An update of the Angiosperm Phylogeny Group classification for the orders and families of flowering

17 Pages·2009·0.17 MB·English

Botanical Journal of the Linnean Society, 2009, 161, 105–121. With 1 figure
An update of the Angiosperm Phylogeny Group
classification for the orders and families of flowering
plants: APG III
boj_996105..121
THE ANGIOSPERM PHYLOGENY GROUP*1
1Recommended citation: APG III (2009). This paper was compiled by Birgitta Bremer, Kåre Bremer,
Mark W. Chase, Michael F. Fay, James L. Reveal, Douglas E. Soltis, Pamela S. Soltis and Peter F.
Stevens, who were equally responsible and listed here in alphabetical order only, with contributions
from Arne A. Anderberg, Michael J. Moore, Richard G. Olmstead, Paula J. Rudall, Kenneth J.
Sytsma, David C. Tank, Kenneth Wurdack, Jenny Q.-Y. Xiang and Sue Zmarzty (in alphabetical
order). Addresses: B. Bremer, The Bergius Foundation at the Royal Swedish Academy of Sciences, PO
Box 50017, SE-104 05 Stockholm, Sweden; K. Bremer, Vice Chancellor, Stockholm University, SE-106
91 Stockholm, Sweden; M. W. Chase, M. F. Fay, Jodrell Laboratory, Royal Botanic Gardens, Kew,
Richmond, Surrey, TW9 3DS, UK; J. L. Reveal, L.H. Bailey Hortorium, Department of Plant Biology,
412 Mann Building, Cornell University, Ithaca, NY 14853-4301, USA; D. E. Soltis, Department of
Biology, University of Florida, Gainesville, Florida 32611–8525, USA; P. S. Soltis, Florida Museum of
Natural History, University of Florida, Gainesville, Florida, 32611–7800, USA; and P. F. Stevens,
Department of Biology, University of Missouri-St. Louis and Missouri Botanical Garden, PO Box 299,
St. Louis, Missouri 63166–0299, USA
Received12August2009;acceptedforpublication18August2009
A revised and updated classification for the families of flowering plants is provided. Many recent studies have
yielded increasingly detailed evidence for the positions of formerly unplaced families, resulting in a number of
newlyadoptedorders,includingAmborellales,Berberidopsidales,Bruniales,Buxales,Chloranthales,Escalloniales,
Huerteales, Nymphaeales, Paracryphiales, Petrosaviales, Picramniales, Trochodendrales, Vitales and Zygophylla-
les.Anumberofpreviouslyunplacedgeneraandfamiliesareincludedhereinorders,greatlyreducingthenumber
of unplaced taxa; these include Hydatellaceae (Nymphaeales), Haptanthaceae (Buxales), Peridiscaceae
(Saxifragales), Huaceae (Oxalidales), Centroplacaceae and Rafflesiaceae (both Malpighiales),Aphloiaceae, Geisso-
lomataceae and Strasburgeriaceae (all Crossosomatales), Picramniaceae (Picramniales), Dipentodontaceae
and Gerrardinaceae (both Huerteales), Cytinaceae (Malvales), Balanophoraceae (Santalales), Mitrastemonaceae
(Ericales) and Boraginaceae (now at least known to be a member of lamiid clade). Newly segregated families
for genera previously understood to be in other APG-recognized families include Petermanniaceae (Liliales),
Calophyllaceae (Malpighiales), Capparaceae and Cleomaceae (both Brassicales), Schoepfiaceae (Santalales),
Anacampserotaceae, Limeaceae, Lophiocarpaceae, Montiaceae and Talinaceae (all Caryophyllales) and Linder-
niaceae and Thomandersiaceae (both Lamiales). Use of bracketed families is abandoned because of its unpopu-
larity, and in most cases the broader circumscriptions are retained; these includeAmaryllidaceae,Asparagaceace
and Xanthorrheaceae (all Asparagales), Passifloraceae (Malpighiales), Primulaceae (Ericales) and several other
smaller families. Separate papers in this same volume deal with a new linear order forAPG, subfamilial names
thatcanbeusedformoreaccuratecommunicationinAmaryllidaceaes.l.,Asparagaceaces.l.andXanthorrheaceae
s.l.(allAsparagales)andaformalsupraordinalclassificationforthefloweringplants. ©2009TheLinneanSociety
of London, Botanical Journal of the Linnean Society, 2009, 161, 105–121.
ADDITIONAL KEYWORDS: angiosperm classification – phylogenetic classification – DNA phylogenetics –
classification system – APG system.
*Corresponding author: Mark W. Chase. E-mail: [email protected]
© 2009 The Linnean Society of London, Botanical Journal of the Linnean Society, 2009, 161, 105–121 105
106 THE ANGIOSPERM PHYLOGENY GROUP
INTRODUCTION along APG lines. They have all agreed to adopt
APG III as their standard and the linear order of
Since the previousAPG classification (APG II, 2003),
Haston etal. (2009). In general, the broader cir-
a great deal more information about flowering plant
cumscriptionshavebeenfavouredandareadopted
relationships has emerged, and a more refined and
here.
better-resolvedclassificationisnowpossible.Ifawell-
2. Papers over the last few years have clarified the
supported hypothesis of monophyly is a necessary
positions of isolated families including Cerato-
prerequisite for a group to be named, it is not suffi-
phyllaceae, Chloranthaceae and Picramniaceae
cient. Not all clades need be named and, indeed, it
(Jansen etal., 2007; Moore etal., 2007; Wang
would barely be practicable to do this, so to decide
etal., 2009), and this has necessitated addition of
whichcladesshouldbenamed,additionalcriteriacan
orders not previously recognized by APG.
be invoked. Backlund & Bremer (1998) provided a
3. A few genera/families, members of which had
usefuldiscussionontheprinciplesofrank-basedphy-
either not been sequenced before or for which
logenetic classification that is applicable at all levels
chimaeric sequences were produced, were wrongly
apartfromspeciesandimmediatelyabove(seeAlbach
placed. Thus, families like Guamatelaceae have
etal., 2004; Entwisle & Weston, 2005; Pfeil & Crisp,
been added; Guamatela used to be placed in
2005, etc., for examples). We follow these principles
Rosaceae, but molecular data places it in
here. Backlund and Bremer’s main principle is that
Crossosomatales (Oh & Potter, 2006). Hydatel-
taxa that are recognized formally should be mono-
laceae have been moved from Poales to Nymphae-
phyletic. However, this does not indicate which par-
ales (Saarela etal., 2007).
ticularcladesshouldbenamedasfamilies,ordersetc.
