Introduction to the Orders of this Volume

V. B I T T R I C H AND J.W. K A D E R E I T

The present volume of this book series completes – Leaves simple or compound, petiole usually sheath-
the treatment of the Asterids. Asterids are now ing at base; inflorescences or their ultimate units
contained in Vols. VI (Cornales, Ericales, 2004), often umbellate; petals usually shorter; stamen fila-
VII (Lamiales, 2004), VIII (Asterales, 2007), XIV ments inflexed in bud; stylodia 2–many, ovary infe-
(Aquifoliales, Boraginales, Bruniales, Dipsacales, rior; nectary on ovary roof; fruit a schizocarp or
Escalloniales, Garryales, Paracryphiales, Sola- drupaceous 5
nales, Icacinaceae, Metteniusaceae, Vahliaceae, 5. Plants herbaceous, rarely woody; leaves mostly com-
2016) and the present volume, which contains pound, rarely entire, usually membraneous; petals
the orders Apiales and Gentianales (except usually clawed and with an inflexed tip; ovules 2 per
Rubiaceae). The only families of Asterids not locule, one abortive; fruit usually dry and schizocar-
treated in the series are Acanthaceae (Lamiales), pic Apiaceae
Convolvulaceae (Solanales) and Rubiaceae (Gen- – Plants mostly shrubs or small trees; leaves simple to
tianales). compound, usually subcoriaceous to coriaceous;
petals usually broadly inserted, rarely clawed, and
without inflexed tip; ovule 1 per locule; fruit usually
drupaceous, rarely dry schizocarpic 6
CONSPECTUS OF THE FAMILIES OF APIALES
6. Calyx with evident lobes; sepals and petals 5, petal
apex without pointed adaxial thickening, stamens 5,
1. Plants without secretory canals; leaves simple; nec-
carpels 2; fruit with secretory vesicles located imme-
tary absent or present; fruit fleshy, 1-seeded 2
diately adjacent to the endocarp Myodocarpaceae
– Plants with secretory canals throughout; leaves sim-
– Calyx with minute to obscure lobes, often forming a
ple or composed; gynoecial nectary mostly present;
truncate rim; sepals and petals (3–)5(–12), petal apex
fruit fleshy or dry, sometimes schizocarpic, 1- to
with pointed adaxial thickening, stamens 5 (3–
many-seeded 4
numerous), carpels 2–5(–100+); fruit without secre-
2. Petiole not sheathing; petals valvate; nectary absent;
tory vesicles Araliaceae
ovary superior, unilocular Pennantiaceae
– Petiole
sheathing; petals (sub-)imbricate, rarely
induplicate-valvate; nectary present or absent; ovary Seven families (about 522 genera, 6000 spp.) are
inferior, 3-locular at least in upper part 3 currently included: Apiaceae (466 / 3820), Aralia-
3. Leaves distichous or subopposite, blade minutely ceae (40 / 1900), Griseliniaceae (1 / 7), Myodocar-
pellucid-punctate; ovary 3-locular above, 1-locular paceae (2 / 17), Pennantiaceae (1 / 4),
below Griseliniaceae Pittosporaceae (9 / 250) and Torricelliaceae (s.l.
– Leaves spiral, blade not punctate; ovary 3-locular ¼ incl. Aralidiaceae and Melanophyllaceae; 3 /
throughout Torricelliaceae 10). The phylogeny currently accepted is (Pen-
4. Leaves simple, petiole not sheathing at base; nantiaceae + (Torricelliaceae + (Griseliniaceae +
inflorescences not umbellate; petals 4–40 mm long; (Pittosporaceae + (Araliaceae + (Myodocarpa-
stamen filaments straight in bud; style simple, ovary ceae + Apiaceae)))))).
superior; nectary at base of ovary (rarely absent); Few of the families now included in the
fruit a capsule or berry, rarely woody indehiscent Apiales were placed in the order before data
Pittosporaceae from DNA sequencing became available. Undis-
puted were only Apiaceae + Araliaceae (see

