THAI FOR. BULL. (BOT.) 43: 46–50. 2015.

Revisiting taxonomic circumscriptions in Gaertn. and Blume for the of Thailand

BRUCE L. WEBBER1 & BOB HARWOOD2

ABSTRACT. The split of the into Achariaceae and has necessitated an updated treatment of these families for regional fl oras. In revising the Achariaceae for the Flora of Thailand, new insights on taxon circumscriptions in the family were generated based on a robust interrogation of delimiting characters and historical taxonomic decisions. Justifi cations for accepting certain taxa and synonymising others are here presented, along with recommendations for guiding future taxonomic work.

KEY WORDS: Achariaceae, delimiting characters, Flacourtiaceae, Hydnocarpus, Ryparosa, Hermann Sleumer, Thailand.

INTRODUCTION (e.g. Ryparosa fasciculata King and Ryparosa scortechinii King), and characterise important Revisions for Thailand of the genera now morphological differences between (Sleumer, included in Achariaceae have often lagged behind 1954), do not appear to hold when subjected to current circumscriptions at both the family and closer scrutiny, particularly when applying fi eld- species levels. The most recent regional revision based knowledge of the species in question. To covering the 11 genera that were once placed in complement the revision of Achariaceae for the Flacourtiaceae is now 30 years old (Sleumer, 1985). Flora of Thailand (Harwood & Webber, 2015), here Since then, Chase et al. (2002) concluded that there we revisit species from two of the four genera in was no justifi cation for maintaining Flacourtiaceae, Thailand – Hydnocarpus and Ryparosa – providing and placed the majority of genera in either Salicaceae detailed notes on the justifi cation behind our taxo- or Achariaceae. Of the 13 genera occurring in nomic treatment. Thailand, four ( R.Br., Hydnocarpus Gaertn., Ryparosa Blume and Scaphocalyx Ridl.), Hydnocarpus anthelminthicus Pierre ex Laness., were transferred to Achariaceae and the remaining H. castaneus Hook.f. & Thomson and nine were placed in Salicaceae. Chase et al. (2002) H. castaneus ssp. pseudoverrucosus Sleumer recognised four tribes in Achariaceae: Acharieae, Pangieae, Lindackerieae and Erythrospermeae. Previous authors have treated H. castaneus The four genera occurring in Thailand belong to and H. anthelminthicus as separate species, and further Pangieae and two are monotypic (Gynocardia and detailed investigation with new evidence may sup- Scaphocalyx). port this hypothesis. However, H. anthelminthicus is synonymised here because specimen and fi eld There is an emerging pattern of uncertainty studies failed to fi nd any reliable characters to around species level delimitation of certain genera separate it from H. castaneus. Kerr (1930), discussing in the Achariaceae (Webber & Woodrow, 2006). H. castaneus said: ‘This is a large tree, not unlike Some characters used by Hermann Sleumer, one of H. anthelminthicus, but with larger leaves’. In his the experts on these genera, to synonymise certain key (Kerr, 1930), he separated the two species as species (e.g. Ryparosa wrayi King with Ryparosa follows: javanica Koord. & Valeton), maintain other species

1 CSIRO Land and Water, Private Bag 5, Wembley, WA 6913, Australia. School of Biology, The University of Western Australia, 35 Stirling Highway, Crawley WA 6009, Australia. email: [email protected] 2 [email protected]