4. Thereareafewcaseswherethegeneralpatternof
It is helpful if (1) taxa formally recognized are
relationships has not changed much sinceAPG II,
easily recognizable, (2) groups that are well estab-
but our appreciation of the pattern of variation
lished in the literature are preserved, (3) the size of
has. For example, this helps justify inclusion of
groups is taken into account (particularly small ones,
Ixerbaceae in Strasburgeriaceae.
which should be combined with others whenever pos-
5. Finally,afewfamilycircumscriptionssuggestedby
sible) and (4) nomenclatural changes are minimized
APG II did not reflect general usage, so we have
(Backlund & Bremer, 1998). Thus, on the one hand,
modified these, an example being the broadly
numerous small groups have little to recommend
circumscribed Brassicaceae, which are here split
them, as individually they summarize only a small
into three families.
amount of information and tend to clog the memory,
whereas groups that are too large may have few
In general, we have tried not to change the status
obvious shared traits that can be used to recognize
of families if they have long been recognized, unless
them.Asparagales and Lamiales in particular have a
there are other good reasons for combining them.
number of problems in this regard and include fami-
However, we have taken the opportunity to combine
lies that are still in a state of flux in this respect.
mono- or oligogeneric families. Most of the family-
Changes are being made to the classification
level changes mentioned below have resulted in the
adopted by APG II for several reasons, but bearing
families now recognized being relatively well charac-
the Backlund and Bremer guidelines in mind.
terized. However, we realize that it is almost impos-
1. In the earlier versions of the Angiosperm Phylog- sible to achieve universal agreement for change – of
eny Group classification, alternative circumscrip- any sort. Note that we do not see theAPG classifica-
tions were permitted for some families. However, tion as continuing to mutate for the indefinite future.
this seems unnecessary and more likely to cause Given the amount of phylogenetic work that has
confusion than clarity. Here we indicate one of the taken place in the last five years, the changes pro-
alternatives, a choice based in part on the circum- posed here are modest. We hope the classification
scriptions adopted by textbooks (e.g. Judd etal., below will be found to be reasonable and, hence, will
2007), dictionaries (e.g. Mabberley, 2008) and the not need much further change, although we do note
general literature. Note that, in preparation for those few areas where there is particular phylo-
the third edition of The Plant Book, Mabberley genetic uncertainty that may necessitate further
(2008: xi, 927, 929) consulted widely among tax- revision of familial or ordinal limits. For further dis-
onomists about which alternative they preferred, cussion on the variation in the groups discussed,
and, more recently, the issue of these alternative potential apomorphies, etc., see the literature cited
circumscriptions was discussed by researchers and Stevens (2001); particularly important recent
representingseveralEuropeanherbaria(e.g.K,E, work includes Wang etal. (2009: rosids), Tank &
BM, P, G and the Dutch herbaria collectively) that Donoghue(inpress),Mooreetal.(2008,inpress:core
are in the process of reorganizing their collections eudicots), Wurdack & Davis (2009: Malpighiales) and
© 2009 The Linnean Society of London, Botanical Journal of the Linnean Society, 2009, 161, 105–121
APG III 107
Refulio-Rodriguez & Olmstead (2008, pers. comm.: Austrobaileyales Takht. ex Reveal (1992)
Lamiales). Austrobaileyaceae Croizat (1943), nom. cons.
Forthoseresearcherswhowishtoemployaformal, $Schisandraceae Blume (1830), nom. cons. (includ-
higher-level classification for the land plants, Chase ing Illiciaceae A.C.Sm., nom. cons.)
& Reveal (2009) have proposed a system. It is based Trimeniaceae L.S.Gibbs (1917), nom. cons.
on the recognition that most previous systems Schisandraceae s.l. are well characterized.
have inflated the ranks of the angiosperms and the
†Chloranthales R.Br. (1835)
other major groups of land plants. In this system,
Chloranthaceae R.Br. ex Sims (1820), nom. cons.
all embryophytes are a class, and, therefore, the
angiosperms are recognized collectively as a single Chloranthaceae are probably sister to magnoliids
subclass, Magnoliidae, which necessitated the use of (Moore etal., 2007). Separate ordinal status is
superorders for the major angiosperm clades recog- warranted because of their phylogenetic position;
nized here (rosids, asterids etc.). they are also morphologically distinctive.
The general sequence of orders follows the left to
right sequence of the largely ladderized tree in
MAGNOLIIDS
Haston etal. (2009). Within orders, the sequence of
families is alphabetical. Symbols: *new family place- Canellales Cronquist (1957)
ment; †newly recognized order for the APG system; Canellaceae Mart. (1832), nom. cons.
§new family circumscription described in the text; Winteraceae R.Br. ex Lindl. (1830), nom. cons.
$families that represent the broader circumscription
of options available in APG II and favoured here, Piperales Bercht. & J.Presl (1820)
$$families that were in square brackets in APG II, Aristolochiaceae Juss. (1789), nom. cons.
thenarrowercircumscriptionsfavouredhere.Thelist Hydnoraceae C.Agardh (1821), nom. cons.
reflects a starting date for all flowering plant family Lactoridaceae Engl. (1888), nom. cons.
namesas4August1789(Jussieu,Generaplantarum). Piperaceae Giseke (1792), nom. cons.
Fullcitationsareavailableelsewhere(Reveal,2008– Saururaceae F.Voigt (1811), nom. cons.
onward). A summarized phylogenetic tree represent- The relationships of Hydnoraceae are unclear
ing the relationships among the major groups within Piperales.
recognized here is presented in Figure1.
Laurales Juss. ex Bercht. & J.Presl (1820)
Atherospermataceae R.Br. (1814)
CLASSIFICATION OF FLOWERING PLANTS Calycanthaceae Lindl. (1819), nom. cons.
Gomortegaceae Reiche (1896), nom. cons.
