Systematic Botany (2011), 36(1): pp. 33–48 © Copyright 2011 by the American Society of Plant Taxonomists DOI 10.1600/036364411X553108 Revision of the African Genus Hexalobus (Annonaceae) Marleen Botermans , 1 Marc S. M. Sosef , 1 Lars W. Chatrou , 1 and Thomas L. P. Couvreur 2 , 3 1 Netherlands Centre for Biodiversity (section NHN) / Biosystematics Group, Wageningen University, Generaal Foulkesweg 37, 6703 BL Wageningen, The Netherlands 2 The New York Botanical Garden, 200th St. and Kazimiroff Blvd, Bronx, New York 10458-5126, U. S. A. 3 Author for correspondence ([email protected]) Communicating Editor: Andrew Hipp Abstract— The genus Hexalobus consists of five species characterized by six basally fused petal lobes that are transversally folded in bud, which is unique within Annonaceae. The genus is widespread across tropical Africa occurring in rain forest, savanna, and woodland. The species H. callicarpus , occurring in Madagascar, is excluded from Hexalobus , so the genus is now restricted to continental Africa. The present revision provides a synthesis of previously published information and discussions on morphology, taxonomy, phylogeny, and palynology. Conservation status assessments are provided for each species, as well as a diagnostic key and detailed species descriptions. Furthermore, four species are illustrated and all species are mapped. Keywords— Africa , Annonaceae , distribution , Hexalobus , IUCN conservation status , pollen , taxonomy. Annonaceae is a pantropical family of trees, shrubs, and The usually-fragrant flowers of Hexalobus are solitary or lianas contributing significantly to the diversity of trees in clustered in groups of two or three, on an axillary short shoot, rain forests around the world ( Gentry 1993 ; Tchouto et al. referred to as a flower stalk in our descriptions. The flower 2006 ; Punyasena et al. 2008 ). Africa (including Madagascar) stalk is divided by an articulation into an upper and a lower is the least diverse region in terms of species numbers (ca. part. The subsessile or stalked flowers grow on leafy or leaf- 390) when compared to Southeast Asia (ca. 1,000) and the less branches, or on the trunk. Cauliflory is common within Neotropics (ca. 900) (Richardson et al. in press). The African the Annonaceae, having been documented in several other genera were last treated as a whole over 100 yr ago by Engler genera ( van Heusden 1992 ). and Diels (1901) and today the state of our taxonomic knowl- Flower buds are ovoid to almost globose. Up to six con- edge of African Annonaceae is poor ( Couvreur et al. 2006 ). vex, soon-falling bracts develop in the lower part of the stalk Recently a few taxonomic revisions of African genera have and sometimes produce an additional axillary shoot. The two been published ( Versteegh and Sosef 2007 ; Couvreur 2009 ) upper bracts are attached near the articulation enclosing the and the one presented here is another step towards clarifying bud when young. These bracts are free or appear to be fused the taxonomy of this important tropical family. ( Fig. 2 ) at their base and then form a tube ( Fries 1930 ; pers. Hexalobus contains five species of large trees or shrubs dis- obs.). Fused bracts might appear unusual as they normally tributed across tropical Africa varying in their habitat from develop one at a time. The possibility of this feature being the primary rain forests to savannas and woodlands. Two spe- result of a single bract enveloping the flower bud and then cies are relatively widespread, while the other three have rupturing when the flower develops, as reported in Fusea restricted distributions. Hexalobus monopetalus has one of the ( Chatrou and He 1999 ), does not seem likely. Indeed, after the widest distributions known in African Annonaceae, ranging examination of several specimens, the bracts appeared identi- Delivered by Ingenta to IP: 192.168.39.151 on: Fri, 24 Sep 2021 12:35:23 Copyright (c) American Society for Plant Taxonomists. All rights reserved. from West Africa to East Africa. The genus’ center of diver- cal in shape and are never found to be irregularly ruptured. sity lies in Cameroon with four species, including one narrow As for the majority of Annonaceae genera, the flowers endemic. Cameroon is also the center of diversity for sev- consist of three sepals and six petals ( van Heusden 1992 ). eral other closely related African Annonaceae genera such as The sepals are large and enclose the petals until anthesis, a Isolona (9 out of 20 species ( Couvreur 2009 )), Monodora (6 out character shared with its sister genus Uvariastrum . In con- of 14 species ( Couvreur 2009 )) and Uvariastrum (three out of trast, the sepals in both Asteranthe and Isolona enclose the ca. five, Couvreur unpublished data). petals only during the early stages of flower development, In a recent molecular phylogenetic study focusing on while in Monodora the sepals almost never enclose the petals African Annonaceae ( Couvreur et al. 2008b ), Hexalobus clus- ( Couvreur 2009 ). In bud the sepal margins are valvate and tered within the so-called long-branch clade (LBC), one of never reduplicate-valvate, (i.e. margins curved outwards), as the largest clades recognized in the family ( Richardson et al. reported by van Heusden (1992) . Reduplicate-valvate sepals 2004 ). Within the LBC, Hexalobus was nested in a large clade of are, however, found in Uvariastrum (Couvreur pers. obs.). 