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Breadth of leaves less than 1/3 length. Ovary single sampling trips. Further investigation would be with short brown tomentum. H. anthelminthicus advisable to explore fl owering states and phenology in these species, and other Pangieae species in Breadth of leaves 1/3 the length or more. general. Ovary with rather long straw-coloured tomentum. H. castaneus There are 41 specimens that are either H. castaneus or H. anthelminthicus at BKF, and Leaf shape and size vary considerably on any considerable time was spent trying to distinguish one H. castaneus tree, and even on individual the two species. Stipule size seemed to vary too herbarium specimens. There are specimens at BKF much to be one species, from 2 mm to 7 mm, but that could be identifi ed as either H. castaneus or H. couldn’t be co-related with any other character anthelminthicus, using Kerr’s leaf characters, consistently. There is a large amount of variation in depending on which leaf of the specimen is selected. fl ower and fruit pedicel size. Gardner ST123 from Ovary tomentum also proves to be unreliable as a Trang was exceptional, having slender fl ower discriminating character. None of the specimens pedicels to 60 mm long. More common on other examined had ‘short brown tomentum’, all being specimens were slender pedicels ca. 20 mm, but straw-coloured to orange, even on the same ovary. Phengkhlai 2135 from Krabi has an ovary just The length of the tomentum is quite variable, but starting to develop into a fruit with a stout pedicel never short, even though the indumentum on mature only 9 mm long. The length of the fruiting pedicels fruits is always short. Sleumer (1985) separates the also varied considerably. two species in his key as follows: If H. castaneus and H. anthelminthicus are to Leaves ovate-lanceolate or ovate-oblong, remain synonymised as we have treated them here, base markedly inequilateral, olivaceous when dry H. castaneus is the older name and takes priority. above, nerves 8–10 pairs. Fruit globose (8–) 10–12 However, we acknowledge that there may be a case cm diam. H. anthelminthicus for conserving H. anthelminthicus because the name Leaves elliptic-oblong or oblong, base ± has been widely used medicinally, but we are not at equilateral, red-brown when dry, nerves 6–7(–8) that point yet. That is, we have only examined pairs. Fruit globose or depressedly so, (4–)5–6.5 specimens collected in Thailand and neither of the cm diam. H. castaneus types have been examined (H. anthelminthicus from Vietnam, H. castaneus from Malaysia), so the Again, leaf characters are unreliable, including treatment presented here provides a working number of veins and colour, and fruit size is also hypothesis that would benefi t from further detailed variable. In his description of H. castaneus following investigation. the key, Sleumer (1985) gives fruit size as (4–)6–8 cm diam., so species characteristics even vary between Hydnocarpus castaneus ssp. pseudoverrucosus key and description! also cannot be maintained. Sleumer described it from Myanmar, and said it differed from the type Inexplicably, Sleumer (1985) described H. by the number of lateral veins 9–11 versus 7–8(9), castaneus and H. anthelminthicus as dioecious, fruit size (7.5–8.5 mm versus 5–6.5 mm), fruit apex even though he correctly stated in his 1954 Flora of slightly conical versus not, and fruit indumentum Malesiana treatment that H. castaneus (and H. curtisii (densely brown velutinous versus fulvous tomentose). King), were monoecious (H. anthelminthicus wasn’t As shown for H. anthelminthicus, none of these in that treatment). Kerr (1930) had previously pointed characters are enough to justify a separate taxon. out that both H. castaneus and H. anthelminthicus are monoecious. This is not the fi rst time where Kerr (1930) discusses some of the medicinal there has been confusion between monoecy and uses for H. castaneus (as H. anthelminthicus) in dioecy in the Pangieae (van Slooten, 1925; Webber The Record, stating that extracts from the seeds et al., 2008). As staminate and carpellate fl owering were principally used for the treatment of leprosy periods can be temporally distinct in monoecious and other skin diseases. Between 1925 and 1930, Pangieae species (e.g. Ryparosa kurrangii; Webber an average of 225 tons of seed were exported each et al., 2008), monoecy could easily be missed in year, mainly to China. Kerr (1930) provided some