†Amborellales Melikyan, A.V.Bobrov & Zaytzeva Hernandiaceae Blume (1826), nom. cons.
(1999) Lauraceae Juss. (1789), nom. cons.
Amborellaceae Pichon (1948), nom. cons. Monimiaceae Juss. (1809), nom. cons.
The evidence that Amborellaceae are sister to all Siparunaceae Schodde (1970)
other angiosperms is clear (e.g. Hansen etal., 2007; Magnoliales Juss. ex Bercht. & J.Presl (1820)
Jansenetal.,2007;Mooreetal.,2007).However,even Annonaceae Juss. (1789), nom. cons.
if they were sister to Nymphaeales (e.g. Goremykin, Degeneriaceae I.W.Bailey & A.C.Sm. (1942), nom.
Viola & Hellwig, 2009), they should be kept separate cons.
as their inclusion in Nymphaeales would result in a Eupomatiaceae Orb. (1845), nom. cons.
taxon without characters. Himantandraceae Diels (1917), nom. cons.
†Nymphaeales Salisb. ex Bercht. & J.Presl (1820) Magnoliaceae Juss. (1789), nom. cons.
$$Cabombaceae Rich. exA.Rich. (1822), nom. cons. Myristicaceae R.Br. (1810), nom. cons.
*Hydatellaceae U.Hamann (1976)
$$Nymphaeaceae Salisb. (1805), nom. cons.
MONOCOTS
There seems to be a general preference for keeping
Acorales Link (1835)
Cabombaceae and Nymphaeaceae separate, although
Acoraceae Martinov (1820)
both are small in terms of species. The two families
are easily characterizable. The inclusion of Hydatel- Alismatales R.Br. ex Bercht. & J.Presl (1820)
laceae (previously included in Poales) here was unex- §Alismataceae Vent. (1799), nom. cons. (including
pected, but it is well supported morphologically and Limnocharitaceae Takht. ex Cronquist)
embryologically(Saarelaetal.,2007;Friedman,2008; Aponogetonaceae Planch. (1856), nom. cons.
Rudall etal., 2008). Araceae Juss. (1789), nom. cons.
© 2009 The Linnean Society of London, Botanical Journal of the Linnean Society, 2009, 161, 105–121
108 THE ANGIOSPERM PHYLOGENY GROUP
Amborellales†
Nymphaeales†
Austrobaileyales
a Piperales
n Canellales
g magnoliids
io Magnoliales
s Laurales
p
Chloranthales†
e
r Commelinales
m
Zingiberales
s
Poales commelinids
Arecales
Dasypogonaceae
m
Asparagales
o
n Liliales
o Pandanales
c
o Dioscoreales
ts Petrosaviales†
Alismatales
Acorales
Ceratophyllales†
Ranunculales
Sabiaceae
Proteales
Buxales†
e
u Trochodendrales†
d Gunnerales
ico Cucurbitales
t Fagales
s
Rosales
Fabales
Celastrales fabids
Oxalidales
Malpighiales
Zygophyllales†
Malvales
c r Brassicales
o o
r s Huerteales†
e id Sapindales malvids
e s Picramniales†
u
d Crossosomatales
ic Myrtales
o Geraniales
t
s Vitales†
Saxifragales
Dilleniaceae
Berberidopsidales†
Santalales
Caryophyllales
Cornales
Ericales
Garryales
a
s Gentianales
te Lamiales lamiids
rid Solanales
s Boraginaceae
Aquifoliales
Escalloniales†
Asterales
Dipsacales campanulids
Paracryphiales†
Apiales
Bruniales†
Figure1. Interrelationships of the APG III orders and some families supported by jackknife/bootstrap percentages
greaterthan50orBayesianposteriorprobabilitiesgreaterthan0.95inlarge-scaleanalysesofangiosperms.Seetextfor
literaturesupportingtheserelationships.Newly-recognized-for-APGordersaredenoted(†).Someeudicotfamiliesnotyet
classified to order are not shown.
© 2009 The Linnean Society of London, Botanical Journal of the Linnean Society, 2009, 161, 105–121
APG III 109
Butomaceae Mirb. (1804), nom. cons. Liliales Perleb (1826)
Cymodoceaceae Vines (1895), nom. cons. §Alstroemeriaceae Dumort. (1829), nom. cons.
Hydrocharitaceae Juss. (1789), nom. cons. (including Luzuriagaceae Lotsy)
Juncaginaceae Rich. (1808), nom. cons. Campynemataceae Dumort. (1829)
Posidoniaceae Vines (1895), nom. cons. Colchicaceae DC. (1804), nom. cons.
Potamogetonaceae Bercht. & J.Presl (1823), Corsiaceae Becc. (1878), nom. cons.
nom. cons. Liliaceae Juss. (1789), nom. cons.
Ruppiaceae Horan. (1834), nom. cons. Melanthiaceae Batsch ex Borkh. (1797), nom. cons.
Scheuchzeriaceae F.Rudolphi (1830), nom. cons. *Petermanniaceae Hutch. (1934), nom. cons.
Tofieldiaceae Takht. (1995) Philesiaceae Dumort. (1829), nom. cons.
Zosteraceae Dumort. (1829), nom. cons. Ripogonaceae Conran & Clifford (1985)
Smilacaceae Vent. (1799), nom. cons.
Convincing evidence for the monophyly of
Alismataceaes.s.islacking(e.g.Chenetal.,2004a,b) Petermanniaceae are morphologically and phylo-
andthefamilydoesnothaveanyapomorphies.When genetically distinct. Luzuriagaceae, consisting of two
combined with Limnocharitaceae, a family that was small genera with generalized lily floral morphology,
only relatively recently described (Cronquist, 1981), are sister to Alstroemeriaceae and have the same
the enlarged family has several distinctive charac- distinctivetwistedpetioles,socombinationisinorder
ters. It may be necessary to split off Maundia from (see also Mabberley, 2008).
Juncaginaceae(Ilesetal.,2009;S.vonMering&J.W.
Asparagales Link (1829)
Kadereit, pers. comm.), and Maundiaceae Nakai is
$Amaryllidaceae J.St.-Hil., nom. cons. (including
available. However, it might be better in this case to
Agapanthaceae F.Voigt, Alliaceae Borkh., nom.
createalargersinglefamilyforthelargerclade.More
cons.)
study is needed before another monogeneric family is
$Asparagaceae Juss. (1789), nom. cons. (including
recognized in Alismatales.
