A revision of the Adenophorus Group and other glandular-leaved species of Croton (Euphorbiaceae) from northern Madagascar and Mayotte, including three new species Author Kainulainen, Kent Author Ee, Benjamin van Author Razafindraibe, Hanta Author Berry, Paul E. text Candollea 2017 2017-09-27 72 2 371 402 journal article 20729 10.15553/c2017v722a15 3daa21e6-497a-466b-b4f6-ef0ae1dd0ba4 2235-3658 5722061 Croton nudatus Baill. in Adansonia 1: 168. 1861 [as nudatum ] ( Fig. 1A , 2A , 3 , 4 A-B). Ξ Oxydectes nudata (Baill.) Kuntze, Revis. Gen. Pl. 2: 612. 1891 . Typus : MADAGASCAR . Prov. Antsiranana : « Baie de Diego-Suarès », XII.1848 , Boivin 2659 (holo-: P [ P00389498 ]!). Epitypus (designated here): MADAGASCAR . Prov. Antsiranana : Diana Reg. , Antsiranana II, Orangea , road going uphill from military checkpoint at entrance to Orangea , 12°14’08”S 49°21’40”E , 50 m , 25.X.2009 , van Ee et al . 1081 (epi-: MICH [ MICH1517189 ]!; isoepi-: P, TAN) . = Croton boivinianus var. brevifolius Radcl.-Sm. , Gen. Croton Madag. Comoro 12. 2016 . Typus: MADAGASCAR . Prov. Antsiranana : à 79 km au S d’Antsiranana par route RN6, et 15 km à l’E de l’ancien chantier du Colas à Marotaolana, Campement à l’E du village d’Ampantsona , 12°51’20’’S 49°18’10’’E , 394-551 m , 3-6.VI.1997 , Andrianantoanina & Bezara 1068 (holo-: K ; iso-: MO , P [ P00433267 ]!), syn. nov. = Croton hirsutissimus Radcl.-Sm. , Gen. Croton Madag. Comoro 99. 2016 . Typus: MADAGASCAR . Prov. Antsiranana : versant E du massif de l’Ankarana (partie S du massif de Mafokovo) , au N de Vohémar , 50-450 m , 17.XII.1966 , Service Forestier 27363 (holo-: P [ P00154439 ]!), syn. nov. Fig. 2. Distribution maps. A. Croton nudatus Baill. (white), C. stanneus Baill. (yellow); B. Croton adenophorus Baill. (green) and C. tsiampiensis Leandri (white); C. Croton bathianus Leandri (light blue), C. loucoubensis Baill. (yellow), and Croton scoriarum Leandri (red); D. Croton orangeae Kainul. & Berry (red) and C. sahafariensis Kainul. & Berry (yellow); E. Croton mayottae P.E. Berry & Kainul. [Google Earth Image © 2017 DigitalGlobe. Reproduced per attribution guidelines] = Croton menabeensis var. furfuraceus Radcl.-Sm. , Gen. Croton Madag. Comoro 101. 2016 . Typus MADAGASCAR . Prov. Mahajanga : Sofia Reg. , Antsohihy Distr ., Antsatrana , Bora , 17.VII.1970 , Service Forestier 30011 (holo-: P [ P00154438 ]!), syn. nov . Shrubs 0.5-4(5) m tall, dichotomously branched, internodes sometimes so short as to appear whorled, twigs terete, from green when newly emergent to dark gray or almost black, becoming noticeably lenticellate. Young shoots and inflorescence axes with a whitish to ferrugineous indument of stellate trichomes (rarely nearly glabrous). Stipules minute, inconspicuous. Leaves opposite, deciduous. Petioles 0.5-10 (-30) mm long, adaxially canaliculate, stellate, with 2 minute, shortly stipitate, discoid acropetiolar glands c. 0.1-0.3 mm diam., usually obscured by the surrounding trichomes. Leaf blades softly membranaceous, entire, narrowly to broadly ovate, 1.5-4(-7.7) × 0.5-2(-4) cm, apex shortly acuminate, base rounded to shallowly cordate, young leaves usually densely white-woolly, becoming more discolorous as they expand, the adaxial surface with stellate trichomes with a long porrect central ray, abaxial surface with a denser stellate indument; venation 3-palminerved at the base, remaining secondaries in 3-4 pairs and widely