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other interesting statistics, including that the fruits thickness of the mesocarp of all Hydnocarpus species on one tree were counted, and the total was 643. He varies too much to be a useful taxonomic character, states that some trees would have more than this, the vein numbers Sleumer uses above overlap, all but also many with less, and estimated 200 fruits species have somewhat blotched fruits due to vari- per tree as an average. The seeds of 22 fruits were ation in the presence and density of indumentum counted, with the number varying from 8 to 115, (there is some indication that this is due to damage with a mean of 60. rather than natural variation), and the distinctness of the tertiary venation is somewhat subjective. Hydnocarpus ilicifolius King and Hydnocarpus Whether fruits are rugose or not may depend on serratus Warb. maturity or it may depend on the drying process, We agree with Sleumer (1938) that H. serratus but there are specimens of other Hydnocarpus is a synonym of H. ilicifolius, but provide a few species at BKF that have both rugose and non rugose details here on the variation found in H. ilicifolius. fruits on the same branch. Based on the above, H. Kerr(1930) says H. serratus was only known from kurzii ssp. australis is treated as a synonym of H. Phrae and Prachuap Khiri Khan (type location), kurzii. and separates it from H. ilicifolius by H. serratus Hydnocarpus macrocarpus (Bedd.) Warb. ssp. having free petals. Williams 1633 is from Prachuap malabaricus Sleumer and H. macrocarpus ssp. Khiri Khan, and the fi rst bud dissected had a petal burmanicus Sleumer on one side, and the rest combined into a tube with one side open, with no hint at all of where the petals In his monograph of Hydnocarpus, Sleumer making up the tube started or fi nished. The one petal (1938) described two new subspecies of H. macro- was suborbicular, with both margins overlapping carpus (ssp. malabaricus and ssp. burmanicus). He and outside the two margins of the incomplete tube. describes ssp. malabaricus in detail, but for ssp. A second bud revealed two more or less equal sized burmanicus simply states that it differs from ssp. petals, each occupying about half the circumference. malabaricus by the number of lateral veins: 8–9(–10) Each had one margin inside and one margin outside for ssp. burmanicus, (6–)7 for ssp. malabaricus. the other petal. A third bud had only one petal Sleumer (1938) appears to have regarded ssp. forming a tube, but overlapping where the two malabaricus as the type of H. macrocarpus, as it is margins of the tube joined. In all cases, the scales from the type location (Travancore, on the Malabar formed an entire tube. Geesink 6802 (Saraburi) Coast of India), and he describes it fully in his appeared to be a continuous tube in the two buds monograph, and doesn’t describe H. macrocarpus examined, but it is hard to be sure because of the at all (nor make any mention of a subspecies mac- membranous nature of the tube. Phengklai 15864 rocarpus). He describes every other Hydnocarpus (Surat Thani) had 4 petals in both buds examined, species fully in his monograph, and only uses a although there size varied considerably. In one short diagnosis for all new subspecies described bud, the petals were all approximately the same other than ssp. malabaricus. In his Thai Flacourtiaceae size, while the other had two broad and two narrow. revision, Sleumer (1985) said that ssp. burmanicus One had 24 stamens, the other 25. Many fresh male was the only subspecies occurring in Thailand, yet fl owers were examined at Soi Dao and the tube was two specimens cited by him mostly have only six always complete and seamless. Stamens were also lateral veins, one leaf only having fi ve. The subspecies counted, varying between 26 and 37. are consequently treated as synonyms. Hydnocarpus kurziii (King) Warb. and H. kurzii Ryparosa inconstans Craib, R. scortechiniii King ssp. australis Sleumer and R. fasciculata King When he described H. kurzii ssp. australis, Ryparosa inconstans and Ryparosa scortechinii Sleumer (1938) separatedd ssp. australis from H. kurzii are tentatively treated as synonyms of Ryparosa by the thicker exocarp: 3–4(–6) versus 1–2 mm, less fasciculata for the following fi ve reasons. Firstly, lateral veins: (6–)7 versus 7–8(–9), fruits rugose in his Ryparosa treatment for Flora Malesiana, and blotched, and tertiary venation more distinct. Sleumer (1954) noted how similar R. fasciculata He also noted that he had not seen any fl owers. The and R. scortechinii were, his description of R.

