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 adenophorus Baill. in Adansonia 1: 153. 1861 [as adenophorum ] ( Fig. 1C , 2B , 4 E-F, 6). – Croton adenophorus var. genuinus Müll. Arg. in A. DC., Prodr. 15(2): 589. 1866 [nom. inval.]. Ξ Oxydectes adenophora (Baill.) Kuntze, Revis. Gen. Pl. 2: 610. 1891 . Lectotypus (designated here): MADAGASCAR . Prov. Antsiranana : Diana Reg. : Nossi-bé , 1837, Richard 214 ( P [ P00123689 ]!; isolecto-: P [ P00123690 ]!). Syntypi : MADAGASCAR . Prov. Antsiranana : Nossi-bé , s.d., Richard 574 ( P [ P00123691 ]!); ibid. loc. , 1849, Boivin 2187 ( G [ G00446358 , G00446359 ]!, P [ P00301515 ]!). = Croton payerianus Baill. in Adansonia 1: 154. 1861 [as payerianum ]. Ξ Oxydectes payeriana (Baill.) Kuntze, Revis. Gen. Pl. 2: 612. 1891 . Lectotypus (designated here): MADAGASCAR . Prov. Antsiranana : “ Nossibé ”, 1849, Boivin 2187 ( P [ P00389508 ]!; isolecto-: G-DC [ G00311984 ]!, G [ G00446358 , G00446359 ]!, P [ P00389509 , P00404480 , P00404481 , P00123684 ]!). = Croton subaemulans Baill . in Bull. Mens. Soc. Linn. Paris 2: 850. 1890 . Typus: M ADAGASCAR : “Central Madagascar”, Baron 5795 (holo-: K [ K000422590 ]!; iso-: P [ P00133593 ]!), syn. nov. = Croton tenuicuspis Baill . in Bull. Mens. Soc. Linn. Paris 2: 927. 1891 . Typus: M ADAGASCAR : “Madag. centr.”, Baron 5846 (holo-: P [ P00133364 ]!, iso-: K [ K000422590 ]!), syn. nov. = Croton tulasnei Baill. in Adansonia 1: 156. 1861 . Ξ Oxydectes tulasnei (Baill.) Kuntze, Revis. Gen. Pl. 2: 613. 1891 . Lectotypus (designated here): FRANCE . Dept. Mayotte : Bouzi , 1850, Boivin s.n. ( P [ P00133305 ]!; isolecto-: P [ P00133306 , P00466148 ]), syn. nov. Shrubs or trees , 1-9 m tall, dichotomously branching, internodes sometimes so short as to give the appearance of whorled branches. Branches flattened on new growth but becoming terete with age, bright green and sparsely covered with whitish stellate indument, soon turning reddish brown, glabrous, ± glossy. Bark smooth and conspicuously lenticellate. Stipules 6-17 × 2-4 mm , lanceolate or auriculate, tapering to a thin apex, sometimes with marginal glands (and glandular filaments), caducous. Leaves opposite. Petioles 0.6-8.5 cm , adaxially canaliculate, stellate-pubescent, usually with a pair of subsessile, concave, discoid, yellow, glabrous glands ( 0.3-0.8 mm in diam.) by the base of the lamina. Leaf blades membranaceaous to chartaceous, glandular crenulate, denticulate, or serrate, ovate, 4.2-17.0 × 2.3-11.5 cm , apex acute to acuminate, base rounded to cordate; abaxial and adaxial surfaces sparsely stellate-pubescent on young leaves, ± glabrous on older leaves, pale green when fresh (turning orange in old leaves) and drying matte pale green to brown; venation evident on the adaxial side, prominent below, with 5-10 pairs of brochidodromus, ± penninerved secondary veins (the lowermost pairs congested and appearing palmate), and crossvenulate tertiary venation; glands are usually present in some of the axils of the secondary veins on the abaxial side ( Fig 1C ). Inflorescences terminal, raceme-like thyrses, 1.5-22 cm long, terminal, often