|Morphological support for Ericoideae (as
here delimited, i.e., including the traditional Rhododendroideae, see(Fig.
the erect to more or less horizontal position of the flowers (char.
loss of stamen appendages (char. #59), and septicidal capsules (char.
All these characters, however, show homoplasy (see Figures 14, 15, and
16). The last is probably most useful, but it is important to note that
loculicidal capsules have evolved in Erica, a very species-rich group.
Viscin threads (char. #69; Fig.
17) are restricted to this group (among
extant Ericaceae) and may represent another synapomorphy for these plants.
Within Ericoideae, five major clades can be recognized: Bejarieae, Phyllodoceae, Ericeae, Empetreae, and Rhodoreae, although their interrelationships are unclear (Fig. 7). Ericeae, Empetreae, and Rhodoreae each have strong bootstrap support. Bejarieae and Phyllodoceae lack support above 50% but these clades are found in all of the most parsimonious trees obtained in both the combined molecular and molecular plus morphological data analyses. All of the tribes in Ericoideae can be recognized by means of morphological synapomorphies.
|Ericoideae Link, Handbuch 1: 602. 1829 (as Ericeae). – Type
genus: Erica L.
Empetroideae Nutt. ex Sweet, Hort. Brit.: 491. 1826 (as
Ledoideae Alef., Linnaea 28: 3, 7. 1856. (as Ledeae).
|Shrubs to trees, evergreen or deciduous, with alternate, decussate, 3- or 4 (6)-whorled or pseudo-whorled, ericoid or non-ericoid leaves, revolute or convolute in bud, with margin entire to serrulate or serrulate-ciliate. Leaf epidermal cells not lignified. Indumentum of unbranched, variously branched, peltate, or scale-like, glandular to non-glandular hairs, and sometimes papillae. Inflorescence terminal or axillary, racemose, spicate, corymbose, umbellate, fasciculate, capitate, or of solitary flowers; bracts and bracteoles extremely various; flower articulated or continuous with pedicel. Flowers usually 4—7 (-9)-merous, actinomorphic or slightly zygomorphic, sometimes variably reduced and wind pollinated, with a distinct calyx and corolla or perianth parts ± undifferentiated, pendulous to erectly held. Calyx lobes (or sepals) usually 1—7, or lacking, variable in size, persistent or deciduous; corolla choripetalous or more commonly sympetalous, and variously shaped, persistent or deciduous, with the usually 1—7 lobes small to large; stamens 2—15, included or sometimes exserted, the filaments straight to curved or S-shaped, distinct or connate, unicellular-pubescent or glabrous (and smooth); anthers tetrasporangiate, inverting early in development, variably roughened or smooth, with or without a pair of dorsal appendages (spurs), lacking disintegration tissue, usually lacking a fibrous endothecium, dehiscing by terminal pores or longitudinal slits. Pollen in tetrads, with viscin threads present or absent. Ovary 2—14-locular, with axile placentation, superior; style gradually tapered or impressed; stigma truncate, capitate, peltate, cup-shaped, funnel-shaped, or strongly lobed, considerably enlarged in wind pollinated species. Fruit a septicidal to loculicidal capsule, indehiscent pod, or drupe; seeds with variable testa cells; embryo with 2 cotyledons.|
|Bejarieae may be diagnosed by their separate petals (char. #44) a feature they share with a few other Ericaceae (see Fig. 18). In fact, this character may be a synapomorphy of Bejaria, Ledothamnus, and Bryanthus, but the placement of Bejaria is not, at present, strongly supported. Ledothamnus and Bryanthus also share ericoid leaves (char. #13). Possible additional synapomorphies for Ledothamnus and Bryanthus are the presence of adaxial calyx stomata (char. #42), and a style articulated with the ovary (char. #73). Finally, Ledothamnus and Bryanthus differ from Bejaria in the lack of an endothecium. The Bejarieae may be sister to Phyllodoceae (Fig. 7) although this relationship is not supported in some most parsimonious trees; both clades are characterized by homogeneous pith (char. #8), which may be synapomorphic.|
|Bejarieae Copeland, Am. Midl. Nat., 30: 547, 1943. – Type
genus: Bejaria Mutis ex L.
