vegetative and reproductive parts, however, the taxonomic utility of most of their morphological characters is limited to inter- and infraspecific delimitations.
Habit: The species of Neotropical Sabicea are predominantly vines, lianas or (sub-) shrubs with lianescent branches. Only two species, S. brasiliensis and S. humilis, are known as erect. Few species occasionally display the erect and few a suffruticose growth habit. The habit character is taxonomically barely applicable in recognizing the species of Neotropical Sabicea.
Indumentum: In most of Neotropical Sabicea, indumentum of branchlets is comprised of two to few types and appears taxonomically useless. However, the exclusively arachnose or lanate to lanuginose indumentum types or their presence-absence in addition to other indument types are taxonomically useful in specific or infraspecific delimitation. The indumentum types of upper and lower surface of leaves, especially the presence-absence of arachnose or lanuginose to lanate indumentum appears stable in most species (Chapter 6.3, Fig. 2A, F, G, I, J, K, Fig. 18A-C, 21A-C, 23A-C, 28A-C). The presence-absence, types and distribution of indumentum at inner surface of stipules (Chapter 6.3, Fig. 5A, 35E), bracts, and
calyces (Chapter 6.3, Fig. 5E, F, J, 21G, J, 25G, 30F, 32G, 34J, 35H, K, 42I), especially at upper part, entire or serrulate to sparsely denticulate margins, and presence-absence of cilia (Chapter 6.3, Fig. 5D, J, 11H, 22G, 28H, 35D, G, K, 37F) appear stable for some species or group of species. The indumentum types of outer surface of corolla tube, especially the erectness and orientation of trichomes (Chapter 6.3, Fig. 5H, 8H, 13G, 21H, 23F, 41F, 44F), are stable in most of the species and have been found applicable in interspecific delimitation.
The indumentum characters of upper and lower surface of leaves, inner and external surface of stipules, bracts, and calyces, and external surface of corolla tubes, and ovaries are useful in taxonomic delimitation, usually with and sometimes without the combination of other diagnostic characters. The usefulness of indument characters of stipules bracts and inners surface of calyx lobes is hardly known from previous studies.
The colleters of Sabicea are almost unknown from the previous studies except those of Steyermark (1967, 1974). In this study, the position of colleters has been found as an important source of taxonomic characters. The number and location of colleters inside the base or basal part of bracts and at or near the sinus or near the middle inside the calyx tubes (Chapter 6.3, Fig. 5F, J, 26G, 32G, 34J, 42I) have been found as discrete and consistent which indicate their taxonomic utility in species delimitation.
Stipules: The ranges of variation in size (2–20 × 2–15 mm), margins (Chapter 6.3, Fig.
5D), orientation, division, and number of main veins (5–24) per stipule seem stable in some species. The stipule characters of Neotropical Sabicea appear useful for some inter- or infraspecific delimitations.
Leaves: Although the leaf shape or size hardly have been found constant, the variation in leaf apex and leaf base (Chapter 6.3, Fig. 5A, 23A, 34A, 44A), and thickness, length (2–18 cm) and width (0.5–11 cm) of lamina appear discrete and stable in some species, indicating the limited usefulness of these characters. The variation in number (7–20 pairs) and position of costa and secondary veins at upper leaf surface, and the length (0.2–5 cm) of petioles appear occasionally constant due to which their taxonomic utility is very narrow.
Inflorescences: The inflorescences are variable from sessile to (sub-) sessile, (sub-) sessile to shortly (3–8 mm long) pedunculate, and distinctly (1–4.5 cm long) pedunculate.
Accordingly, the inflorescence are comprised of verticillate to glomerulate, verticillate (Chapter 6.3, Fig. 36A, D, Fig. 17A, E, 46A, E,), capitate (Chapter 6.3, Fig. 40A, F), capitate to compact fasciculate (Chapter 6.3, 15A, F, 34A, F), compact fasciculate (Chapter 6.3, Fig. 5A, E, 32A, D42E), verticillate to umbellate, umbellate (Chapter 6.3, Fig. 26D, 31E, 35F), or paniculate (Chapter 6.3, Fig. 37E), and lax paniculate or thyrsoid (Chapter 6.3, Fig. 22A, 41A) types.