appearing unisexual, or bisexual with pistillate flowers at the base and staminate flowers at the distal end, axes stellate-pubescent, flattened; bracts narrowly triangular, 1.0- 3.5 mm long. Staminate flowers with stellate-pubescent, subglobose buds 1.8-2.3 mm diam., pedicels elongating from bud to anthesis, 1.0- 3.5 mm long; sepals 5, pale green, shortly connate at base, lobes broadly triangular to ovate, often unequal in size, 1.5-3.5 × 1.3-2.0 mm, apex acute, inflexed at anthesis, abaxially stellate-pubescent, adaxially sparsely ciliate, margins densely ciliate; petals 5, yellowish, ellipticspatulate, 1.9-2.4 × 0.7-1.0 mm, recurved at anthesis, abaxially stellate-pubescent and papillose, adaxially ciliate towards apex, margins densely ciliate; disc glands 5, opposite the sepals, sessile, deltoid, truncate or with an apical depression, c. 0.3 × 0.5 mm , yellow; stamens 10-16, white, filaments 1.6- 3.1 mm long, ciliate, anthers broadly elliptic, c. 0.7 × 0.6 mm ; receptacle pilose. Pistillate flowers with stellate-pubescent buds, 2-3 mm diam., pedicels 2-4(-9) mm long; sepals 5, elliptic, spreading at anthesis, often unequal in size, 2.5-11.5 × 1.1-2.5 mm , apex acute, shortly connate at base, glandular margin, abaxially and adaxially subglabrous, sometimes bearing glands similar to those on the leaves, bright green, persistent in fruit; petals usually absent/reduced, but when present, c. 1.5 × 0.3 mm , abaxially stellate-pubescent, adaxially glabrous, margin ciliate; disc glands 5, opposite the sepals, sessile, ellipsoidal, c. 0.3 × 0.6 mm , pale yellow; ovary densely covered by ferruginous to dark brown, stellate trichomes, pale green, globoid-ellipsoid, 2-3 mm in diameter, styles 3, 2- 3 mm long, each branch flattened and 1-3 times bifurcate, the first bifurcation often congested and fused, spreading, recurved at the apices, abaxially stellate-pubescent, adaxially glabrous, (pale) yellow, turning brown, persistent. Capsules , 5.0-6.0 × 5.5-8.0 mm, smooth, pale brown, covered with contrasting dark brown stellate trichomes, exocarp not separating, endocarp woody, 0.3-0.4 mm thick ( Fig. 4E ); columella 3-4 mm long, cornute, capitate. Seeds ± compressed-ellipsoid, 3.1-4.1 × 2.3-3.1 × 1.8-2.5 mm ( Fig. 4F ); testa glossy, verrucose, brown; caruncle reniform, c. 0.5 × 1 mm . Fig. 6. Croton adenophorus Baill. A. Habit , in a heavily disturbed and cultivated area along RN 6, near turnoff for Ampampamena airstrip; B. Leaves; C. Smooth bark on young twigs; D-E. Close-ups of stipules and leaf bases; note the auriculate, elongate stipules, the acropetiolar glands, and the laminar glands on the adaxial side of the lamina (arrows); F. Inflorescence with staminate flowers and buds; G-H. Inflorescences with pistillate flowers; note the green, unequal sepals, the patent stigmas, and the variable occurrence of petals; I . Capsule. [ A , F: van Ee et al. 2288 ; B , G : van Ee et al. 2382 ; C : van Ee et al. 2287 ; D, H: van Ee et al. 2384 ; E : van Ee et al. 2295 ; I : van Ee et al. 1165 ] [Photos: A , F: K. Kainulainen; B-E, G-I: P. Berry] Fig. 7. Croton bathianus Leandri