Low shrubs, evergreen, with alternate or 3-4 whorled or decussate ericoid to flat leaves, revolute in bud. Leaf epidermal cells not lignified. Indumentum of glandular and elongate, or non-glandular hairs. Inflorescence terminal or axillary, racemose to paniculate, or a solitary flower; bracts present, bracteoles paired, ± basal to just below calyx; calyx articulated or continuous with pedicel. Flowers 4—7(-9)-merous, actinomorphic. Calyx lobes variable in size, persistent or withering-persistent; corolla ± choripetalous, rotate, campanulate, salverform, fusiform or infundibular; stamens (5-)-6-14(-18), the filaments straight, smooth pubescent; anthers smooth or roughened, lacking appendages, dehiscing by short to elongate slits. Pollen with viscin threads. Ovary 4—7-locular, with axile placentation, superior; style articulated with the ovary; stigma truncate to capitate. Fruit a septicidal capsule, warty in Ledothamnus, seeds with ± isodiametric to elongate testa cells; embryo with 2 cotyledons.
|Ericeae may be supported by a gradually tapering style (char. #73; Fig. 19). However, this character is quite homoplasious. A persistent corolla (char. #48; Fig. 20) is a synapomorphy for Calluna plus remaining Ericeae, but this character is lacking in Daboecia. As pointed out by Stevens (1971), Daboecia is rather similar to Erica in its anatomy, having flanges of lignified tissue in the petiole; it also has small revolute leaves, which are nearly ericoid in form. Some South African species of Erica are wind-pollinated and have dramatically expanded cup-shaped or funnel-shaped stigmas.|
|Ericeae DC. ex Duby, Bot. Gall. 1: 316.
1829 (as Ericaceae). – Type genus: Erica L.
Calluneae Klotzsch, Monatsber. Königl. Preuss. Akad. Wiss.
Berlin 1857: 3. 1857.
Daboecieae Cox, Am. Midl. Nat., 39: 238. 1948.
Eleutherostemoneae Klotzsch, Linnaea 12: 217. 1838 (as
Eleutherostemoninae Meisn., Pl. Vasc. Gen.: Tab. Diagn.
244. 1839 (as Eleutherostemones).
Ericinae D. Don, New Philos. J. Edinburgh 17: 152. 1834 (as
Salaxideae Drude in Engl. & Prantl, Nat. Pflanzenfam. IV,
1: 32. 1889.
Salaxidinae Engl., Gen. Pl.: 751. 1839 (as Salaxideae)
Shrubs to trees, evergreen, with 3- or 4(6)-whorled, rarely decussate or alternate, ericoid leaves, revolute in bud. Leaf epidermal cells not lignified. Indumentum of unbranched or branched, glandular to non-glandular hairs. Inflorescence racemose to umbellate, at end of branch; bract always present, on the main axis or partially recaulescent to fully recaulescent forming the abaxial lobe of calyx; bracteoles lacking, solitary, or paired, usually fully recaulescent as the lateral lobes of calyx, rarely more than two. Flowers usually 4-merous, actinomorphic. Calyx lobes 1—4(-5), or lacking, variable in size, persistent; corolla sympetalous, urceolate, cylindric, or campanulate, the lobes ± small, usually persistent; stamens (3-)8(-10), sometimes exserted, the filaments straight to S-shaped, distinct or connate, unicellular-pubescent or smooth; anthers variably roughened, with or without a pair of dorsal appendages, dehiscing by terminal pores. Pollen without viscin threads. Ovary (1-)4(-8)-locular, with axile placentation, superior; style gradually tapered or impressed; stigma truncate, capitate, peltate, cup-shaped, funnel-shaped, or strongly 4-lobed, considerably enlarged in wind pollinated species. Fruit a loculicidal capsule, indehiscent pod, or drupe; seeds with variable testa cells; embryo with 2 cotyledons.