This variation in inflorescence structures is not always discrete and constant, however, mostly found as important taxonomic character for species delimitation, in addition to other characters. The range of variation in inflorescence size (1–8 × 0.7–7.5 cm, excluding peduncles), lengths of primary axis (0.1–6.5 cm) and flower numbers (1–88) per inflorescence appear as constant for few groups of species. The division of bracts, length and diameter of
involucre, length and width of exinvolucrate bracts, and apex and margins of bracts appear as the source of some important characters that can be useful for interspecific delimitation.
Flowers: Many Neotropical Sabicea species produce usually pedicellate flowers, 16 species sessile to subsessile flowers, and only four species strictly sessile flowers. The ranges of variation in pedicel lengths (0.5–15 mm) are mostly coinciding but distinct only in a few species. The types of calyces (Chapter 6.3, Fig. 5H, J, 8E, H, J, 29E, H, 32E, G, 42G, I), lengths and diameters of calyx tubes (0.3–11 mm and 0.8–6.5 mm respectively) and lengths and widths (0.2–15 mm and 0.1–7 mm, respectively) of calyx lobes, and the shape (Chapter 6.3, Fig. 5J, H, 8H, J 23F, 28F, H, 33F, 34H, 43F, H), erectness, margins and apex type of calyx lobes in Neotropical Sabicea are proved as noteworthy, though sometimes labile.
Markedly unequal calyx lobes exist in few species (Chapter 6.3, Fig. 30D, F). Lengths of corolla tubes (2.7 mm to 25 mm) and widths (1.5 to 7 mm), length-width ratios or shape of corolla lobes appear to be species-specific for some species. The insertion points of stamens in corolla tubes (at 1.8–20 mm from the base of tubes) and anther’s lengths (0.8–4 mm) show a considerable range of variation that seem consistent for few groups of species. The taxonomic utility of locule number seems unreliable due to its overlapping and unstable variation.
Fruits and Seeds: The ranges of variation in colour (pale to dark red or crimson, pinkish, purplish, violet), size of fruits (5–18 × 5–18 mm) and size of seeds (0.3–1 × 0.2–0.8) appear as narrow and unstable for most of the species due to which these characters appear taxonomically inapplicable for inter- and infraspecific delimitation.
It has not yet been investigated in detail whether the sharing of characters by two or more species of Neotropical Sabicea is due to homoplasy or synapomorphy. In this study it appeared impossible to recognize all Neotropical Sabicea from African Sabicea based on any consistent character. Apart from African Sabicea, the Neotropical species of Sabicea do not share also any synapomorphic character. Therefore, the characteristics of Neotropical Sabicea found in this revisionary study are inconsistent to their emerging as a monophyletic group in Khan & al. (2007), but consistent to their close relationships with African Sabicea. It has been shown in other families that geography is sometimes a better indication of relationship than character similarity, which might have evolved due to similar environmental pressures (e.g., Liede-Schumann & al., 2005). In this study, it has been revealed that it is impossible to characterize most of the Neotropical species Sabicea based on any single or unique character. Finally, this study forecasts the prospects of further comprehensive studies for the reclassification within the tribe Sabiceeae, especially within the genera Sabicea s.l.
and Virectaria, continuing the exploration of the genus Sabicea in the Neotropics, and the revisionary work on African Sabicea. Based on the formidability and restrictions experienced during the revisionary work, this study evokes the urgency of collaborative scientific involvements to accomplish the revision of the genus of tropical Africa.