A. Coppiced individuals; B. BVE with a sucker shoot; C. Leaves; D. Stipules; E. Young leaves and inflorescence; note the dense covering of ferrugineous, granulate trichomes; F. Staminate flowers; G-H. Inflorescence with staminate and pistillate flowers; note the presence of petals in the pistillate flowers; I . Young fruits. [ A : van Ee et al. 1139 ; B : van Ee et al. 2290 ; C , I : van Ee et al. 1140 ; E : van Ee et al. 2296 ; D, F: van Ee et al. 2383 ; G-H: van Ee et al. 2289 ] [Photos: A : B . van Ee; B-I: P. Berry] Phenology. – We have seen flowering specimens from August to April, and in bud in May (we have not seen any specimens from June or July), so it is likely that this species flowers more or less continuously throughout the year. Distribution, habitat and ecology. – Croton adenophorus occurs both in evergreen forest and in secondary or degraded vegetation, and it is often collected in riparian or moist habitats. It occurs from sea level to c. 450 m elevation. It is locally frequent in the Sambirano Domain ( HUMBERT, 1955 ), and there is also a population from the littoral forest of Analabe in northernmost Vohémar, Antsiranana Province on the northeast coast ( Fig. 2B ). Cours 3207 , collected in the Mainampango forest (Andapa, SAVA Reg.), was indicated as a shade plant in a vanilla plantation. It is possible that the disjunct outliers from southern Mahajanga, i.e., Decary 2359 from Morafenobe, Service Forestier 16 from Tsingy de Namoroka, and van Ee et al. 1165 from Ambodiriana, were also escaped from cultivation, since this species is not only used as a shade plant but also in hedgerows (see Randrianarivelo et al. 145 ). The only known specimen from Mayotte is Boivin s.n. (the type of C. tulasnei ), collected in 1850, and it is therefore uncertain whether C. adenophorus still occurs there, and if the gathering was made from a native or introduced plant. Conservation assessment. – Since C. adenophorus is widespread and known from numerous localities, including the protected areas of Ampasindava, Galoko, and Manongarivo, we assign the species as “Least Concern” [LC] according the IUCN Red List Categories and Criteria ( IUCN, 2012 ). Vernacular names. – “Bemasaho” (Rabenantoandro et al. 1070), “Hazomafaiky” (Madiomanana & Ammann 181), “Hazomafaitra” (Nusbaumer & Tahinarivony 2977), “Matifioditra” (Cours 3207), “Mavokely” (Decary 999), “Sakaiala” (Randrianarivelo 145), “Sakaitomendry” (Randrianarivelo 145). Notes. – The species epithet adenophorus means “bearer of glands.” This species is distinct in the glabrous and glossy reddishbrown bark; acuminate leaves that usually dry matte green; contrasting white stellate hairs on the young leaves (and shoots), whereas the mature leaves are ± glabrous ( Fig. 1C ); the usually large, foliaceous stipules that may be auriculate at the base and then taper to a fine point ( Fig. 6 D-E); the flattened, patent stigmas; and the often unequal and foliaceous, bright green sepals that sometimes have glands similar to those on the leaves. The lectotype of C. adenophorus (P [P00123689]), which was collected by Achille Richard, bears