# Springer International Publishing AG, part of Springer Nature 2018 1

J.W. Kadereit, V. Bittrich (eds.), Flowering Plants. Eudicots, The Families and Genera of Vascular Plants 15,
https://doi.org/10.1007/978-3-319-93605-5_1
2 V. Bittrich and J.W. Kadereit

below). Diversification and evolution of the order 1994). Ignorance of this evidence by most specia-
is discussed in detail in Stevens (2001 onwards), lists in angiosperm classification suggests that
Kårehed (2003), Chandler and Plunkett (2004) these characters were given low weight. Cronquist
and Nicolas and Plunkett (2014). The current (1981) insisted on the traditional Rosales affinity
phylogenies (e.g. Soltis et al. 2011) show the of Pittosporaceae and did not even mention root
monogeneric Pennantiaceae as sister to the anatomical data in the family descriptions of Pit-
remainder of Apiales. Kårehed (2001), based on tosporaceae, Apiaceae and Araliaceae, and he
DNA sequence data, was the first to point out that cited neither van Tieghem (1884) nor Hegnauer
Pennantia does not belong in Icacinaceae, as (1969). Takhtajan (1980) preferred Saxifragales
believed since the mid-19th century (cf. Miers for placement of Pittosporaceae, and Thorne
1852), but in Apiales. Because of the position of (1983) his superorder Rosiflorae. Only Dahlgren
Pennantia in the phylogeny, recognition of the (1983) relatively early classified Pittosporales
genus as a separate family had to be accepted. The (assessing the position of Tremandracae and
next branch in the Apiales phylogeny is formed Byblidaceae in this order as highly uncertain)
by the small but heterogeneous Torricelliaceae. close to Araliales (Apiaceae and Araliaceae). The
The three genera of this family were often apparently considerable difference in the ovary
included in separate monogeneric families and position, inferior in Apiaceae and Araliaceae, but
only DNA sequence data suggested that they superior in Pittosporaceae, possibly was another
form a clade in the Apiales (Plunkett et al. 1996; reason for the resistance of many authors to
Savolainen et al. 2000; Kårehed 2003). Although accept a close relationship among these families.
Aralidium was often included in Araliaceae in the As Erbar and Leins (2010) pointed out, however,
19th century, the lack of schizogenous secretory in this case the difference is of lesser importance
canals suggested different positions—for exam- than thought by most systematists, as the inter-
ple, inclusion in Cornales (e.g. Thorne 1983). The calary growth in the floral axis resulting in the
other two genera, Melanophylla and Torricellia, inferior ovaries is only a gradual difference. Fur-
were usually included in Cornales or Rosales. The thermore, one surely can make an argument that
monogeneric Griseliniaceae, forming the next the superior ovary of Pittosporaceae is derived.
branch in the Apiales phylogeny, was usually Apiaceae and Araliaceae were early consid-
included in Cornales or even Cornaceae (Hooker ered closely related (e.g. Jussieu 1789; Lindley
1867; Cronquist 1981), although already Endli- 1830). While this close relationship has long
cher (1850) had placed Griselinia in Araliaceae. been accepted due to the obvious similarities
Chase et al. (1993), in the first large angiosperm between the two, their circumscription and
phylogeny based on DNA (rbcL) sequence data, delimitation has proved much less simple. With-
recovered a clade composed of Araliaceae, Apia- out DNA sequence data, phylogenetic relation-
ceae, Griseliniaceae [as Cornaceae p.p., that fam- ships could not be recovered correctly (e.g. Judd
ily was shown to be polyphyletic] and et al. 1994). The two genera of Myodocarpaceae as
Pittosporaceae (see also Olmstead et al. 1993). circumscribed here were originally placed in
Pittosporaceae here is sister to Araliaceae + Apiaceae (Myodocarpus) and Araliaceae (Delar-
(Myodocarpaceae + Apiaceae), a large clade of brea) respectively, and sometimes considered to
Apiales, which is also morphologically well char- link these families, and later were mostly placed
acterized. van Tieghem (e.g. 1884) had already in tribe Myodocarpeae of Araliaceae. The need to
early emphasized that schizogenic resin canals place the two genera in their own family has only
in many parts of the plants and a root anatomy recently been realized based on DNA sequence
with a characteristic arrangement of the canals data (Plunkett and Lowry 2001). Nevertheless, the
and lateral roots suggested a close relationship first attempts to clarify the delimitation of Apia-
among Pittosporaceae, Apiaceae and Araliaceae. ceae and Araliaceae by using DNA sequence data
The root anatomy of Myodocarpaceae apparently still gave ambiguous results (e.g. Plunkett and
has not been investigated. Hegnauer (1969) was Lowry 2001). Especially problematic was the cir-
one of few who endorsed the proposal of van cumscription of subfamily Hydrocotyloideae,
Tieghem and added some supporting evidence, which apparently was polyphyletic (Plunkett
especially chemical data (see also Judd et al. et al. 1997). Based on extensive taxon sampling
 Introduction to the Orders of this Volume 3