|The tribe comprises three genera, Ceratiola,
Corema, and Empetrum. Samuelsson (1913) was the first to show that the
Empetreae were closely related to the Ericaceae, and later Anderberg (1993),
Judd & Kron (1993), and Kron & Chase (1993) demonstrated them to
be nested within the Ericaceae. Prior to Samuelsson’s (1913) investigation
the relationships of empetrids to other plants were unclear with various
proposed systematic positions, e.g., in the orders Euphorbiales (Don, 1827),
Sapindales (Pax, 1891) or Celastrales (Hutchinson, 1969). A position as
a section of Conifers was put forward early in the 19th century (Nuttall,
1818). In recent years, most authors (e. g., Cronquist, 1981, Takhtajan
1997) have placed empetrids close to the Ericaceae, albeit as a separate
Empetreae are easily diagnosed because this clade has numerous distinctive apomorphic characters, most relating to a shift from insect to wind pollination. Unlike most Ericaceae, Empetreae exhibit a high degree of dioecy (found elsewhere in Ericaceae only in Epigaea and possibly some Gaultherieae). Unique (or nearly unique) synapomorphies of Empetreae include imperfect flowers (char. #32, evolving independently in Epigaea), flowers with persistent tepals (chars. #39, 48; although persistent corollas are found in most Ericeae), stigma flabellate to pinnatifid (char. #70), and drupaceous fruits (char. #77, 81, occurring elsewhere only in Arbutoideae, some Styphelioideae, and some Vaccinioideae). Additional, more homoplasious synapomorphies of Empetreae are their lack of multicellular hairs on the leaves (char. #21), flowers with separate perianth parts (char. #44), stamens less than two times the number of petals (char. #51; see Fig. 21), and indehiscent (fleshy) fruits (char #78). In many (but not all) of the most parsimonious trees resulting from the combined morphology, matK, and rbcL analysis, the Empetreae and Ericeae form a clade, which is supported by the absence of bud scales (char. #9, also in some Phyllodoceae, Diplarche, Ledothamnus, Cassiope, and Harrimanella) and smooth filaments (char. #55, also quite homoplasious). In addition, the presence of 4-(or 2-) merous flowers may be synapomorphic, but this feature is also homoplasious. Both Empetreae and Ericeae have ericoid leaves (char. #13). However, it is noteworthy that the occurrence of gossypetin (char. #87) links Empetreae with Rhodoreae.
Although the data strongly indicate that Empetreae are derived from within Ericoideae, the exact relationships to the other tribes are not fully understood. In the analysis of morphological data set (Fig. 3) Empetreae are placed in the same clade as Erica and Calluna but the support for this is very low. The matK data (Fig. 4) indicate a position for the Empetreae as sister to the Rhodoreae, but again with low support. In the combined analysis of morphological and molecular data sets, the position of Empetreae remains unresolved in relation to the Bejarieae, Ericeae, Rhodoreae and Phyllodoceae. Relationships among the genera and species of Empetreae have been studied by Anderberg (1994b).
|Empetreae D. Don, Edinburgh New Phil.
J. 1827: 59. 1827. – Type genus: Empetrum L.
Coremateae Pax in Engl. & Prantl, Nat. Pflanzenfam. III, 5:
Shrubs, or shrublets, sometimes mat-forming, evergreen with alternate or almost verticillate, ericoid leaves, revolute in bud; leaf epidermal cells not lignified. Inflorescence axillary with solitary flowers, few-flowered clusters, or in terminal heads; bracts and bracteoles various; perianth not articulated with the pedicel. Flowers actinomorphic, reduced, choripetalous, wind-pollinated, unisexual or bisexual. Sepals and petals three to six, inconspicuous, more or less undifferentiated. Stamens 2 or 3, exserted, the filaments straight and smooth, anthers ± smooth, lacking appendages, without fibrous endothecium, dehiscing by longitudinal slits. Pollen without viscin threads. Ovary 2 to many locular, with axile placentation, superior, style short, impressed, stigma lobes deeply divided. Fruit a dry or fleshy drupe with two to many pyrenes; seeds with ± isodiametric testa cells; embryo with 2 cotyledons.
Morphological synapomorphies supporting the Rhodoreae include the
flowers on shoots of the previous season (char. #30),
ovoid to cylindric fruits (char. #83), and the presence of gossypetin (char. #87).
Rhodoreae have zygomorphic flowers with spots or a blotch
(chars. #33, 47), and it is probably significant
that these features are both found in Therorhodion, which is the sister
taxon to the rest of the
clade. It is probable that zygomorphic corollas evolved only once (in
Rhodoreae DC. ex Duby, Bot. Gall. 1: 318. 1828 (as Rhodoraceae). - Type
genus Rhodora L. (= Rhododendron L.)
