Research Article |
Corresponding author: Thomas L.P. Couvreur ( thomas.couvreur@ird.fr ) Academic editor: Pavel Stoev
© 2015 Thomas L.P. Couvreur, Raoul Niangadouma, Bonaventure Sonké, Hervé Sauquet.
This is an open access article distributed under the terms of the Creative Commons Attribution License (CC BY 4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Citation:
Couvreur TLP, Niangadouma R, Sonké B, Sauquet H (2015) Sirdavidia, an extraordinary new genus of Annonaceae from Gabon. PhytoKeys 46: 1-19. https://doi.org/10.3897/phytokeys.46.8937
|
A distinctive new monotypic genus from Gabon is described in the tropical plant family Annonaceae: Sirdavidia, in honor to Sir David Attenborough. Molecular phylogenetic analyses confirm that Sirdavidia, which is very distinct from a morphological standpoint, is not nested in any existing genus of Annonaceae and belongs to tribe Piptostigmateae (subfamily Malmeoideae), which now contains a total of six genera. The genus is characterized by long acuminate leaves, fully reflexed red petals, 16–19 bright yellow, loosely arranged stamens forming a cone, and a single carpel topped by a conspicuous stigma. With just three known collections, a preliminary IUCN conservation status assessment is provided as “endangered” as well as a distribution map. The discovery of Sirdavidia is remarkable at several levels. First, it was collected near the road in one of the botanically best-known regions of Gabon: Monts de Cristal National Park. Second, its sister group is the genus Mwasumbia, also monotypic, endemic to a small area in a forest in Tanzania, some 3000 km away. Finally, the floral morphology is highly suggestive of a buzz pollination syndrome. If confirmed, this would be the first documentation of such a pollination syndrome in Magnoliidae and early-diverging angiosperms in general.
Un nouveau genre monotypique du Gabon est décrit dans la famille tropicale des Annonaceae: Sirdavidia, en honneur à Sir David Attenborough. Des analyses phylogénétiques confirment que Sirdavidia, caractérisé par une morphologie unique, n’appartient à aucun genre connu d’Annonaceae et se place au sein de la tribu des Piptostigmateae (dans la sous-famille des Malmeoideae), laquelle compte désormais un total de six genres. Le genre est caractérisé par des feuilles avec un long acumen, des pétales rouges réfléchis, 16–19 étamines jaunes qui forment un cône lâche et un carpelle surmonté d’un stigmate bien visible. Avec seulement trois récoltes connues, un statut de conservation préliminaire de “endangered” est proposé sur la base des critères de l’UICN. Une carte de distribution est également fournie. La découverte de Sirdavidia est remarquable pour plusieurs raisons. Tout d’abord le nouveau genre a été collecté près de la route dans l’une des régions les plus connues botaniquement du Gabon: le Parc National des Monts de Cristal. Ensuite, son groupe-frère est le genre, Mwasumbia, également monotypique, endémique d’une petite région en Tanzanie à plus de 3000 km. Enfin, les caractères floraux suggèrent un syndrome de pollinisation appélé « buzz pollination». Si cela se confirme, ce sera la première documentation de ce type de syndrome pour les Magnoliidae et les Angiospermes basales en général.
Piptostigmateae , Monts de Cristal, buzz pollination, vicariance, Annonaceae , Central Africa, Magnoliidae
The Central African country of Gabon is merely 270 000 km² in size, but is home to an incredible botanical diversity (
Annonaceae (Magnoliidae) is a pantropical flowering plant family of trees, shrubs and lianas. With around 2500 species (
A probable new genus of Annonaceae was collected during field work in Monts de Cristal National Park, as part of a larger field trip focusing on the study Magnoliidae floral diversity. The objective of this paper was to confirm its status as a new species and its classification in a new genus. The taxon was first seen near the Kinguélé dam, and further prospection in the area revealed several individuals. It is the unusual floral structure of this species for Annonaceae that led us to suspect it might represent a new taxon and to undertake both a phylogenetic analysis and more thorough morphological observations. As we show here, interesting tropical taxa unknown to science can still be discovered in places even considered to be well known botanically.