and two DNA plastid markers, Nicolas and Plun- petals are mostly free at anthesis, but Erbar and
kett (2009) finally could convincingly show that Leins (2004, 2011) found early sympetaly in Ara-
the subfamily as traditionally circumscribed (e.g. liaceae (incl. Hydrocotyle) and Pittosporaceae,
Drude 1898) is indeed polyphyletic and com- although not (yet) in Apiaceae (only members
posed of several lineages dispersed among the of Saniculoideae and Apioideae studied).
Apiaceae and Araliaceae. Hydrocotyloideae s.str. Stamens have free filaments and anthers open
(only four genera) appeared as sister group to the by longitudinal slits (except in a few Pittospora-
Araliaceae s.str. and today is included in that ceae). Pollen is nearly exclusively tricolporate and
family. Some systematists, like Thorne (e.g. usually more or less spherical. Small flowers, nec-
1983), had complained that the taxonomic world taries or nectar-less but fragrant flowers (in Pen-
kept Apiaceae separate from Araliaceae in spite of nantia) suggest insect pollination for Apiales.
“numerous non-missing links”. Only the new Superior ovaries exist in Pennantiaceae and,
molecular data could clarify details of the rela- apparently derived from the inferior condition, in
tionships between the two families. Pittosporaceae. All other members of the order
In the phylogenies of Winkworth et al. (2008) have inferior ovaries. Free or only shortly connate
and Soltis et al. (2011), the Apiales appear as stylodia are characteristic for the order, with the
sister to the Paracryphiales (only family Paracry- exception of Pittosporaceae, part of the Aralia-
phiaceae) + Dipsacales clade. These orders are ceae and a few Apiaceae. Trans-septal bundles in
part of the subclass Campanulidae. the ovary occur in Torricelliaceae and Griselinia-
Woodiness occurs in all families of Apiales ceae. A nectary is absent in Pennantiaceae, but it
and is certainly plesiomorphic; large trees are is usually present in the other families and of
very rare, however, and the predominantly her- gynoecial origin, as also in most Asterales. At
baceous Apiaceae have by far the largest number anthesis, it is situated on the lower carpel flanks
of species. Plants are evergreen or deciduous. in the superior ovaries of Pittosporaceae and on
Schizogenous canals containing ethereal oils, the ovary roof, typically in an enlarged stylopo-
resin or gums occur in the large majority of spe- dium, in part of the Torricelliaceae (Aralidium
cies, but are restricted to the core Apiales (¼ and Torricellia, absent in Melanophylla), Apia-
Pittosporaceae, Araliaceae, Myodocarpaceae, cae, Araliaceae and Myodocarpaceae. According
Apiaceae) and are absent in the three basal to Erbar and Leins (2010), the different position
families of the order. Vessel elements have scalar- of the nectary in most Apiales families compared
iform or simple perforation plates, helical thick- with Pittosporaceae is related to the intercalary
enings in vessels are sometimes present, and growth in the floral axis which results in the
fibres are septate and non-septate. Nodes are inferior ovaries in these families. The nectary is
normally 3-lacunar to multilacunar. Phyllotaxy always formed, however, at the dorsal base of the
is usually spiral, the leaves are simple to com- carpels. Families of the basal grade of Apiales
pound and their margins entire or not. Stomata (Pennantiaceae, Torricelliaceae, Griseliniaceae)
are paracytic in Pennantiaceae as well as in the apparently have a 3-carpellate gynoecium, but
core Apiales, but anisocytic, anomocytic, diacytic only one carpel is fertile. Pennantiaceae have
and encyclocytic types are also reported for the pseudomonomerous 1-locular ovaries with a 3-
order. The petiole is nearly always exstipulate and lobed stigma. The bicarpellate condition is
very often sheathing at the base (but not in the derived and is found in most core Apiales, includ-
basal Pennantiaceae and some Pittosporaceae). ing nearly all Apiaceae, and all carpels are fertile.
The inflorescences are mostly described as In Pittosporaceae the ovary is 2(3–5)-carpellate,
paniculate, more rarely cymose. In the Araliaceae the placentation axile or parietal, and there are
/ Myodocarpaceae / Apiaceae clade at least the several ovules. Other core Apiales have one fertile
ultimate units are mostly umbellate. The pedicel ovule per carpel, and the ovule is unitegmic and
is often articulated, the flowers are unisexual or tenuinucellate or more rarely crassinucellate.
bisexual, typically pentamerous with the excep- One-seeded drupes, as in the Pennantiaceae,
tion of the ovary. Dioecy occurs at least in some are common in the order and are probably the
species of most families of the Apiales. The calyx plesiomorphic condition, but schizocarpic fruits
often has more or less strongly reduced lobes; the with dry mericarps on a carpophore are typical
4 V. Bittrich and J.W. Kadereit