spaced, veins somewhat prominent below and sometimes with scurfy ferrugineous-stellate indument along the midrib and secondaries, sometimes with a few sparse, yellowish globular glands between the midvein and the margin, these sometimes associated with the vein junctions ( Fig. 1A ). Inflorescences terminal, racemose, 2-10(-20) mm long, few-flowered (2-10 buds), bracts inconspicuous, c. 1 mm long, buds globose, 1.5-2.5 mm diam., densely yellowish-stellate, the trichomes with an elongate porrect central ray ( Fig. 3D, F, H ), pedicels 2-5 mm long and divergent from the axis. Staminate flowers with 5 broadly triangular sepals, 5 oblong-spathulate petals, and 8-10 stamens, anthers oblong, c. 0.6 mm long, basifixed, filaments 1.5-2.5 mm long, curving inwards; receptacle villous. Pistillate flowers with 5 bluntly triangular sepals 1.5-2.5 mm long, basally connate, densely stellate-rosulate; petals 5, oblong-subspatulate, ciliate, 2-2.5 × 0.6-1.4 mm , ovary trilobate-subglobose, c. 2 mm diam., fulvous-hirsute, the trichomes with elongate porrect central rays; styles 3, 1- 1.5 mm long, 4-fid (with 12 terminal tips), reddish-brown, basally stellate. Bisexual flowers occasionally present, with 5 stamens opposing the petals, filaments 1.5-2 mm long, anthers broadly elliptic-ovate, c. 0.5 × 0.5 mm . Capsules globose, c. 5 × 5 mm , lightly to densely hirsute, the exocarp separating, endocarp thinly woody, c. 0.3 mm thick; columella 3.5-5 mm long, triquetrous, tricornute, erect and persistent ( Fig. 4A ). Seeds ovoid, 3.5-4 × 2.5-3 × 1.5-2 mm , rounded-apiculate, biconvex in cross-section, smooth, shiny, yellowish-brown to brown ( Fig. 4B ); caruncle transversely oblong, slightly curved, 0.7-0.9 × 0.5 mm , whitish to golden. Fig. 3. Croton nudatus Baill. A. Leafless branch with young inflorescences.; B. Understory dwarf shrub; C. Leaves; D. Young inflorescence. Note the white woolly pubescence on the young leaves and shoots of this specimen; E. Leaves of a more hirsute specimen; F. Pistillate flower; G. Inflorescences with predominantly staminate flower; H. Close up of staminate and pistillate flowers; I. Immature capsules on a specimen with subglabrous leaves. [ A : van Ee et al. 1064 ; B : van Ee et al. 2302 ; C : van Ee et al. 2321 ; D: van Ee et al. 2341 ; E-F: Callmander et al. 253 ; G-H: Burivalova 34 ; I : Randrianaivo et al. 1424 ] [Photos: A : B . van Ee; B : K. Kainulainen; C-D: P. Berry; E-F: M. Callmander; G-H: Z. Burivalova; I : R. Randrianaivo] Phenology. – Croton nudatus drops its leaves towards the end of the dry season, which typically runs from April to November in northern Madagascar . It can retain floral buds for much of the year and presumably flowers with the first heavy rains, usually in November-December, followed by leaf flush and fruiting, but there appears to be much variability in rainfall regimes across its distribution and from year to year. Distribution, habitat and ecology. – Croton nudatus occurs in deciduous forests and secondary scrub vegetation in northern Antsiranana and in Mahajanga Province , from sea level to about 500 m elevation, growing mainly on sandy or rocky soils ( Fig. 2A ). Conservation assessment. – Croton nudatus occurs in Antsiranana Prov. , in northern Madagascar , where it is known from 17 locations, including the protected areas of Andrafiamena, Ankarana, and Orangea (Oronjia). Three localities are also known from Mahajanga (Bora, Maintirano, Soalala), although these collections are more than 40 years old. We recommend that C. nudatus should be assigned as “Least Concern” [LC] according the IUCN Red List Categories and Criteria ( IUCN, 2012 ). Vernacular names. – “Lazalaza” (Be et al. 11), “Mamalifolay” (Service Forestier 16390). Notes. –The species epithet nudatus refers to the “naked” (leafless) branches of the type . The holotype of C. nudatus is leafless, and no botanist since BAILLON (1861) had successfully matched it to any other collection. However, the stems have opposite leaf scars, and the locality is clearly given as coming from the area of the bay of Diego Suarez in Antsiranana Province . The protologue also mentions the presence of petals in the pistillate flowers as well as some hermaphroditic flowers, which is very rare in Malagasy Croton . We have observed that several recent collections from northern Antsiranana Province , namely Be et al. 11 , van Ee et al. 1079 , and van Ee et al. 1081 , all have some hermaphroditic flowers as well as opposite leaves and petals in the pistillate flowers, and consequently we are quite confident that these specimens represent the same species as the type. To better document the leaves and fruits of the species, we designate an epitype (van Ee 1081) that comes from the type locality area and has leaves and fruits, with photographs available in TROPICOS (2017) . Croton nudatus is usually a spindly understory shrub, with thin dark gray to blackish branches. It may also form a compact dwarf shrub that is no more than 0.5 m tall, with all leaves level in a single plane ( Fig 3B ). The leaves are opposite and entire, but quite variable in shape and degree of pubescence. The short, raceme-like inflorescences with pedicellate, buff-colored buds are characteristic, as are the well-developed petals of the pistillate flowers ( Fig 3 C-E), and the smooth glossy seeds ( Fig 4B ). Despite having opposite leaves and sometimes a few laminar glands, it does not belong to the Adenophorus Group. In the molecular phylogenetic study by HABER et al. (2017) , C. nudatus did not form part of the highly supported Adenophorus-Mongue clade. Two of RADCLIFFE-SMITH (2016) ’s names, Croton hirsutissimus and C. boivinianus var. brevifolius , are synonymized here. They were both described from single specimens, one from Ankarana the other from nearby Ampantsona. They differ markedly in the degree of pubescence, and they could be considered as representing the extremes in a gradient within C. nudatus . Service Forestier 27363 , for instance, is hirsute, whereas Andrianantoanina & Bezara 1068 is nearly glabrous. Both have laminar glands, although there are very few in the latter specimen. Preliminary phylogenetic analyses of nrDNA strongly support the inclusion of Andrianantoanina & Bezara 1068 in C. nudatus . The type of C. menabeensis var. furfuraceus Radcl. -Sm., from northern Mahajanga (see Fig. 2A ), also shows the characteristic raceme-like inflorescences with buff-colored buds, and we therefore consider it to be another synonym of C. nudatus . The young leaves of this specimen are stellate on both sides, whereas the older leaves are nearly glabrous. Two specimens from western Mahajanga are included here, namely Morat 997 (Soalala) and Service Forestier 16390 (Beleza). The former is nearly leafless, but both specimens conform to C. nudatus in their opposite leaves and the buff-colored buds. Additional specimens examined. – MADAGASCAR . Prov. Antsiranana : Diana Reg. , Mahamasina Massif de l’Ankarana , Betsimipohaka , 12°57’23”S 49°08’52”E , 13.V.2007 , Bardot-Vaucoulon 1788 ( MO , P); Analabolona , 3 km à l’W d’Irodo , 12°37’21”S 49°30’01”E , 102 m , 20.VII.2004 , Be et al. 11 ( CNARP , MO , P , TAN ); Andrafiamena , forêts aux alentours d’Anjahankely , 12°54’50”S 49°19’13”E , 361 m , 23.XI.2010 , Burivalova et al . 