a label with the name “ Croton acuminatum” in Richard’s hand, which BAILLON (1861) cited in his protologue. BAILLON (1861) also cited Boivin 2187 at P [P00301515] as a syntype of C. adenophorus , which he annotated as such, despite citing and annotating other sheets of the same collection number as syntypes of C. payerianus on the next page. Since C. adenophorus and C. payerianus were published in the same article, either one could be the accepted name, but we follow the precedent of LEANDRI (1939) , who synonymized C. payerianus . It is important to note that our concept of C. adenophorus differs from that of LEANDRI (1939) . By including C. loucoubensis as a synonym of C. adenophorus , LEANDRI confounded this group, and his description of C. adenophorus corresponds to what we recognize here as C. loucoubensis . He then went on to recognize C. subaemulans , which is really the same as the true C. adenophorus . BAILLON (1861) separated C. tulasnei from his C. payerianus (to us, a synonym of C. adenophorus ) by its poorly developed or absent laminar glands, somewhat different leaf shape (oval-ovate and acute vs cordate and acuminate), linear stipules, and different branching pattern of the stigma. However, similar variation in the shape of the leaves and stipules, and in the number of laminar glands, is also seen within populations of C. adenophorus in Madagascar , and the stigma branches may vary from 1-3 times bifurcate ( Fig. 6 G-H). We therefore do not consider C. tulasnei as a distinct species from C. adenophorus . Additional specimens examined. – MADAGASCAR . Prov. Antsiranana : Diana Reg. , Nosy Be , env. d’Ambatozavany , 50-250 m , 14.XII.1967 , Bernardi 11863 ( G , K , P ); Nosy Be , 1847-1852, Boivin s.n. ( G , P ); SAVA Reg. , forêt de la montagne de Mainampango Est , village Ambalavoanio , c. 450 m , 1.III.1949 , Cours 3207 ( P ); Ampasindava , 10 m , 14.VIII.1957 , Cours 5232 ( P ); Analanantsoa , Ambodisakoana , 14°04’S 48°15’E , 40 m , 1.XI.1994 , Derleth 145 ( G , K , MO , P , TAN ); ibid. loc. , 14°04’S 48°15’E , 50 m , 3.IV.1996 , Gautier 2966 ( G , K , MO , P ); Manongarivo RS , Beraty , 14°01’51”S 48°14’53”E , 65 m , 22.X.2012 , Gillespie et al . 10651 ( CAN , MICH , MO , TAN ); Ambanja , Antsatsaka-Ambato , 13°27’23”S 48°32’39”E , 26 m , 30.VIII.2002 , Hong-Wa 71 ( MO , P , TAN , TEF ); Vallée de la Lokoho (NE), près d’Ambalavohino , 75-300 m , 9-10.I.1949 , Humbert & Cours 22834 ( K , P ); Ampasindava , 7.IX.1967 , Jacquemin H501J ( P ); Ampasindava , 13°45’39”S 48°06’38”E , 370 m , 29.XI.2008 , Madiomanana & Ammann 181 ( G , K , MO , P , TEF , WAG ); Vohemar Distr ., Nosibe , Anjiabe , Anaborano , Analabe forest , 13°04’08”S 49°54’20”E , 5 m , 9.XII.2004 , Manjakahery & Sola 80 ( MO ); Ampasindava , 13°48’17”S 48°10’48”E , 218 m , 29.XI.2007 , Nusbaumer 2615 ( G , K , MO , P , TEF ); ibid. loc. , 13°43’59”S 48°04’15”E , 141 m , 23.XI. 2008 , Nusbaumer & Tahinarivony LN 2966 ( G , MO , P , TEF ); ibid. loc. , 13°46’09”S 48°06’12”E , 312 m , 24.XI.2008 , Nusbaumer & Tahinarivony LN 2977 ( G , K , MO , P , TEF ); Anaborano , 13°04’42”S 49°54’13”E , 25 m , 2.XI.2002 , Rabenantoandro et al. 1070 ( MICH , MO , P ); Analabe forest , 13°04’14”S 49°53’40”E , 22.II.2003 , Rabevohitra et al. 4481 ( MO , P , TEF ); ibid loc. , 13°04’09”S 49°54’08”E , 18 m , 11.X.2004 , Randrianarivelo et al. 145 ( MICH , MO ); Ambilobe Distr ., Beramanja , Anketrabe Bilinta , Ambahatra , Galoko forest , 13°36’11”S 48°42’37”E , 430 m , 7.X.2013 , Randriatsivery et al . 