Herbarium, alcohol and photographic materials were used to produce the descriptions. In order to identify other specimens of this new genus, we looked at all undetermined Annonaceae specimens in the herbaria located at BR, BRLU, LBV, P and YA (herbarium acronyms according to
A preliminary phylogenetic analysis indicated that the new taxon was nested in tribe Piptostigmateae of the Malmeoideae subfamily. Therefore, the data matrix of
DNA extractions of silicagel-dried leaf samples from two individuals of Sirdavidia solannona Couvreur & Sauquet were performed using a DNeasy Plant Mini Kit (Qiagen, Valencia, CA). The universal primers C/D and E/F (
Maximum Parsimony (MP) analyses were performed using PAUP* (version 4.10b;
Maximum likelihood analyses were conducted using RAxML version 7.2.7 (
All Genbank numbers used can be found in
Both markers represented 2669 total characters, 187 of which were excluded because of ambiguity in the alignment and 407 (16.5%) were parsimony informative. Both MP and ML phylogenetic analyses led to the same topology, with similar levels of support (Fig.
Genus with Solanum-like flowers, inflorescences axillary or cauliflorous, sepals valvate, petals valvate, subequal, recurved at anthesis, red; stamens bright yellow; carpel single; monocarp sessile, placentation lateral, ovules uniseriate.
Sirdavidia solannona Couvreur & Sauquet.
Small trees with distichous, simple pinnately veined leaves with an entire margin and reticulate third-order venation. Species androdioecious (?) (flowers unisexual staminate or bisexual). Inflorescences one to three-flowered, axillary on old branches or at base of trunk, with one to three short sympodial rachilla. Flowers actinomorphic. Perianth of 9 free tepals in 3 alternate, valvate whorls of 3 each, differentiated in outer tepals (sepals) and middle and inner tepals (petals). Petals similar (subequal in length), spreading horizontally or reflexed at anthesis. Stamens 16-19, free, basifixed with a very short filament. Anthers introrse, probably opening by two longitudinal slits, connectives tongue shaped, yellow. Carpel one, densely pubescent, stigma cylindrical coiled, ovules 7–10, uniseriate. Monocarp sessile, cylindrical densely pubescent.
A single species only known to Gabon (Fig.
We dedicate this new genus to Sir David Attenborough, British broadcaster and naturalist, in honor of his lifelong dedication to nature, conservation, evolution and natural history programs. His passion for nature have influenced and inspired a generation of biologists and naturalists, including the first and senior authors of this paper.
Maximum likelihood tree with support values indicated on branches (ML bootstrap above; MP bootstrap below). Flower morphology of the genera in the Piptostigmateae tribe. a Annickia affinis (Exell) Versteegh & Sosef b Greenwayodendron suaveolens (Engl. & Diels) Verdc c Piptostigma multinervium Engl. & Diels d Polyceratocarpus parviflorus (Baker) Ghesq e Sirdavidia solannona f Mwasumbia alba. Photos: TLP Couvreur. Note: there is some confusion around the proper identification of the accession Lugas 111 (Woodiellantha sp in this study).
Gabon, Estuaire, Monts de Cristal, near first bridge after Kinguele, 0°46'66"N, 10°27'81"E, T.L.P. Couvreur 596, 15 Nov 2013, Fl. & Fr., holotype: WAG!; isotypes: LBV!, P!, YA!.