3. SUMMARY
The pantropical tribe Sabiceeae (Ixoroideae s.l., Rubiaceae) has been variously circumscribed previously, resulting in strong conflicts in its tribal and generic limits. The monophyly of Sabiceeae including its all established genera or the monophyly of any non-monotypic genus traditionally included in this tribe has never been examined using molecular data sets. Neither the relationships within this tribe, nor the relationships within any of its genera have ever been explored using molecular data. Sabicea, the type and most species rich genus of the tribe and the single genus of Rubiaceae showing African-Asian-American disjunction, has not been revised to any extent after its first monographic treatment (Wernham, 1914), mostly based on typological concept, although the second major genus Virectaria has been revised recently (Dessein & al., 2001b). These lacunae in phylogenetic and descriptive knowledge on the tribe Sabiceeae and its genera have evoked the need of the present study. This study has focused on the tribal circumscription of Sabiceeae and Virectarieae, monophyly and biogeography of Sabicea, phylogenetic relationships within the tribe Sabiceeae, monophyly of the genus Virectaria and relationships between its species, phylogeography of Virectaria, taxonomic revision of Neotropical Sabicea, and taxonomical utility of morphological characters for the classification of Neotropical Sabicea.
The present study reveals for the first time that neither the tribe Virectarieae, currently established as the associated tribe of Sabiceeae, nor the subtribe Virectariinae, recently proposed to accommodate the genera of Virectarieae, is monophyletic; rather, the tribe Sabiceeae including the genera of Virectarieae or Virectariinae is strongly resolved as a monophyletic group in trnT-F (Chapter 6.1, Fig. 1) and combined ITS-trnT-F trees (Chapter 6.1, Fig. 3). Consequently, this study suggests the broad circumscription of the tribe Sabiceeae (Sabiceeae s.l.) consisting of eight genera: Ecpoma, Hekistocarpa, Pseudosabicea, Sabicea, Schizostigma, Stipularia, Tamridaea, and Virectaria based on the robust phylogeny inferred from the analysis of ITS and trnT-F data (Chapter 6.1, Fig. 3).
Additionally, this study suggests the placement of both Pentaloncha and Temnopteryx, previously included in Sabiceeae, in subfamily Rubioideae. There is no potential morphological synapomorphy to diagnose this newly delimited Sabiceeae, nor to distinguish Virectarieae or Virectariinae. Therefore, the monophyly of the newly delimited Sabiceeae s.l.
is entirely based on molecular data.
This study further reveals that the genera Ecpoma, Pseudosabicea, Sabicea, Schizostigma, and Stipularia, traditionally associated with the tribe Sabiceeae, together form a monophyletic group and their morphological distinctions are not clear-cut. Therefore, all of these genera are merged under Sabicea s.l., and as result, finally the tribe Sabiceeae s.l. is recognized with four genera: Hekistocarpa, Sabicea s.l., Tamridaea, and Virectaria. The resolved clades of combined ITS-trnT-F tree (Chapter 6.1, Fig. 3) indicate that the São
Tomean, Malagasy, and all Neotropical Sabicea presumably originated from African ancestors. They reached São Tomé & Principe, Madagascar, and the Neotropics independently via three single long-distance dispersal events. Two hypotheses are postulated here for explaining the means of the major dispersal events- 1) by wind and/or ocean currents or 2) by birds. This study also indicates that most probably the major diversification of Sabicea s.l. started in mainland Africa and the second major radiation occurred through starting the colonization of the genus in the Neotropics. The presence of only one species– Sabicea ceylanica in Sri Lanka indicates the unsuccessful diversification of the genus in Asia.
The results of combined ITS-rpoC1-trnT-F analysis (Chapter 6.2, Fig. 1) suggest that the monotypic genus Hekistocarpa, restricted to Cameroon and Nigeria, is closely related with the group of the Guineo-Congolian wide genus Virectaria, the monotypic Tamridaea, confined to Socotra of Yemen, and the Pantropical Sabicea s.l., as Hekistocarpa is constantly resolved as sister to the Tamridaea-Virectaria-Sabicea clade. Within the Tamridaea-Virectaria-Sabicea clade, the Tamridaea-Virectaria Clade and the Sabicea Clade change their positions depending on the data set. Supporting morphological synapomorphies are absent here as well as in the whole tribe Sabiceeae s.l. The clade of all Virectaria accessions strongly resolved in the ITS-rpoC1-trnT-F tree supports the monophyly of the genus Virectaria, consistent with its ample morphological synapomorphies. The combined ETS-ITS-rpoC-trnT-F tree (Chapter 6.2, Fig. 2) exhibits the close relationships within the genus under two highly resolved groups, and the monophyly of the six sampled species of Virectaria in correspondence to their morphological characters.