Agavaceae Dumort., nom. cons.,Aphyllanthaceae
Burnett, Hesperocallidaceae Traub, Hyacintha-
†Petrosaviales Takht. (1997)
ceae Batsch ex Borkh., Laxmanniaceae Bubani,
Petrosaviaceae Hutch. (1934), nom. cons.
Ruscaceae M.Roem., nom. cons., Themidaceae
The isolated position of Petrosaviaceae here is well Salisb.)
supported (e.g. Tamura etal., 2004; Chase etal., Asteliaceae Dumort. (1829)
2006), hence its ordinal status. Blandfordiaceae R.Dahlgren & Clifford (1985)
Boryaceae M.W.Chase, Rudall & Conran (1997)
Dioscoreales R.Br. (1835) Doryanthaceae R.Dahlgren & Clifford (1985)
Burmanniaceae Blume (1827), nom. cons. Hypoxidaceae R.Br. (1814), nom. cons.
Dioscoreaceae R.Br. (1810), nom. cons. Iridaceae Juss. (1789), nom. cons.
Nartheciaceae Fr. ex Bjurzon (1846) Ixioliriaceae Nakai (1943)
Lanariaceae R.Dahlgren & A.E.van Wyk (1988)
ThismiaceaeJ.Agardh(1858)mayturnouttobein Orchidaceae Juss. (1789), nom. cons.
a clade separate from Burmanniaceae and, similarly, Tecophilaeaceae Leyb. (1862), nom. cons.
the morphologically distinctive Taccaceae Dumort. $Xanthorrhoeaceae Dumort. (1829), nom. cons.
(1829), nom. cons., from Dioscoreaceae. Phylogenetic (includingAsphodelaceae Juss. and Hemerocalli-
relationships in Dioscoreales that support such daceae R.Br.)
changes have been found by Merckx etal. (2006) Xeronemataceae M.W.Chase, Rudall & M.F.Fay
and Merckx & Bidartondo (2008), and Merckx etal. (2000)
(2009) even suggest that Thismiaceae s.s. may be
paraphyletic. Given the problems in understanding An expanded Amaryllidaceae, including Agapan-
relationships of mycoheterotrophic groups, we have thaceae and Alliaceae, are recognized here (Amaryl-
been conservative and not adopted any altered cir- lidaceae was recently conserved over Alliaceae,
cumscriptions at this stage. despiteAlliaceaebeingtheoldername).Severalchar-
acterssupportthecombinedgroup.Agapanthaceae,if
Pandanales R.Br. ex Bercht. & J.Presl (1820) keptseparate,areweaklycharacterized;thefamilyis
Cyclanthaceae Poit. ex A.Rich. (1824), nom. cons. monogeneric.
Pandanaceae R.Br. (1810), nom. cons. The area aroundAsparagaceae is difficult from the
Stemonaceae Caruel (1878), nom. cons. standpointofcircumscription.AlthoughAsparagaceae
Triuridaceae Gardner (1843), nom. cons. s.l. are heterogeneous and poorly characterized,
Velloziaceae J.Agardh (1858), nom. cons. Asparagaceae s.s., Agavaceae, Laxmanniaceae, Rus-
© 2009 The Linnean Society of London, Botanical Journal of the Linnean Society, 2009, 161, 105–121
110 THE ANGIOSPERM PHYLOGENY GROUP
caceae and even Hyacinthaceae have few if any dis- Restionaceae R.Br. (1810), nom. cons.
tinctivefeatures.AgavaceaeandRuscaceaesensuAPG Thurniaceae Engl. (1907), nom. cons.
II(2003)areheterogeneousandhavebeendividedinto §Typhaceae Juss. (1789), nom. cons. (including
several families in the past, further confusing the Sparganiaceae Hanin, nom. cons.)
issue. This solution at least keeps the number of Xyridaceae C.Agardh (1823), nom. cons.
difficult-to-recognize families to a minimum;Amaryl-
Sparganiaceae are included in Typhaceae; the two
lidaceae s.l. andAsparagaceae s.l. are easily differen-
familiesaremonogeneric,occupysimilarhabitatsand
tiated by umbels with a pair of enclosing bracts vs.
share a number of features. That they were treated
racemes or rarely umbels, but if umbels are present
separately in APG II was a mistake (M. W. Chase,
theycontainthreeormorebracts(e.g.Brodiaea,Milla
pers. comm.). They have in the past been combined;
and relatives, Themidaceae) and lack the enclosing
Mabberley (2008) suggested that their combination
pair of bracts. Xanthorrhoeaceae s.l. have been
would be in order.
maintained for similar reasons to Asparagaceae
s.l. Xanthorrhoeaceae s.s. are monogeneric, and Zingiberales Griseb. (1854)
Asphodelaceae are impossible to distinguish from Cannaceae Juss. (1789), nom. cons.
genera such as Anthericum inAsparagaceae s.l. Costaceae Nakai (1941)
For convenience and better communication, Heliconiaceae Vines (1895)
a subfamilial classification of Amaryllidaceae, Lowiaceae Ridl. (1924), nom. cons.
AsparagaceaeandXanthorrhoeaceaesensuAPGIIIis Marantaceae R.Br. (1814), nom. cons.
proposed in Chase, Reveal & Fay (2009). This will Musaceae Juss. (1789), nom. cons.
allow researchers to use a subfamily name where Strelitziaceae Hutch. (1934), nom. cons.
previously they would have used one of the APG II Zingiberaceae Martinov (1820), nom. cons.
bracketed family names.
PROBABLE SISTER OF EUDICOTS
COMMELINIDS
Ceratophyllales Link (1829)
Dasypogonaceae Dumort. (1829) Ceratophyllaceae Gray (1822), nom. cons.