Tree 4–6 m tall, 2 to 4 cm in diameter at breast hight (d.b.h.), bark dark brown with patches of green, old branches black, glabrous, young branches black, sometimes pubescent. Leaves distichous, simple, entire, pinnately veined. Petiole 3–4 mm long, 2–3 mm in diameter, glabrous or sparsely pubescent when young, slightly grooved on top, leaf lamina inserted on top. Lamina 20–26 cm long, 4.5 to 9 cm wide, length:width ratio 2.5 to 4.5, narrowly elliptic to elliptic to narrowly ovate to ovate, apex long acuminate, acumen 2–3 cm long, base obtuse, coriaceous, young sparsely pubescent to glabrous above, glabrous below, old leaves glabrous above and below, mid rib sunken above, sparsely pubescent when young below, glabrous above, glabrous above and below when old, secondary veins 9–12 pairs. Inflorescences axillary, on old branches and cauliflorous towards the base of the trunk. Sympodial rachis up to 6 mm long, but sometimes up to 1.5 cm long, densely covered with short appressed hairs, with 0–10 minute densely packed lower bracts densely pubescent brown. Flowering pedicels 2 to 10 mm long, densely covered with short appressed hairs, red, upper bract inserted at base or up to ½ of pedicel, covered with short appressed hairs, red. Flowers actinomorphic, bisexual or unisexual staminate (androdioecious), with 9 tepals in total, differentiated in one whorl of 3 sepals and 2 whorls of 3 petals, all alternate. Sepals 2–3 mm long, 1.5–2 mm wide, length:width ratio 1.5, ovate, valvate, apex acute, base truncate, densely covered with short appressed hairs outside, glabrous inside, red. Outer petals 4–10 mm long, 2.5 to 5 mm wide, length:width ratio 2 to 2.5, elliptic, apex acute, base truncate, densely pubescent with appressed hairs outside, densely pubescent with short tomentose hairs inside, deep red. Inner petals 4–9 mm long, 2–4 mm wide, length:width ratio=2 to 2.5, elliptic, apex acute, base truncate, densely pubescent with short tomentose hairs outside, densely pubescent with short tomentose hairs inside along margins, glabrous towards center, deep red. Petals spreading horizontally or recurving backwards at anthesis. In staminate and bisexual flowers, stamens 16–19, 3–4 mm long, outer ones shorter than inner ones, filament shorter than 0.2 mm, narrow, connective umbonate (tongue shaped), glabrous, bright yellow. Anthers introrse, probably opening by two longitudinal slits. In bisexual flowers, carpel one, 4–5 mm long, ca. 1 mm wide, densely pubescent with silvery long appressed hairs, ovules uniseriate, 7–10, stigma cylindrical coiled, 2–3 mm long, sparsely pubescent towards the top, white cream. Mature fruits not seen, young fruiting pedicel 6 mm long, densely pubescent with appressed hairs. Young monocarp cylindrical, densely pubescent with silvery appressed hairs. Seeds not seen. (Figs
Flowers collected in April and November, young fruits collected in November.
Sirdavidia is endemic to Gabon, with three known collections: two near the Kinguele dam in the Monts de Cristal National Park, Mbé sector, and one south of the Ivindo National Park (Fig.
Endangered [EN B1ac]. Two localities in Gabon are known for this species: Monts de Cristal N.P. and south of the Ivindo N.P. The population found in Kinguele (Monts de Cristal) was close to the road and several (around 10) individuals were seen. We also looked for this species in other parts of the Park (around Tchimbélé) and did not see it again. The herbarium specimen collected from Ivindo indicates “en peuplement” (in population) suggesting that several individuals were seen. However, the coordinates on the herbarium sheet place this collection outside the national park. The Area of occupancy (AOO) is 12,000 km² and the Extent of occurrence (EOO) is 6.2 km², suggesting a very restricted overall distribution. We thus suggest a status of endangered given that only a handful of individuals have been seen and that these populations are quite close to disturbances.
The species name epiteth highlights the striking resemblance with flowers of some species of Solanum, an unusual and new feature for a flower of Annonaceae.
The androdioecious nature of Sirdavidia solannona has yet to be properly confirmed. We only saw two individuals one of which appeared to have only staminate flowers. Because other members of the tribe Piptostigmateae are known to have this condition, it would not be surprising.