11 African genera referred to as the African long-branch clade The sides of the rather fleshy sepals are densely covered with (ALBC; Fig. 1 ) and was recovered as sister to Uvariastrum , curly hairs interlocking adjacent sepals in bud. these two being in turn sister to the East African endemic In Hexalobus the petals are fused at the base, forming a genus Asteranthe . These three genera were in turn sister to a short tube with six corolla lobes. Fusion of petals, or sym- clade consisting of Isolona and Monodora . petaly, is an uncommon character within Annonaceae ( van The last revision of Hexalobus dates back to 1930 ( Fries Heusden 1992 ). However, Asteranthe , Isolona , Monodora, and 1930 ). However, in the subsequent 80 yr several new spe- the monotypic endemic East African genus Sanrafaelia all cies names have been published and a large amount of plant share this feature ( Couvreur et al. 2008b ). Sympetaly has material has been collected. This paper presents a taxonomic also independently evolved in isolated species within such revision of the genus Hexalobus and is based on an extensive genera as Disepalum ( Johnson 1989 ), Fusaea ( Chatrou and He examination of herbarium collections and additional field 1999 ), and Haplostichantus ( van Heusden 1994 ), and in small observations. clades within large genera such as in species formerly placed 33 34 SYSTEMATIC BOTANY [Volume 36 appearance (e.g. Fig. 3A ). They are cream to yellow, some- times with a dark red or purple basal rim on the inner side. The stamens are numerous, being narrowly obtriangular or oblong in shape. The two thecae are united by the connective which is often prolonged apically. The shape of the apex is variable and is referred to here as the connective shield. The pollen of Hexalobus is shed as tetrads, a character shared by most genera of the ALBC ( Couvreur et al. 2008a ; Couvreur et al. 2008b ). As with most Annonaceae, the gynoecium is apocarpous with the carpels freely arranged. Within Annonaceae, only the sister genera Isolona and Monodora have a syncarpous gynoe- cium ( Deroin 1997 ; Couvreur et al. 2008b ; Couvreur 2009 ), Fig. 1. Cladogram of the phylogenetic relationships within the while various others develop syncarpous fruits from apocar- African long branch clade (modified from Couvreur et al. 2008b ). All branches received high values after maximum parsimony bootstrap anal- pous gynoecia (termed pseudosyncarpy, found for example ysis (> 85%) and Baysian inference posterior probabilities (> 0.95). in the Neotropical/African genera Duguetia and Annona , ( Chatrou et al. 2000 ). Carpel number varies between one to ca. 16 topped by a sessile stigma which is fleshy and essen- in Raimondia ( Westra 1995 ), but now included in Annona tially flat, but with in-rolling lateral margins, thus becom- ( Rainer 2001 ). ing seemingly bilobed ( Fig. 4E ). Hexalobus mossambicensis is The corolla lobes are thin and transversely folded in the bud, unique in the genus, as the flowers have only a single car- which is a unique character within the family ( van Heusden pel. Monocarpelly is thought to be found in ca. 10% of the 1992 ). The unfolded petals have a characteristic “wrinkled” Annonaceae species ( Deroin 1997 ). Other genera contain- ing monocarpellate species include Cyathocalyx ( Wang and Saunders 2006b ; Wang and Saunders 2006a ), Pseuduvaria ( Su and Saunders 2006 ) and Uvaria ( Verdcourt and Mwasumbi 1988 ), while all species in Mezzettia and in the monotypic gen- era Sanrafaelia ( Verdcourt 1996 ), Dielsiothamnus , and Tridimeris are monocarpellate ( van Heusden 1992 ). The fruits of Hexalobus are apocarpous with up to eight ses- sile or subsessile, indehiscent monocarps that are obovoid to ellipsoid. The surface of the monocarps varies from smooth to irregularly ridged and verrucose. The sessile or subsessile monocarps represent the only morphological character known to be common to all eleven genera of the ALBC ( Couvreur et al. 2008b ). Taxonomic History— Richard (1831) was the first to describe a species that was later accommodated in Hexalobus : Uvaria monopetala A. Rich. The genus Hexalobus was established a Delivered by Ingenta to IP: 192.168.39.151 on: Fri, 24 Sep 2021 12:35:23 Copyright (c) American Society for Plant Taxonomists. All rights reserved. year later by de Candolle (1832) , distinguishing it from the genus Uvaria by its corolla lobes fused at their base. Within this genus he described two species: H. senegalensis A. DC. and H. madagascariensis A. DC. The latter species name has been transferred to the genus Isolona ( Diels 1925 ) as I. mada- gascariensis (Baill.) Engl. ( Couvreur 2009 ). Unfortunately, de Candolle (1832) treated the previously published name Uvaria monopetala as a synonym of H.