Relationships of Dasypogonaceae remain unclear. The molecular evidence that Ceratophyllaceae are
They are not particularly distinctive morphologically sister to eudicots is becoming clearer (Jansen etal.,
and so do not warrant immediate ordinal status, 2007; Moore etal., 2007, but cf. Goremykin etal.,
although Dasypogonales Doweld is available. They 2009). In this and all other relationships that have
could probably be combined with one of the other been suggested for Ceratophyllaceae, including sister
commelinid orders should they fall as sister groups. tothemonocotsorChloranthaceae(Endress&Doyle,
2009), they are morphologically divergent from their
Arecales Bromhead (1840)
putative closest relatives.
Arecaceae Bercht. & J.Presl (1820), nom. cons.
Commelinales Mirb. ex Bercht. & J.Presl (1820)
EUDICOTS
Commelinaceae Mirb. (1804), nom. cons.
Haemodoraceae R.Br. (1810), nom. cons. Ranunculales Juss. ex Bercht. & J.Presl (1820)
Hanguanaceae Airy Shaw (1965) Berberidaceae Juss. (1789), nom. cons.
Philydraceae Link (1821), nom. cons. $Circaeasteraceae Hutch. (1926), nom. cons.
Pontederiaceae Kunth (1816), nom. cons. (including Kingdoniaceae Airy Shaw)
Eupteleaceae K.Wilh. (1910), nom. cons.
Poales Small (1903)
Lardizabalaceae R.Br. (1821), nom. cons.
Anarthriaceae D.F.Cutler & Airy Shaw (1965)
Menispermaceae Juss. (1789), nom. cons.
Bromeliaceae Juss. (1789), nom. cons.
$Papaveraceae Juss. (1789), nom. cons. (including
Centrolepidaceae Endl. (1836), nom. cons.
Fumariaceae Marquis, nom. cons., Pteridophyl-
Cyperaceae Juss. (1789), nom. cons.
laceae Nakai ex Reveal & Hoogland)
Ecdeiocoleaceae D.F.Cutler & Airy Shaw (1965)
Ranunculaceae Juss. (1789), nom. cons.
Eriocaulaceae Martinov (1820), nom. cons.
Flagellariaceae Dumort. (1829), nom. cons. We adopt broad limits for Circaeasteraceae and
Joinvilleaceae Toml. & A.C.Sm. (1970) Papaveraceae, as this is commonly done (Judd etal.,
Juncaceae Juss. (1789), nom. cons. 2007; Mabberley, 2008), and the two families are
Mayacaceae Kunth (1842), nom. cons. well characterized in their broader circumscriptions.
Poaceae Barnhart (1895), nom. cons. The two families into which Circaeasteraceae have
Rapateaceae Dumort. (1829), nom. cons. been divided (Circaeasteraceae and Kingdoniaceae)
© 2009 The Linnean Society of London, Botanical Journal of the Linnean Society, 2009, 161, 105–121
APG III 111
are both monogeneric; they are herbaceous and This family has no stable position as yet (Moore
their leaves have the same distinctive dichotomous etal., in press). The ordinal name, Dilleniales DC. ex
venation. Bercht. & J.Presl, is available.
Sabiaceae Blume (1851), nom. cons. Saxifragales Bercht. & J.Presl (1820)
Altingiaceae Horan. (1841), nom. cons.
Although Moore etal. (2008) placed Sabiaceae as
Aphanopetalaceae Doweld (2001)
sister to Proteales, support is only moderate.
Cercidiphyllaceae Engl. (1907), nom. cons.
However, if further work confirms this position,
Crassulaceae J.St.-Hil. (1805), nom. cons.
Sabiaceae will be included in a broadened circum-
Daphniphyllaceae Müll.-Arg. (1869), nom. cons.
scription of Proteales; the two have features in
Grossulariaceae DC. (1805), nom. cons.
common. Sabiaceae remain poorly known.
$$Haloragaceae R.Br. (1814), nom. cons.
Proteales Juss. ex Bercht. & J.Presl (1820) Hamamelidaceae R.Br. (1818), nom. cons.
Nelumbonaceae A.Rich. (1827), nom. cons. $Iteaceae J.Agardh (1858), nom. cons. (including
$$Platanaceae T.Lestib. (1826), nom. cons. Pterostemonaceae Small, nom. cons.)
$$Proteaceae Juss. (1789), nom. cons. Paeoniaceae Raf. (1815), nom. cons.
$$Penthoraceae Rydb. ex Britt. (1901), nom. cons.
Platanaceae, although monogeneric, are morpho-
*§Peridiscaceae Kuhlm. (1950), nom. cons.
logically distinct from Proteaceae, and the two have
(including Medusandraceae Brenan, nom. cons.,
never been combined previously; members of the
Soyauxia Oliver)
broader family would have few features in common.
Saxifragaceae Juss. (1789), nom. cons.
†Trochodendrales Takht. ex Cronquist (1981) $$Tetracarpaeaceae Nakai (1943)
$Trochodendraceae Eichler (1865), nom. cons.
The limits of Iteaceae are broadened because the
(including Tetracentraceae A.C.Sm., nom.
combined clade is well characterized and Pteroste-
cons.).
monaceae are monogeneric. The limits of Halor-
A separate order for this morphologically distinct agaceae are drawn narrowly as the inclusion of
clade is warranted; the two monospecific genera in Penthoraceae and Tetracarpaeaceae would result in
Trochodendraceae s.l., Tetracentron and Trocho- a family with no obvious characters and totally
dendron, have much in common. novel limits. The three families are individually tol-
erably well characterized. Recent molecular analyses
†Buxales Takht. ex Reveal (1996)
strongly support a placement of Peridiscaceae
$Buxaceae Dumort. (1822), nom. cons. (including
within Saxifragales, as sister to all other members
Didymelaceae Leandri)
of this clade (Soltis etal., 2007a; Jian etal., 2008),
*Haptanthaceae C.Nelson (2002)
rather than in Malpighiales as previously proposed.
The limits of Buxaceae are expanded. The monoge- Peridiscaceae continue to be expanded (Davis &
neric Didymelaceae have the same distinctive pollen Chase, 2004; Wurdack & Davis, 2009), but all
and chemistry as at least part of Buxaceae, although members of the expanded family have similar dis-
thereiscurrentlynoevidencefortheparaphylyofthe tinctive seeds etc.
latter. Some morphological features suggest that Cynomoriaceae are another family of holoparasitic
Haptanthaceae are best placed here, but they are angiosperms that have been difficult to place. Some
distinctfromallotherangiosperms(Doust&Stevens, molecular analyses had placed them in Santalales
2005). An order for the two families is warranted. (Jian etal., 2008), although with little support.