34 ( G , MICH ); ibid loc. , 12°54’58”S 49°20’01”E , 512 m , 27.XII.2010 , Burivalova et al . 137 ( G , MICH ); massif de l’Ankerana , S du massif de Mafokovo , 13°18’S 49°52’E , 206 m , 22.X.2004 , Callmander et al . 253 ( G , MO , P ); Daraina , forêt de Bekaraoka , partie N , 13°04’58”S 49°42’04”E , 140 m , 22.XI.2006 , Gautier & Chatelain 4898 ( G , MICH ); Forêt d’Analamaitso entre Anivorano Nord et les falaises de l’Ankarana , III.1962 , Keraudren 1708 ( K , P ); SE of Ambilobe , near Daraina on road to Vohemar ( Iharana ), 13°12’S 49°46’E , 200 m , 20.XII.1989 , McPherson 14737 ( MO , P ); Daraina , Ambohitsitondroina forest , 13°07’48”S 49°27’55”E , 248 m , 5.I.2006 , Nusbaumer & Ranirison 1842 ( G , MICH , MO ); Daraina , Antsahraingy forest , 12°55’08’’S 49°40’31’’E , 95 m , 28.II.2005 , Nusbaumer & Ranirison 2301 ( G ); Ampisikina , Tsaratanana , Antsiraka forest , 12°57’50”S 49°41’38”E , 500 m , 8.XI.2005 , Rakotonandrasana et al. 977 ( CNARP , G , MO , P , TAN ); Daraina , Befarafara , 13°04’33”S 49°34’45”E , 260 m , 7.XII.2006 , Randrianaivo et al. 1424 ( CNARP , MICH , MO , P , TAN ); Daraina , Ambohitsitondroina forest , 13°08’55’’S 49°27’36’’ E , 200 m , 9.I.2006 , Ranirison & Nusbaumer 1068 ( G , MICH , MO ); Vohimarina , Fanambana , Antsatoby , 13°35’52”S 49°59’33”E , 171 m , 3.VII.2007 , Rasoafaranaivo 204 ( MO , P ); W slope of Montagne des Français , 12°22’02”S 49°19’10”E , 300 m , 23.X.2009 , van Ee et al. 1064 ( MICH , P ); Orangea , 12°14’08”S 49°21’40”E , 50 m , 25.X.2009 , van Ee et al. 1079 ( MICH , MO , P ); Sahafary forest in the Saharaina River basin , 12°34’51”S 49°27’02”E , 270 m , 26.X.2009 , van Ee et al. 1104 ( MICH , MO , P ); ibid loc. , 12°35’38”S 49°26’04”E , 280 m , 26.X.2009 , van Ee et al. 1107 ( MICH ); Betsiaka , Andavakoera forest , 13°07’26”S 49°13’52”E , 500 m , 27.X.2009 , van Ee et al. 1127 ( MICH , P ); Ambatomikiny forest , 12°49’53”S 49°16’15”E , 311 m , 28.II.2016 , van Ee et al. 2302 ( MICH , TAN ); Sahafary forest , 12°35’03”S 49°26’59”E , 231 m , 2.III.2016 , van Ee et al. 2321 ( MICH , TAN ); ibid loc. , 12°34’54”S 49°26’25”E , 191 m , 4.III.2016 , van Ee et al. 2333 ( MICH , TAN ); ibid loc. , 12°34’53”S 49°26’24”E , 192 m , 4.III.2016 , van Ee et al. 2336 ( MICH , TAN ); ibid loc. , 12°34’57”S 49°26’07”E , 182 m , 4.III.2016 , van Ee et al. 2339 ( MICH , TAN ); ibid loc. , 12°34’56”S 49°26’06”E , 180 m , 4.III.2016 , van Ee et al. 2340 ( MICH , TAN ); ibid loc. , van Ee et al. 2341 ( MICH , TAN ); Orangéa peninsula , 12°13’59”S 49°21’33”E , 24 m , 5.III.2016 , van Ee et al. 2344 ( MICH , TAN ); ibid loc. , 12°14’47”S 49°22’46”E , 30 m , 5.III.2016 , van Ee et al. 2360 ( MICH , TAN ); Ankarana National Park , 12°57’11”S 49°07’45”E , 101 m , 7.III.2016 , van Ee et al. 2374 ( MICH , TAN ). Prov. Mahajanga : Boeny Reg. , X.1964 , route de Soalala , Morat 997 ( P ); Melaky Reg. , Forêt de Beleza , Campement de Beleza , Maintirano , 30.V.1956 , Service Forestier 16390 ( P ).