for many Apiaceae, Myodocarpus and a few Ara- tralia as the likely centre of origin. Many
liaceae. The drupes suggest endozoochory but palaeoendemics of the core Apiales today occur
reports of this exist only for Pennantiaceae and in Australia and especially New Caledonia. This
some Araliaceae. The dry mericarps are dispersed island apparently offered refugia to “relictual
either by autochory or, when winged, by wind lineages” because, unlike Australia, it suffered
and/or water, when with barbs or spines by epi- much less aridification and was much later colo-
zoochory. Most Pittosporaceae have many- nized by humans. However, it was submerged at
seeded capsules, and the sticky fluid around the least partly during the Palaeogene. The early
seeds of Pittosporum (produced by multicellular diversification of Apiales was probably due to
epidermal hairs in the septal region (Erbar and vicariance events during the break-up of Gond-
Leins 1995)) suggests bird dispersal which may wana. Younger lineages more probably developed
explain the wide distribution of the genus in the after long-distance dispersal to Madagascar, Asia
Indo-Pacific region. Seeds contain copious endo- and the Americas (Pittosporum and Araliaceae).
sperm, apparently mostly oily, and a small Apiaceae probably also originated in Australia
straight embryo. and migrated to South America and South Africa
There are little phytochemical data for several before the complete Gondwana break-up, and
families, making meaningful comparisons diffi- later to north temperate regions.
cult. Fruit or seed oils containing petroselinic
acid were found in Griselinia, Araliaceae and
Apiaceae, and may occur also in Myodocarpaceae
CONSPECTUS OF THE FAMILIES OF GENTIANALES1
(no data). They are apparently lacking in Pittos-
poraceae. As Pennantiaceae and Torricelliaceae
1. Ovary inferior (rarely semi-inferior and very rarely
have not yet been investigated, the distribution
superior); plants usually with interpetiolar stipules
and phylogenetic significance of this fatty acid in
(sometimes deciduous); internal phloem absent
the Apiales is unclear. Polyacetylenes are known
Rubiaceae
from Torricellia, Pittosporaceae, Araliaceae,
– Ovary superior, rarely semi-inferior; interpetiolar sti-
Myodocarpaceae and Apiaceae. Cyanogenic com-
pules usually absent (often with interpetiolar ridges);
pounds are very rare in the order. The lack of
internal phloem present 2
proanthocyanidins and ellagic acid (or their
2. Latex in non-articulated laticifers present in vegeta-
restriction to the seed coat) is also typical for
tive parts, usually white, less often translucent or
Apiales. Many Pittosporaceae, Apiaceae and Ara-
yellowish or reddish; ovary mostly apocarpous, less
liaceae contain triterpenoid saponins and flavo-
often (congenitally or postgenitally) syncarpous
noids (especially the flavonols kaempferol and
Apocynaceae
quercetin). The occurrence of the iridoid gluco-
– Latex absent in vegetative parts; ovary syncarpous,
side griselinoside in Aralidium, Torricellia and
less often partially apocarpous (then Australian her-
Griselinia supports their close relationship, but
baceous species) 3
data for Pennantiaceae are needed to conclude
3. Style apically divided into 4 long stigmatic lobes,
whether iridoids are plesiomorphic in the order.
rarely with two free styles (then a tree with alternate
A basic chromosome number of x ¼ 6 was sug-
leaves and fruit a 1-seeded samara) Gelsemiaceae
gested for the order by Yi et al. (2004). The Apia-
– Style single, rarely two free styles (then leaves not
ceae are extremely variable in their chromosome
alternate and fruit not a 1-seeded samara) 4
numbers (see Plunkett et al., this volume).
4. Corolla lobes mostly contorted in bud; rarely valvate
The historical biogeography of the Apiales
or imbricate (then plants either herbaceous and from
clade has recently been analyzed in detail by
N temperate or palaeotropical regions, or shrubby
Nicolas and Plunkett (2014), who also estimated
with pitcher-shaped leaves, or tropical trees with
the divergence times for all major clades of the
very long and narrow corolla tubes); placentation
order. They concluded that the order originated
usually parietal, rarely axile Gentianaceae
in Australasia in the Early Cretaceous, with Aus-