Note that relationships of Trochodendrales and However, Barkman etal. (2007) found no support for
Buxales remain unclear, although they are certainly a position in that order or anywhere else. Neverthe-
to be placed in this part of the tree. less, Nickrent (2002) and Nickrent etal. (2005)
suggested that Cynomoriaceae should be placed in
Saxifragales, but the evidence for placing them here
versus in Santalales is not strong. Confounding the
CORE EUDICOTS
placement of this taxon is evidence for horizontal
Gunnerales Takht. ex Reveal (1992) gene transfer involving its host for some mitochon-
$$Gunneraceae Meisn. (1842), nom. cons. drial genes (Barkman etal., 2007). Zhang, Li & Li
$$Myrothamnaceae Nied. (1891), nom. cons. (2009) analyzed sequences from the plastid inverted
repeat and found that Cynomorium fell as sister
The two families share no important features and
to Rosaceae (Rosales) with high bootstrap support
so are kept separate, although both are monogeneric.
(99%). Due to these discordant results, we do not
Dilleniaceae Salisb. (1807), nom. cons. assign Cynomoriaceae to an order here.
© 2009 The Linnean Society of London, Botanical Journal of the Linnean Society, 2009, 161, 105–121
112 THE ANGIOSPERM PHYLOGENY GROUP
ROSIDS Balanopaceae Benth. & Hook.f. (1880), nom. cons.
Bonnetiaceae L.Beauvis. ex Nakai (1948)
†Vitales Juss. ex Bercht. & J.Presl (1820)
*Calophyllaceae J.Agardh
Vitaceae Juss. (1789), nom. cons.
Caryocaraceae Voigt (1845), nom. cons.
Vitaceaeremainisolatedandordinalstatusisappro- *Centroplacaceae Doweld & Reveal (2005)
priate. They are sister to the fabids+malvids (rosid $$Chrysobalanaceae R.Br. (1818), nom. cons.
I+II) clade in most recent analyses, albeit without §Clusiaceae Lindl. (1836), nom. cons.
strong support (reviewed in Wang etal., 2009). Ctenolophonaceae Exell & Mendonça (1951)
$$Dichapetalaceae Baill. (1886), nom. cons.
FABIDS Elatinaceae Dumort. (1829), nom. cons.
$$§Erythroxylaceae Kunth (1822), nom. cons.
†Zygophyllales Link (1829)
(including Aneulophus Benth.)
$$Krameriaceae Dumort. (1829), nom. cons.
Euphorbiaceae Juss. (1789), nom. cons.
$$Zygophyllaceae R.Br. (1814), nom. cons.
$$Euphroniaceae Marc.-Berti (1989)
Although Krameriaceae are monogeneric, they are Goupiaceae Miers (1862)
readily distinguished from the heterogeneous Humiriaceae A.Juss. (1829), nom. cons.
Zygophyllaceae; the two are sister taxa. Combin- Hypericaceae Juss. (1789), nom. cons.
ing the two would simply make a heterogeneous Irvingiaceae Exell & Mendonça (1951), nom. cons.
Zygophyllaceae still more so. An order is needed for Ixonanthaceae Planch. ex Miq. (1858), nom. cons.
this family pair as it is placed with strong support as Lacistemataceae Mart. (1826), nom. cons.
sister to a clade containing more than two fabid Linaceae DC. ex Perleb (1818), nom. cons.
orders in the analysis by Wang etal. (2009). Lophopyxidaceae H.Pfeiff. (1951)
Malpighiaceae Juss. (1789), nom. cons.
Celastrales Link (1829) $Ochnaceae DC. (1811), nom. cons. (including
$Celastraceae R.Br. (1814), nom. cons. (including Medusagynaceae Engl. & Gilg, nom. cons.,
Lepuropetalaceae Nakai, Parnassiaceae Marti- Quiinaceae Choisy, nom. cons.)
nov, nom. cons., Pottingeriaceae Takht.) Pandaceae Engl. & Gilg (1912–1913), nom. cons.
Lepidobotryaceae J.Léonard (1950), nom. cons. $Passifloraceae Juss. ex Roussel (1806), nom. cons.
[including Malesherbiaceae D.Don, nom. cons.,
The limits of Celastraceae are broadened because
Turneraceae Kunth ex DC. (1828), nom. cons.]
the three small families included show every sign
Phyllanthaceae Martinov (1820), nom. cons.
of making Celastraceae paraphyletic if excluded
Picrodendraceae Small (1917), nom. cons.
(Zhang & Simmons, 2006). The dismemberment of
Podostemaceae Rich. ex Kunth (1816), nom. cons.
Celastraceae needed to maintain the families, of
Putranjivaceae Meisn. (1842)
which only Parnassiaceae are well known, would be
*Rafflesiaceae Dumort. (1829), nom. cons.
extensiveandyieldpoorlycharacterizedfamilies,and
$$Rhizophoraceae Pers. (1807), nom. cons.
Celastraceae s.l. are better characterized than Celas-
Salicaceae Mirb. (1815), nom. cons.
traceae,excludingParnassiaceae(formorphology,see
$$Trigoniaceae A.Juss. (1849), nom. cons.
Matthews & Endress, 2005a).
Violaceae Batsch (1802), nom. cons.
Oxalidales Bercht. & J.Presl (1820)
Brunelliaceae Engl. (1897), nom. cons. The holoparasitic Rafflesiaceae are best assigned
Cephalotaceae Dumort. (1829), nom. cons. to Malpighiales, perhaps making Euphorbiaceae s.s.
Connaraceae R.Br. (1818), nom. cons. paraphyletic (e.g. Davis & Wurdack, 2004; Davis
Cunoniaceae R.Br. (1814), nom. cons. etal., 2007); the recognition of Peraceae Klotzsch
Elaeocarpaceae Juss. ex DC. (1816), nom. cons. (1859) would be needed to maintain monophyly of
*Huaceae A.Chev. (1947) Euphorbiaceae. However, pending further studies,
Oxalidaceae R.Br. (1818), nom. cons. Peraceae are not recognized here. Limits of clades in
the Bonnetiaceae–Podostemaceae area are becoming
Huaceae are tentatively included in Oxalidales
clearer (Wurdack & Davis, 2009), and this necessi-
because a number of recent studies (e.g. Wurdack &
tates the removal of Calophyllaceae from Clusiaceae.