Gabon: Estuaire, Monts de Cristal National Park, near first bridge after Kinguele, 0°46'64"N, 10°27'80"E, T.L.P. Couvreur 597, Fl., 15 Nov 2013, Fl. & Fr. (LBV!, P!, WAG!, YA!); Ougoué-Ivindo, Ivindo National Park, camp elephant, A. Moungazi 1544, Fl., 10 Avr 204 (BR!, LBV, WAG).
Illustration of Sirdavidia solannona Couvreur & Sauquet. A Flowering branch (flower bud just above second leaf from the bottom) B Flower C One sepal, outer side view D One sepal, inner side view E Flower bud F Outer petal, outer side view G detail of pubescence of outer petal, outer side H Outer petal, inner side view I Inner petal, outer side view J detail of pubescence of inner petal, outer side K Inner petal, inner side view L detail of pubescence of inner petal, inner side M Stamen from inner whorl N stamen from outer whorl O Longitudinal section of carpel showing uniseriate row of ovules (stigma missing) P detail of young fruit. Drawing by Hans de Vries based on Couvreur 596 and Couvreur 597.
Sirdavidia solannona. a Opened flower and flower buds (Couvreur 596) b Flower with recurved petals at anthesis (Couvreur 596) c Staminate flower (Couvreur 597) d Flower with all petals and part of the stamens removed, showing the silvery aspect of the carpel and the long stigma (Couvreur 596) e Cauliflorous flower and flower bud (Couvreur 596) f Young fruit, cauliflorous (Couvreur 596). Photos: TLP Couvreur.
Morphological characters of the six genera found in tribe Piptostigmateae. Modified from
Genus | Annickia | Greenwayodendron | Mwasumbia | Sirdavidia | Piptostigma fasciculatum | Piptostigma | Polyceratocarpus |
---|---|---|---|---|---|---|---|
Character | |||||||
Species diversity/distribution | 8 / West and Central Africa, 1 species in East Africa | 2 / West and Central Africa | 1 / Tanzania | 1 /Gabon | 1 / Central Africa | ~14 / Central and West Africa | 8 / West and Central Africa, 2 species in East Africa |
Tertiary venation | intermediate | reticulate | intermediate | reticulate | parallel | parallel | parallel |
Inflorescence position | terminal | terminal | axillary | axillary, cauliflorous | axillary | axillary, cauliflorous | axillary, cauliflorous |
Sex distribution | bisexual | androdioecious | bisexual (?) | androdioecious (?) | bisexual | bisexual | androdioecious |
Sepal aestivation | valvate | imbricate | imbricate | valvate | valvate | valvate | valvate |
Petal number | 3 | 6 | 6 | 6 | 6 | 6 | 6 |
Petal disposition | Upright, appressed forming a pollination chamber | Spreading horizontally, no pollination chamber | Outer petals recurved backwards, inner petals erect upwards, no pollination chamber | Recurving backwards to spreading horizontally, no pollination chamber | Pendulous, no pollination chamber | Upright, appressed forming a pollination chamber | Outer petals recurved backwards or erect upwards, inner petals erect upwards, pollination chamber possible |
Petal relative length | outer absent | outer=inner | outer=inner | outer=inner | outer<inner | outer<inner | outer=inner |
Torus (stamen portion) | flat/conical | flat/conical | short cylindrical | short cylindrical | short cylindrical | short cylindrical | short cylindrical |
Torus (carpel portion) | flat/convex | flat/convex | concave | concave | concave | concave | concave |
Apex of connective | discoid/tongue-shaped | discoid/tongue-shaped | discoid | discoid/tongue-shaped | discoid | discoid | discoid |
Nr of carpels | numerous | 13–20 | 4 | 1 | 4 | 3–14 | 2–20 |
Number of ovules per carpel | 1 | 2 | 5–8 | 7 | ~ 18 | 6–10 | 20–30 |
Ovule arrangement | basal | 1-seriate lateral | 1-seriate lateral | 1-seriate lateral | 2-seriate | 2 or 1-seriate lateral | 2-seriate lateral |
Monocarps | stipitate | stipitate | sessile | sessile | sessile | sessile | sessile |
The molecular phylogenetic analyses presented here confirms that Sirdavidia solannona belongs to tribe Piptostigmateae, which now contains a total of six accepted genera (though Piptostigma is paraphyletic,