479 ( G , MO , P , TAN ); Analabe forest , 13°04’43”S 49°54’04”E , 13.V.2004 , Razakamalala et al . 1270 ( MO , P , TEF ); Nosy Be , 25.IX.1951 . Reserves Naturelles 2992 ( P ); ibid loc ., s.d., Richard 180 ( P ); ibid loc. , 12.III.1971 , Schmitt 252 ( P ); RN [Route Nationale] 6, 41 km N of Ambanja , 13°28’41”S 48°44’03”E , 25 m , 2.XI.2009 , van Ee et al. 1133 ( MICH ); ibid loc. , van Ee et al. 1134 ( MICH ); ibid loc. , van Ee et al. 1135 ( MICH ); RN 6 , 41 km N of Ambanja , 13°31’23”S 48°41’28”E , 20 m , 2.XI.2009 , van Ee et al. 1141 ( MICH ); RN 6 , close to turn off for Ampampamena airstrip , 13°29’33”S 48°38’12”E , 8 m , 27.II.2016 , Van Ee et al . 2287 ( MICH , TAN ); ibid loc. , van Ee et al. 2288 ( MICH , TAN ); RN 6 , N of the turnoff to Belinta , 13°30’22”S 48°42’05”E , 17 m , 27.II.2016 , van Ee et al. 2291 ( MICH , TAN ); ibid loc. , 13°30’09”S 48°42’20”E , 22 m , 27.II.2016 , van Ee et al. 2292 ( MICH , TAN ); ibid loc. , van Ee et al. 2293 ( MICH , TAN ); ibid loc. , 13°28’56”S 48°43’36”E , 17 m , 27.II.2016 , van Ee et al. 2294 ( MICH , TAN ); RN 6 E of Ampampamena , 13°30’46”S 48°40’30”E , 34 m , 27.II.2016 , Van Ee et al . 2295 ( MICH , TAN ); RN 6 E of Ampampamena and south of Ambatomainty , 13°28’26”S 48°44’20”E , 21 m , 27.II.2016 , van Ee et al. 2299 ( MICH , TAN ); RN 6 , PK [ Pointe Kilometrique roadmarker ] 525, 57 km N of Ambanja , 13°26’12”S 48°47’34”E , 17 m , 8.III.2016 , van Ee et al. 2382 ( MICH , TAN ); Ambanja , Nosy Be , 16.XII.1921 , Waterlot 289 ( P ); ibid loc ., Waterlot 291 ( P ); Manongarivo , Ambahatra , 13°58’S 48°27’E , 400 m , 15.III.1999 , Wohlhauser 60050 ( G , K , MO , P ); Manongarivo , Antafia Be , Amatolary , Moyen Ambahatra , 13°55’S 48°27’E , 230 m , 7.V.1999 , Wohlhauser SW60113 ( G , K , MO , P ). Prov. Mahajanga : Sofia Reg. , Analalava Distr ., Maromandia ( Befotaka ), 16.IX.1922 , Decary 999 ( P ); Haut Bemarivo , VIII.1907 , Perrier de la Bâthie 9556 ( P ); Melaky Reg. , env. de Morafenobe , 3.X.1923 , Decary 2359 ( P ); Boeny Reg. , Tsingy de Namoroka , 4.IV.1933 , Service Forestier 16 ( P ); RN 6 , PK 449 , 19 km S of Ambanja , 13°46’56”S 48°20’59”E , 25 m , 3.XI.2009 , van Ee et al. 1142 ( MICH ); RN 6 , PK 413 , 55 km S of Ambanja , 14°00’04”S 48°10’06”E , 100-140 m , 3.XI.2009 , van Ee et al. 1147 ( MICH ); Betsiboka Reg. , RN 4 , PK 227 , 88 km S of Moevaharana , 17°31’03”S 46°58’41”E , 200 m , 6.XI.2009 , van Ee et al. 1165 ( MICH ); RN 6 south of Ambanja , 13°55’44”S 48°12’58”E , 201 m , 8.III.2016 , van Ee et al. 2384 ( MICH , TAN ); Along Route Nationale 6 , at PK 399 , 14°05’22”S 48°06’42”E , 214 m , 8.III.2016 , van Ee et al. 2386 ( MICH , TAN ); ibid loc. , van Ee et al. 2388 ( MICH , TAN ).