Davis, 2009) have indicated that they are sister to
Thealternativeswouldbeafamilythatincludedboth
OxalidalesasrecognizedinpreviousversionsofAPG.
ofthesefamiliesandBonnetiaceae,Hypericaceaeand
This is not a well-characterized clade, and it remains
Podostemaceae or one that included the last two
poorly understood.
families plus Calophyllaceae; in both cases Hyperi-
Malpighiales Juss. ex Bercht. & J.Presl (1820) caceae would be the correct name. The four families
Achariaceae Harms (1897), nom. cons. in the area of Chrysobalanaceae, Dichapetalaceae,
© 2009 The Linnean Society of London, Botanical Journal of the Linnean Society, 2009, 161, 105–121
APG III 113
Euphroniaceae and Trigoniaceae are kept separate similar, even although Rhoipteleaceae have superior
as,althoughclearlyrelated,abroadlydrawnChryso- and Juglandaceae inferior ovaries; ovary position is
balanaceae would be heterogeneous (see Matthews & variable in many families, and in other such cases,
Endress, 2008, for the morphology of this group). e.g. Ebenaceae (including Lissocarpaceae), we have
Bhesa (formerly of Celastraceae) and Centroplacus recognized the larger unit.
(formerly of Euphorbiaceae) form an isolated clade
Rosales Bercht. & J.Presl (1820)
(Davis etal., 2005; Wurdack & Davis, 2009) that has
Barbeyaceae Rendle (1916), nom. cons.
distinguishing features; recognition of a bigeneric
Cannabaceae Martinov (1820), nom. cons.
Centroplacaceae is reasonable. Salicaceae are
Dirachmaceae Hutch. (1959)
broadly drawn, i.e. including Samydaceae Vent. and
Elaeagnaceae Juss. (1789), nom. cons.
Scyphostegiaceae Hutch. Although the combined
Moraceae Gaudich. (1835), nom. cons.
clade is only moderately distinct morphologically and
Rhamnaceae Juss. (1789), nom. cons.
less so phylogenetically (Chase etal., 2002), recogni-
Rosaceae Juss. (1789), nom. cons.
tion of more families in this area is premature
Ulmaceae Mirb. (1815), nom. cons.
pending a more detailed sampling of the genera.
Urticaceae Juss. (1789), nom. cons.
Trichostephanus Gilg, unplaced previously, shares
wood anatomy, disc lobing and seed structure with
SamydeaeVent.(=Salicaceae),andunpublishedDNA MALVIDS
datasupportthisplacement(M.Alford,pers.comm.).
Geraniales Juss. ex Bercht. & J.Presl (1820)
Rhizophoraceae are kept separate from their
$Geraniaceae Juss. (1789), nom. cons. (including
sister taxon, Erythroxylaceae, although Aneulophus,
Hypseocharitaceae Wedd.)
of Erythroxylaceae, is to a certain extent morphologi-
$Melianthaceae Horan. (1834), nom. cons. (includ-
callyintermediate;thetwofamilieshavehithertonot
ing Francoaceae A.Juss., nom. cons.)
been combined. Passifloraceae and Ochnaceae are
§Vivianiaceae Klotzsch, nom. cons. prop. (including
broadly delimited here yet remain readily character-
Ledocarpaceae Meyen)
izable; relationships between the component clades
within the two families are uncertain, and both Geraniales are a heterogeneous and poorly known
Medusagynaceae (Ochnaceae s.l.) and Malesherbi- order. The inclusion of the monogeneric Hypseochari-
aceae (Passifloraceae s.l.) are monogeneric. taceae in Geraniaceae, monogeneric Francoaceae
in Melianthaceae and bigeneric Ledocarpaceae in
Cucurbitales Juss. ex Bercht. & J.Presl (1820)
Vivianiaceae leaves these expanded families with a
Anisophylleaceae Ridl. (1922)
number of characters.
Begoniaceae C.Agardh (1824), nom. cons.
Coriariaceae DC. (1824), nom. cons. Myrtales Juss. ex Bercht. & J.Presl (1820)
Corynocarpaceae Engl. (1897), nom. cons. Alzateaceae S.A.Graham (1985)
Cucurbitaceae Juss. (1789), nom. cons. Combretaceae R.Br. (1810), nom. cons.
Datiscaceae Dumort. (1829), nom. cons. Crypteroniaceae A.DC. (1868), nom. cons.
Tetramelaceae Airy Shaw (1965) Lythraceae J.St.-Hil. (1805), nom. cons.
$Melastomataceae Juss. (1789), nom. cons. (includ-
Fabales Bromhead (1838)
ing Memecylaceae DC., nom. cons.)
Fabaceae Lindl. (1836), nom. cons.
§Myrtaceae Juss. (1789), nom. cons. (including
PolygalaceaeHoffmanns.&Link(1809),nom.cons.
Heteropyxidaceae Engl. & Gilg, nom. cons.,
Quillajaceae D.Don (1831)
Psiloxylaceae Croizat)
Surianaceae Arn. (1834), nom. cons.
Onagraceae Juss. (1789), nom. cons.
Fagales Engl. (1892) §Penaeaceae Sweet ex Guill. (1828), nom. cons.
Betulaceae Gray (1822), nom. cons. (including Oliniaceae Arn., nom. cons., Rhyn-
Casuarinaceae R.Br. (1814), nom. cons. chocalycaceae L.A.S.Johnson & B.G.Briggs)
Fagaceae Dumort. (1829), nom. cons. Vochysiaceae A.St.-Hil. (1820), nom. cons.
§Juglandaceae DC. ex Perleb (1818), nom. cons.
In Melastomataceae, and still more in Myrtaceae,
[including Rhoipteleaceae Hand.-Mazz. (1932),
common usage is for broadened family circumscrip-
nom. cons.]
tions. Both Heteropyxidaceae and Psiloxylaceae are
Myricaceae A.Rich. ex Kunth (1817), nom. cons.
small families and when included in Myrtaceae s.l.