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fasciculata including ‘fl owers light yellowish- the three taxa may be explained by the poor condition brown, exactly as in R. scortechinii, but ovary of type material, altitudinally related morphological more attenuate at base and with 3 stigmas’. plasticity and collection bias to sample or avoid Secondly, in his notes following the description of ant-plant characters. R. fasciculata he states ‘in the sterile state to be distinguished from the very similar R. scortechinii Ryparosa wallichiii Ridl. by the numerous, elongate linear lenticels on the In this treatment, the decision was made to branchlets, which are in R. scortechinii very few in reinstate Ryparosa wallichii as a valid species. number and short orbicular-elliptic in shape’. Sleumer (1985) synonymised R. wallichii with These ‘lenticels’ are now thought to be food body Ryparosa acuminata Merr. without explanation, scars and their size and density most likely driven but citing a number of specimens now determined by ant-related harvesting (Webber et al., 2007). as Ryparosa wrayi (as part of a recent revision of R. Thirdly, the two stigmas of R. scortechinii against javanica sensu lato; Webber & Woodrow, 2006). It the three of R. fasciculata appear to be Sleumer’s best appears that Sleumer had diffi culty in recognizing way of distinguishing the two species, but stigma useful characters to assign specimens between R. numbers are not consistent within the majority of acuminata, R. wallichii, Ryparosa javanica and R. Ryparosa species (B.L. Webber unpublished data; wrayi. Furthermore, he synonymised the latter two Webber & Woodrow, 2006). Fourthly, when Craib taxa in his generic revision of the Flacourtiaceae (1926) described R. inconstans, he stated ‘stigmas (Sleumer, 1954). As such, many collections of R. 2, occasionally 3’. That species supposedly differs wallichii and R. wrayi (reinstated by Webber & from R. scortechinii and R. fasciculata by the more Woodrow, 2006) may be incorrectly determined as numerous lateral veins on the leaves, but the type either R. acuminata or R. javanica. Based on current specimen does not have the 10–12 pairs of lateral circumscriptions, it is extremely unlikely that R. veins the type description says it has! Lastly, all acuminata occurs on the Thai-Malay Peninsula three species are restricted to Peninsular Malaysia and most likely occupies a restricted range in and southern Thailand, and all have been recorded Borneo (B.L. Webber, unpublished data). Ryparosa near the border of Malaysia and Thailand. The type wallichii differs from most other Ryparosa species of R. inconstans is from Pattani, and the other Thai by the sessile fl owers, also by only having 4 anthers specimens are from Narathiwat and Yala, those two (generally Ryparosa have pedicelled fl owers and provinces bordering Malaysia to the south and mostly 5 anthers). Pattani to the north. The type specimens for both R. fasciculata and R. scortechinii were collected in CONCLUSIONS Perak, a Malaysian State on the Thai border. In revising the four genera for the Achariaceae The several immature fruits on one of the treatment in Flora of Thailand (Harwood & Webber, Thai specimens all have three stigmas, so the name 2015), both Hydnocarpus and Ryparosa presented R. fasciculata was chosen for this treatment ahead challenges for resolving clear taxonomic delimitation of R. scortechinii, which is described as having two between species. It was not possible to justify stigmas (both species were described in King, maintaining a number of species, and synonymy 1890). More work, however, needs to be done to has been proposed for these. In contrast, for other confi rm if the taxa treated here together under R. species, previous synonymy was viewed as unjustifi ed, fasciculata represent a single species. In particular, and we have reinstated these species. At the heart the possible differences in reproductive material, of these decisions lies a general trend towards a including infl exed petals and more numerous seeds choice of defi ning character states for species that in R. fasciculata (King, 1890), warrant further at- are either considerably variable within and between tention. Unfortunately, the availability of specimens specimens and taxa, or not representative of the with these features to make observations on is limited, taxa concerned, particularly when fi eld observations and this applies to the full range of material that we are taken into account. Both genera have been most have examinedd across more than 10 herbaria globally. recently revised by Sleumer (1938, 1954, 1985), It is suspected that apparent differences between whose work was largely conducted in Europe on