The resolved clades of the combined ITS-rpoC1-trnT-F tree suggest the tropical African, possibly Guineo-Congolian, origin for the whole Sabiceeae as Hekistocarpa, constantly resolved as sister to the clade of Tamridaea, Virectaria and Sabicea s.l., is Lower-Guinean.
The high number of both molecular and morphological autapomorphies of Tamridaea testifies only for a long isolated evolution. The species of Virectaria are distributed over the four phylogeographical regions, Lower- and Upper-Guinean, Guineo-Congolian and Zambezian region, but the species of these regions are not closely related. The resolved clades of Virectaria (Chapter 6.2, Fig. 2) also indicate the floral exchange between these regions. The ETS-ITS-rpoC-trnT-F tree indicates the presence of at least three (V. herbacoursi and V.
multiflora, V. angustifolia, and V. procumbens, V. major and V. belingana) vicariant couples within the Guineo-Congolian and Zambezian regional center of endemism.
The taxonomic revision of Neotropical Sabicea, based on a large bulk of specimens, recognizes 37 species from the previously described 54 species and merges the remaining 17 with other well-defined species of the genus, as no reason was found for their recognition.
Additionally six new species (S. boyacana, S. chiapensis, S. cochabambensis, S. liedeae, S.
noelii, and S. tayloriae; Chapter 6.3, Figs.11, 18, 22, 29, 34, 40) are reported. Finally, this revisionary study provides a comprehensive taxonomic treatment of 43 species, 37 from South America and five from Mesoamerica, with distribution maps and 30 illustrations
(Chapter 6.3). All descriptions are originally generated from DELTA (Dallwitz & al., 1999) using 620 vegetative and reproductive characters. A detailed indented key to all of 43 species is provided. Lectotypes are designated for six species. This study reveals that the highest degree of endemism of the genus in the Neotropics occurs in Brazil, Bolivia, Venezuela, and Colombia with four species each. Mexico harbors three endemic species, Peru two and Jamaica and Surinam one each.
The studies on morphological characters of Neotropical Sabicea prove that the taxonomic utility of most of the characters is limited for inter- and infraspecific delimitations and it is barely possible to define a Neotropical species based on a single character. Types and composition of indumenta, especially of leaves and flowers, types of inflorescences, lengths of calyx tubes, and shape, size and orientation of calyx lobes are the main sources of taxonomically useful characters for the classification of Neotropical Sabicea. Taxonomical utility of habit types, characters of stipules, leaves, and bracts, and position of colleters in calyces, however, is very limited.
Lastly, this study is an excellent base for the completion of the reclassification within the tribe Sabiceeae, especially within the genera Virectaria and Sabicea s.l. in Africa.
4. ZUSAMMENFASSUNG
Die pantropische Tribus Sabiceeae (Ixoroideae s. l., Rubiaceae) ist in der Vergangenheit mehrfach umschrieben worden, wobei sich große Konflikte sowohl bei der Umschreibung als auch bei der Gattungsabgrenzung innerhalb der Tribus ergaben. Die Monophylie der Tribus ist bislang in keiner ihrer Umschreibungen mit Hilfe molekularer Datensätze bestätigt worden. Sabicea, die Typusgattung, die zugleich auch die artenreichste Gattung der Tribus darstellt, und die einzige Gattung der Rubiaceae mit afrikanisch-asiatisch-amerikanischer Disjunktion, ist seit ihrer ersten monographischen Untersuchung durch Wernham (1914), die überwiegend ein typologisches Artkonzept vertritt, nicht mehr revidiert worden. Die zweitgrößte Gattung, Virectaria, wurde dagegen vor einigen Jahren revidiert (Dessein & al., 2001b). Diese Lücken, sowohl in der Kenntnis der Phylogenie als auch des taxonomischen Merkmalsbestandes der Tribus Sabiceeae, haben die vorliegende Studie angeregt. Zunächst wurde die Umschreibung der Tribus Sabiceeae und Virectarieae geklärt, dann die phylogenetischen Zusammenhänge innerhalb der Sabiceeae untersucht. Weiterhin wurde die Monophylie der Gattung Virectaria sowie die Verwandtschaftsverhältnisse zwischen ihren Arten und ihre Biogeographie geklärt. Schließlich wurde eine taxonomische Revision der Neuweltarten der Gattung Sabicea sowie eine Analyse taxonomische wichtiger morphologischer Merkmale in dieser Gruppe vorgenommen.