Shrubs or small trees, evergreen or deciduous, with alternate,
non-ericoid, entire to serrulate-ciliate leaves, convolute or revolute
in bud. Leaf epidermal cells not lignified. Indumentum very variable,
sometimes glandular, peltate, or highly branched. Inflorescence
terminal or rarely axillary, usually corymbose or umbellate;
bracts present, usually as perulae (except herorhodion where bracts
are green), bracteoles paired, usually ± basal; calyx articulated
with pedicel or not. Flowers usually 4- or 5-merous, slightly zygomorphic,
but occasionally secondarily actinomorphic. Calyx lobes variably
developed, persistent or deciduous; corolla usually sympetalous,
variously shaped, often with spots or blotches, the lobes usually
moderate to large; stamens 5-15, included or exserted, the filaments
straight to curved, unicellular-pubescent or smooth; anthers smooth,
lacking spurs, dehiscing by terminal pores to elongate slits. Pollen
|The Phyllodoceae clade is not strongly
supported by the data (Figs. 4, 5, 6, 7, 8).
The molecular analyses indicate two strongly supported clades: Kalmia s.l.
(also including Leiophyllum and Loiseleuria) and a Phyllodoce clade (also
including Epigaea, Kalmiopsis, and Rhodothamnus). In the rbcL analysis,
these two clades are sister, but without parsimony jackknife support. The
matK data failed to resolve the Kalmia clade and the Phyllodoce clades
as sister. In both of the individual analyses Elliottia is unresolved with
respect to the remaining Ericoideae. But in the combined molecular analysis,
Elliottia is sister to the Kalmia + Phyllodoce clade. This relationship
is also indicated in the combined morphology and molecular tree (Fig.
7) but without bootstrap support. With the exception of Elliottia and
Epigaea, the taxa that fall within the Phyllodoceae clade in this study
have traditionally been considered closely related (e.g., Stevens, 1971).
Further studies of the relationships of the Kalmia, Phyllodoce, and especially
the Elliottia clades are in progress.
Phyllodoceae (as here defined) are characterized by their articulated pedicels (char. #37, but this character also occurs in Bryanthus, and may, therefore, be a synapomorphy for a Phyllodoceae + Bejarieae clade) and lack of abaxial calyx stomata (char. #43, but such stomata are present in Elliottia and Leiophyllum). The monophyly of this group, like that of the Bejarieae, is thus not well supported by morphology. Kalmiopsis and Phyllodoceae are linked by their distinctive multicellular hairs with biseriate stalks (chars. #23, 26) while Leiophyllum, Loiseleuria, and Kalmia are possibly linked by the presence of an exothecium (char. #67). The monophyly of a clade comprising Leiophyllum, Loiseleuria, and Kalmia (i.e., Kalmia s.l.) also has been strongly supported in a detailed phylogenetic analysis of this group (see Kron & King, 1996).
Phyllodoceae Drude, Engl. & Prantl,
Nat. Pflanzenfam. 4, 1: 31, 38. 1889. – Type genus: Phyllodoce
|Shrubs, evergreen, with alternate and spiral, decussate, or whorled, ericoid or non-ericoid leaves, entire to serrulate, convolute or revolute in bud. Leaf epidermal cells not lignified. Indumentum of glandular hairs and elongate non-glandular hairs, and sometimes papillae. Inflorescence terminal, rarely axillary, spicate, racemose, or corymbose, sometimes reduced; bracts, and paired ± basal, bracteoles usually present; calyx articulated with pedicel. Flowers 4—6-merous, actinomorphic. Calyx lobes variable in size, withering persistent or persistent; corolla sympetalous or choripetalous, rotate to urceolate, campanulate, the lobes small to large; stamens 5—10, included or exserted, the filaments straight to curved, unicellular-pubescent or smooth; anthers smooth or roughened, lacking appendages, dehiscing by slits or terminal pores. Pollen usually with viscin threads. Ovary 2—6-locular, with axile placentation; style impressed or not; stigma truncate, sometimes slightly expanded. Fruit a septicidal capsule, sometimes partly loculicidal as well; seeds with testa cells ± isodiametric to elongated; embryo with 2 cotyledons.|