Sirdavidia differs morphologically from Mwasumbia in several important respects, warranting its status as a new species and a new genus. Tertiary venation is a useful character for distinguishing genera within the tribe Piptostigmateae (
We suggest that the morphological differences outlined above are sufficient to erect a new species for Sirdavidia solannona and also justify the creation of a new genus, distinct from Mwasumbia, given the morphological characters that discriminate among genera of Annonaceae in general (
Table
– Inflorescence position: Within Piptostigmateae both terminal or axillary types of inflorescences can be found (
– Monocarp base: Another synapomorphy for the SMPP clade is the sessile monocarps. In contrast, Annickia Setten & Maas and Greenwayodendron Verdc. have monocarps with conspicuous stipes. Even though immature fruits were only observed for Sirdavidia to date, it is clear that the single monocarp is sessile (Fig.
Other characters appear to have little taxonomic use but are interesting as they underline the important floral morphological variability within Piptostigmateae.
– Androdioecy in Annonaceae is not unusual (
– Sirdavidia is unique within the tribe in having a single carpel, a feature found in only 10% of Annonaceae (
Sirdavidia is fascinating at a number of other different levels. First, it had remained undescribed until now, even though it occurred in a well known and well inventoried region of Gabon; second, its closest relative is another monotypic genus restricted to Tanzania, some 3000 km away; and, finally, it could be the first documentation of a buzz pollination syndrome in Magnoliidae.
Sirdavidia was discovered in the Monts de Cristal National Park (N.P.), one of the most species-rich and botanically best collected regions in Gabon (
The closest relative to Sirdavidia is another recently described monotypic genus, Mwasumbia (
Though the flower has all the structural characters of a typical Annonaceae flower (3 sepals, 2 whorls of 3 petals), the overall aspect is very unusual, resembling flowers of some species of Solanum L. (Solanaceae). The morphological appearance is strongly suggestive of a special type of pollination syndrome referred to as buzz pollination syndrome. Buzz pollination relies mostly on sonicating bees that use vibrations to extract pollen from the anthers (
Reflexed petals. Most buzz pollinated flowers show strongly reflexed petals exposing the stamens and the carpels. Reflexed petals are quite common in Annonaceae, occurring in a number of genera such as Uvaria and Isolona.
Stamens: The stamens of Sirdavidia are bright yellow, a color known to attract bees (
Anthers. In typical buzz pollinated flowers, the anthers generally have apical pores or short slits that release the pollen grains during vibration. However, non-poricidal anthers have also been linked with buzz pollination in a number of other genera (
Long stigma. The conspicuous stigma sticking out of the stamens in Sirdavidia is also a typical feature of buzz pollinated flowers (
Annonaceae flowers are visited by a large variety of insects (
Isabelle Morlais and the OCEAC lab members are thanked for allowing us to undertake the DNA extractions and PCR amplifications of the material. Adama Faye is thanked for his assistance in the lab. Richard Saunders and one anonymous reviewer are thanked for detailed comments on the MS. We are also grateful to the Centre National de la Recherche Scientifique et Technique (CENAREST) in Gabon and the Agence National des Parques Nationaux (ANPN) for delivering the necessary research permits. Jan Wieringa is thanked for help with both the genus and epithet names. Hans de Vries is kindly thanked for his botanical illustration of Sirdavidia solannona. Last, we also thank Jürg Schönenberger, Yannick Staedler, and Peter Endress for discussions on buzz pollination and comments on earlier versions of the article. Field work in Gabon was supported by the Agence Nationale de la Recherche (grant number ANR-12-JVS7-0015-01 to HS).