Die vorliegende Studie zeigt zum ersten Mal, daß weder die Tribus Virectarieae, die derzeit als eine den Sabiceeae nahestehnde Tribus gilt, noch die Subtribus Virectariinae, die vor kurzem für die Gattungen der Virectarieae vorgeschlagen wurde, monophyletisch sind, vielmehr stellt die Tribus Sabiceeae zusammen mit den Virectarieae (oder Virectariinae) eine sehr gut unterstützte Gruppe in den molekularen Analysen von trnT-F (Kapitel 6.1, Abbildung 1) und einer Kombination von ITS und trnT-F dar (Kapitel 6.1, Abbildung 3). Entsprechend wird eine weite Umschreibung der Tribus Sabiceeae (Sabiceeae s.l.) mit acht Gattungen, Ecpoma, Hekistocarpa, Pseudosabicea, Sabicea, Schizostigma, Stipularia, Tamridaea und Virectaria, vorgeschlagen. Außerdem wird die Überführung der Gattungen Pentaloncha und Temnopteryx, die bisher als Mitglieder der Sabiceeae angesehen wurden, in die Unterfamilie Rubioideae unterstützt. Eine morphologische Synapomorphie, die diese Umschreibung der Tribus unterstützt, wurde nicht gefunden, auch keine, die es erlauben würde, Virectarieae oder Virectariinae abzutrennen. Folglich basiert die neue Umschreibung von Sabiceeae ausschließlich auf molekularen Daten.
Es konnte gezeigt werden, daß die Gattungen Ecpoma, Pseudosabicea, Sabicea, Schizostigma und Stipularia, die auch traditionell mit der Tribus Sabiceeae in Verbindung gebracht wurden, eine monophyletische Gruppe bilden, wenngleich auch ihre morphologische Differenzierung keinesfalls eindeutig ist. Daher wurden diese Gattungen unter Sabicea s.l.
zusammengefaßt, womit die neue Tribus Sabiceeae nurmehr ´die vier Gattungen Hekistocarpa, Sabicea s. l., Tamridaea und Virectaria enthält. Die aufgelösten Clades der kombinierten ITS-trnT-F Analyse (Kapitel 6.1, Abbildung 3) lassen darauf schließen, daß die Sabicea-Arten der Neotropis, Madagaskars und São Tomés mit großer Wahrscheinlichkeit jeweils von afrikanischen Vorfahren abstammen. Sie sollten unabhängig voneinander vermittels dreier einzelner Fernausbreitungsereignisse in ihre neuen Areale gelangt sein. Es werden zwei Hypothesen für den Mechanismus der Fernausbreitung diskutiert – 1) durch Wind oder Ozeanströmungen oder 2) durch Vögel. Die stärkste Differenzierung innerhalb von Sabicea hat auf dem afrikanischen Festland stattgefunden. Eine weitere Differenzierung ist nach der Kolonisierung der Neotropen durch die Gattung erfolgt. Das Vorkommen von lediglich einer einzigen Art, Sabicea ceylanica, auf Sri Lanka läßt auf eine ausgebliebene Radiation der Gattung in Asien schließen.