1
Key to families by J.W. Kadereit and L. Struwe.
 Introduction to the Orders of this Volume 5

– Corolla lobes imbricate, valvate or exduplicate-val- ences, see account of Loganiaceae in this
vate in bud; placentation usually axile Loganiaceae volume).
As understood here, the well-supported Gentia- Vegetatively, the order almost always has
nales, a name first used by Lindley (1833) to opposite leaves with interpetiolar lines or inter-
rename Bartling’s (1830) ‘Contortae’, comprise petiolar stipules (interpetiolar stipules are almost
Rubiaceae (incl. Dialypetalanthaceae and Theli- always present in Rubiaceae but far less common
gonaceae; 611 genera / 13150 species fide Stevens in the other four families), colleters, defined as
2001 onwards; not treated in this volume), Apoc- multicellular secretory structures, are common
and most often found in the leaf axils and on
ynaceae (incl. Asclepiadaceae; 378 / ca. 5350),
the sepals, and all families except Rubiaceae
Gelsemiaceae (3 / 13), Gentianaceae (102 / ca.
1750) and Loganiaceae (16 / ca. 460). have bicollateral vascular bundles (internal
Following the account by Backlund et al. phloem). Habit is very diverse in the order, rang-
(2000), this circumscription of the order, apart ing from annual or ephemeral herbs to large trees
from details, was essentially established by and lianas, and including several mycohetero-
Downie and Palmer (1992) and Olmstead et al. trophic and sometimes achlorophyllous genera
(1993). Whereas close relationships among Apoc- in Gentianaceae. With very few exceptions flow-
ers are 4- or 5-merous, tetracyclic and sympeta-
ynaceae (incl. Asclepiadaceae), Gentianaceae and
lous with epipetalous stamens on the petal tube
Loganiaceae (at that time incl. part of Gelsemia-
ceae as well as various elements since segregated; (Endress 2011) and a bicarpellate apo- (and then
see below) had been accepted for a long time often postgenitally fused (Endress et al. 1983)) or
(Bentham and Hooker 1862–1883), inclusion of syncarpous ovary which is superior or inferior
Rubiaceae was first suggested by Wagenitz (Rubiaceae). The corolla is often but by no
(1959). Two families placed near (or sometimes means always contorted in bud. Ovules are tenui-
in) Gentianales even in the more recent past nucellar or sometimes reduced tenuinucellar
(Dahlgren 1980; Takhtajan 1987), Menyanthaceae (Endress 2011).
and Oleaceae, rather belong to Asterales and Route I iridoids, seco-iridoids and indole
Lamiales respectively (Downie and Palmer 1992; alkaloids, all part of one biosynthetic pathway
Olmstead et al. 1992). (Jensen et al. 2002), are common in the order.
Of all families in the order (apart from inclu- The intensely bitter gentiopicrin of, amongst
sion of Asclepiadaceae in Apocynaceae; Judd others, Gentiana lutea (Gentianaceae) represents
et al. 1994; Endress et al. 1996; for historical an example for seco-iridoids, and the well-known
account and further references, see family strychnine (Strychnos nux-vomica / Loganiaceae)
account in this volume), most changes took and chinine (Cinchona spp. / Rubiaceae) are
place in Loganiaceae in the highly para- and examples for indole alkaloids. Cardenolides and
polyphyletic circumscription of Leeuwenberg steroid alkaloids are common in Apocynaceae,
and Leenhouts (1980). These resulted not only and xanthones are common in Gentianaceae.
in recognition (Struwe et al. 1994) and later recir- Whereas Gelsemiaceae and Loganiaceae are
cumscription (Struwe et al. 2014) of Gelsemiaceae exclusively pantropical in distribution, Apocyna-
(for details, see account of Gelsemiaceae in this ceae and Rubiaceae are predominantly pantropi-
volume) as part of the order, but also in the cal but have reached temperate regions with some
exclusion of several genera (Buddleja – Scrophu- genera or suprageneric groups. In Rubiaceae, this
lariaceae / Lamiales; Nuxia, Stilbe (Retzia) – Stil- is mainly tribe Rubieae (Bremer and Eriksson
baceae / Lamiales; Polypremum – 2009). In Gentianaceae, the majority of tribes
Tetrachondraceae / Lamiales; Plocosperma – Plo- are tropical in distribution but its largest tribe
cospermataceae / Lamiales; Peltanthera, Sanango Gentianeae, with more than half of the species
– Gesneriaceae / Lamiales; Desfontainia – Colu- diversity of the family and including Gentiana
melliaceae / Bruniales; Anthocleista, Fagraea, as the largest genus of the family, is primarily
Potalia – Gentianaceae / Gentianales; generic, temperate-alpine (Struwe et al. 2002). Consider-
familial and ordinal assignment according to Ste- ing this distribution of the order, an origin in
vens 2001 onwards; for details and further refer- tropical areas appears very likely. Several esti-
mates of the stem age of the order converge on
6 V. Bittrich and J.W. Kadereit

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