cogn. (1881) Monogr. Phan. [A.DC. & C.DC.] 3: 365

(Yueh & L.Q.Huang) H.J.de Boer, stat. nov. – subsect. Yueh & L.Q.Huang (1997) Act. Phytotax. Sinica 35: 127. – Type: F.Muell. ex Cogn.

F.Muell. ex Cogn. (1881) Monogr. Phan. [A.DC. & C.DC.] 3: 366