Aus der kombinierten ITS-rpoC1-trnT-F-Analyse (Kapitel 6.2, Abbildung 1) läßt sich ablesen, daß die auf Kamerun und Nigeria beschränkte monotypische Gattung Hekistocarpa nahe mit der im Guinea-Congo-Gebiet verbreiteten Gruppe um Virectaria, der monotypischen, yemenitischen Tamridaea sowie der pantropischen Sabicea s.l. verwandt ist. Während jedoch Hekistocarpa stets als Schwestergattung zu den restlichen drei Gattungen identifiziert wird, wechseln die Positionen der zwei Clades (Der Tamridaea-Virectaria Clade und Sabicea Clade) auf dem Tamridaea-Virectaria-Sabicea Clade. Für keine der Kombinations-möglichkeiten finden sich morphologische Synapomorphien. Der Clade aller untersuchten Virectaria-Aufsammlungen ist im ITS-rpoC1-trnT-F Cladogram statistisch gut abgesichert und unterstützt damit die Monophylie der Gattung Virectaria, für die auch etliche morphologische Synapomorphien bestehen. Das kombinierte ETS-ITS-rpoC1-trnT-F Cladogram (Kapitel 6.2, Abbildung 2) zeigt die engen Beziehungen innerhalb der Gattung und ihren zwei stark unterstützten Gruppen, und es bestätigt die Monophylie der sechs Virectaria-Arten in Übereinstimmung mit deren morphologischen Merkmalen.
Das konstante Verhältnis von Hekistocarpa als Schwester zu Tamridaea, Virectaria und Sabicea s.l im ITS-rpoC1-trnT-F Cladogram läßt auf einen Ursprung der Tribus im tropischen Afrika, möglicherweise in Guinea-Kongo, schließen. Die große Zahl an molekularen und morphologischen Autapomorphien bei Tamridaea weist auf ihre lang andauernde unabhängige Evolution hin. Die Virectaria-Arten sind über die vier Phylogeographische Regionen Unterguinea, Oberguinea und Guinea-Kongo und der Zambesi-Region verbreitet, jedoch innerhalb der einzelnen Regionen nicht nahe miteinander verwandt. Die erhaltenen Clades in Virectaria (Kapitel 6.2, Abbildung 2) deuten auf lebhaften floristischen Austausch zwischen den Regionen Unterguinea, Oberguinea und Guinea-Kongo hin. Die wenigstens drei vikarianten Artenpaare (V. herbacoursi and V. multiflora, V. angustifolia, and V.
procumbens, V. major and V. belingana) deuten auf einen erheblichen genetischen
Austausch besonders innerhalb den Endemismuszentren Guinea-Kongo und der Zambesi-Region hin.
Die Revision der Neotropischen Sabicea-Arten, die auf einer großen Zahl von Herbarbögen beruht, anerkennt 37 der bisher beschriebenen 54 Arten und subsummiert die verbleibenden 17 unter andere, gut definierte Arten der Gattung. Zusätzlich werden sechs neue Arten beschrieben (S. boyacana, S. chiapensis, S. cochabambensis, S. liedeae, S.
noelii und S. tayloriae ; Kapitel 6.3, Abbildung 11, 18, 22, 29, 34, 40). Diese Revision umfaßt eine umfassende taxonomische Beschreibung der 35 südamerikanischen, 4 mittelamerikanischen und 4 süd- und mittelamerikanischen Arten werden hier umfassend neu beschrieben, inkl. Verbreitungskarten und 30 Illustrationen. Alle Beschreibungen wurden ursprünglich aus DELTA (Dallwitz & al., 1999) generiert, wobei die Merkmalsliste 620 vegetative und generative Merkmale umfaßt. Ein dichotomer Schlüssel zu allen 43 Arten wurde erstellt (Kapitel 6.3). Lektotypen werden für sechs Arten ausgewählt. Diese Analyse zeigt, daß der höchste Endemismusgrad in den Neotropen in Brasilien, Bolivien, Venezuela und Kolumbien mit je vier Arten erreicht wird, während Mexiko nur drei, Peru zwei und Jamaika und Surinam jeweils eine endemische Art aufweisen.
Der taxonomische Nutzen der meisten der untersuchten morphologischen Merkmale ist für die inter- und infraspezifische Abgrenzung sehr beschränkt. Es ist fast unmöglich, eine
Der taxonomische Nutzen der meisten der untersuchten morphologischen Merkmale ist für die inter- und infraspezifische Abgrenzung sehr beschränkt. Es ist fast unmöglich, eine