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dried herbarium material, with little opportunity to King, G. (1890) Materials for a fl ora of the Malayan examine fresh material or for observations of species Peninsula. Journal of the Asiatic Society of in the fi eld. With a better knowledge of the fi eld Bengal, Calcutta 59: 113–206. ecology of these species and better collections of Sahoo, M.R., Dhanabal, S.P., Jadhav, A.N., Reddy, V., more representative material, we envisage taxonomic Muguli, G., Babu, U.V. & Rangesh, P. (2014) revisions of the future making better use of more Hydnocarpus: an ethnopharmacological, phyto- informative and appropriate characters. Moreover, chemical and pharmacological review. Journal given the historical interest in both Hydnocarpus of Ethnopharmacology 154: 17–25. and Ryparosa for pharmacological purposes Sleumer, H.O. (1938) Monographie der Gattung (Sahoo et al., 2014) and plant-animal mutualisms Hydnocarpus Gaertner. Botanische Jahrbücher (Webber et al., 2007), respectively, there is also a für Systematik, Pfl anzengeschichte und clear need for molecular studies on these two genera Pfl anzengeographie 69: 1–94. to support these morphometric insights and resolve further taxonomic uncertainties. Sleumer, H.O. (1954) Flacourtiaceae. In: C.G.G.J. Van Steenis (ed.) Flora Malesiana, Series 1 (Spermatophyta), Volume 5. pp. 1–106. Noordhoff- ACKNOWLEDGEMENTS Kolff N V, Djakarta, Indonesia. We thank Sue Zmarzty at K, who was a Sleumer, H.O. (1985) The Flacourtiaceae of Thailand. tremendous help to us in many ways and Edward Blumea 30: 217–250. Tsen for feedbackk on earlier drafts of this manuscript. van Slooten, D.F. (1925) Contributions à l’étude de la BLW was supported by the Building Resilient Flore des Indes Néerlandaises - The Flacourtiaceae Australian Biodiversity Assets theme in CSIRO of the Dutch East Indies. Bulletin Du Jardin Ecosystem Sciences and a CSIRO Julius Award. Botanique Buitenzorg, Series III 7: 291–421. Webber, B.L. & Woodrow, I.E. (2006) Morphological REFERENCES analysis and a resolution of the Ryparosa javanica Chase, M.W., Zmarzty, S., Lledo, M.D., Wurdack, species complex (Achariaceae) from Malesian K.J., Swensen, S.M. & Fay, M.F. (2002) When and Australian tropical rainforests. Australian in doubt, put it in Flacourtiaceae: a molecular Systematic Botany 19: 541–569. phylogenetic analysis based on plastid rbcL Webber, B.L., Moog, J., Curtis, A.S.O. & Woodrow, DNA sequences. Kew Bulletin 57: 141–181. I.E. (2007) The diversity of ant–plant interactions Craib, W.G. (1926) Contributions to the Flora of in the rainforest understorey tree, Ryparosa Siam. Additamentum XVIII. Bulletin of (Achariaceae): food bodies, domatia, prostomata, Miscellaneous Information (Royal Gardens, and hemipteran trophobionts. Botanical Journal Kew) 1926: 154–174. of the Linnean Society 154: 353–371. Harwood, B. & Webber, B.L. (2015) Achariaceae. Webber, B.L., Curtis, A.S.O., Cassis, G. & Woodrow, In: T. Santisuk & H. Balslev (eds), Flora of I.E. (2008) Flowering morphology, phenology Thailandd 13(1): 1–17. Forest Herbarium, Bangkok. and fl ower visitors of the Australian rainforest Kerr, A.F.G. (1930) The genera Hydnocarpus and tree, Ryparosa kurrangii (Achariaceae). The Taraktogenos in Siam. The Record, Technical Australian Entomologist 35: 7–17. & Science Supplement 7: 1–16.

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