Nothofagaceae Kuprian (1962)
that family remains characterized by possession of
Ticodendraceae Gómez-Laur. & L.D.Gómez (1991)
pellucid glands containing ethereal oils.
Juglandaceae are expanded to include their sister A close relationship between Crypteroniaceae,
clade, the monogeneric Rhoipteleaceae. The two look Penaeaceae, Oliniaceae, Alzataeaceae and Rhyn-
© 2009 The Linnean Society of London, Botanical Journal of the Linnean Society, 2009, 161, 105–121
114 THE ANGIOSPERM PHYLOGENY GROUP
chocalycaceae is clear; Van Beusekom-Osinga & van Brassicales Bromhead (1838)
Beusekom(1975)includedthelasttwofamiliesinthe $Akaniaceae Stapf (1912), nom. cons. (including
first. All families are morphologically similar, Bretschneideraceae Engl. & Gilg, nom. cons.)
although they show variation in floral morphology Bataceae Mart. ex Perleb (1838), nom. cons.
andembryosac,inparticular.Somecombinationisin §Brassicaceae Burnett (1835), nom. cons.
order,andPenaeaceaehavebeenexpandedtoinclude *Capparaceae Juss. (1789), nom. cons.
Rhynchocalycaceae and Oliniaceae; Penaeaceae s.l. Caricaceae Dumort. (1829), nom. cons.
can be characterized. *Cleomaceae Bercht. & J.Presl (1825)
Emblingiaceae J.Agardh (1958)
Crossosomatales Takht. ex Reveal (1993)
Gyrostemonaceae A.Juss. (1845), nom. cons.
*Aphloiaceae Takht. (1985)
Koeberliniaceae Engl. (1895), nom. cons.
Crossosomataceae Engl. (1897), nom. cons.
Limnanthaceae R.Br. (1833), nom. cons.
*Geissolomataceae A.DC. (1856)
Moringaceae Martinov (1820), nom. cons.
*Guamatelaceae S.Oh & D.Potter (2006)
Pentadiplandraceae Hutch. & Dalziel (1928)
Stachyuraceae J.Agardh (1858), nom. cons.
Resedaceae Martinov (1820), nom. cons.
Staphyleaceae Martinov (1820), nom. cons.
Salvadoraceae Lindl. (1836), nom. cons.
*§Strasburgeriaceae Soler. (1908), nom. cons.
Setchellanthaceae Iltis (1999)
(includingIxerbaceaeGriseb.exDoweld&Reveal)
Tovariaceae Pax (1891), nom. cons.
TheadditionofseveralfamiliestoCrossosomatales Tropaeolaceae Juss. ex DC. (1824), nom. cons.
iswelljustified(e.g.Sosa&Chase,2003;Soltisetal.,
2007b; Wang etal., 2009), although monogeneric Inclusion of monogeneric Bretschneideraceae into
Guamatelaceae are a somewhat surprising addition, the monogeneric Akaniaceae is justified by the
Guamatela having previously been included in morphological similarities of the two, which are
Rosaceae (Oh & Potter, 2006). For the most part, sister taxa. Although a broad circumscription of
relationships among families included in Crossoso- Brassicaceae was recognized inAPG (1998) andAPG
matales have not been suggested before. The order is II (2003), the consensus prefers the recognition of
heterogeneous, although the families are all small. three families, all of which can be characterized,
Nevertheless, Matthews & Endress (2005b, 2006) albeit Capparaceae only rather poorly so. The final
found a number of floral features to be at least phylogenetic positions, and hence taxonomic disposi-
common in the order. The sister taxa Strasburgeri- tion, of some genera, particularly those previously
aceae and Ixerbaceae are two monogeneric families included in Capparaceae–Stixeae, remain uncertain
that agree in several characters, including base chro- (Hall, Sytsma & Iltis, 2002; Hall, Iltis & Sytsma,
mosome number and stamen and gynoecial morphol- 2004). Nonetheless, the name Stixaceae Doweld
ogy etc.; combination is in order.As the order is now (2008) is available if it is required.
defined, Staphyleales Mart. (1835) is an older name
Malvales Juss. ex Bercht. & J.Presl (1820)
for Crossosomatales Takht. ex Reveal (1993). It need
$Bixaceae Kunth (1822), nom. cons. (including
not be adopted, however.
CochlospermaceaePlanch.,nom.cons.,Diegoden-
†Picramniales Doweld (2001) draceae Capuron,)
*Picramniaceae Fernando & Quinn (1995) Cistaceae Juss. (1789), nom. cons.
*Cytinaceae A.Rich. (1824)
Picramniaceaewerepreviouslyunplacedrosids,but
Dipterocarpaceae Blume (1825), nom. cons.
thereisnowstrongsupportforapositionintherosid
Malvaceae Juss. (1789), nom. cons.
II/malvid clade (Wang etal., 2009).
Muntingiaceae C.Bayer, M.W.Chase & M.F.Fay
†Huerteales Doweld (2001) (1998)
*Dipentodontaceae Merr. (1941), nom. cons. Neuradaceae Kostel. (1835), nom. cons.
*Gerrardinaceae Alford (2006) Sarcolaenaceae Caruel (1881), nom. cons.
Tapisciaceae Takht. (1987) Sphaerosepalaceae Tiegh. ex Bullock (1959)
Thymelaeaceae Juss. (1789), nom. cons.
This assemblage of three small families is well
supported, and recognition of Huerteales is appro- AbroadcircumscriptionforBixaceaeisadopted;the
priate given their position. Within Huerteales, the threefamiliesincludedareallsmall,andthecombined
recently described Gerrardinaceae (Gerrardina was familycanbecharacterizedmorphologically.Thepara-
previously placed in Flacourtiaceae) are sister to the sitic Cytinaceae (including Bdallophyton Eichl.) find
rest, and Dipentodontaceae, although monogeneric their resting place here (Nickrent, 2007). The novel
like Gerrardinaceae, are distinctive (see Worberg dismemberment of Malvaceae by Cheek (2006), see
etal., 2009). also Cheek in Heywood etal., 2007) is not followed
© 2009 The Linnean Society of London, Botanical Journal of the Linnean Society, 2009, 161, 105–121