Table Of ContentBLUMEA 36 (1991) 1-20
The tuberous epiphytesof the Rubiaceae1:
A new subtribe — The Hydnophytinae
C.R. Huxley & M.H.P.Jebb
Summary
The morphologyandant-association ofthefive generaHydnophytumJack, MyrmecodiaJack,
Anthorrhiza Huxley& Jebb,SquamellariaBecc. andMyrmephytumBecc. aredescribed. On the
basis ofshared characterstatesin tuber cavitydevelopmentand inflorescence structure these five
generaareunited asasubtribe,theHydnophytinae.
Contents
page
Introduction 1
Thegenera 3
Comparativemorphology 5
Tuber 5
Rootsandspines 9
Stems 10
Leaves andstipules 10
Inflorescence andbracts 11
Flowers 12
Fruitand pyrenes 14
Distribution andecology 15
Distribution 15
Ecology 15
Ant-association 15
The recognitionofasubtribeHydnophytinae 16
Rationale ofthe subtribe 16
Position in thePsychotrieae 16
Hydnophytinae 17
Tableofcomparisonofthegenera 18
Key tothegenera 19
Acknowledgements 19
References 19
Introduction
Thetuberousepiphytes oftheRubiaceaehavelong beenasubject ofinterestbe-
cause oftheircomplex chamberedtubers whichareoften inhabitedby ants. The
tubersare derivedfromthehypocotyl which swells, andphellogens arisewithinthe
DepartmentofPlant Sciences,OxfordUniversity, SouthParks Road,Oxford,OX1 3RB,U.K.
2) NowatChristensen Research Institute,P.O.Box 305,Madang,PapuaNew Guinea.
2 BLUMEA VOL. 36,No. 1, 1991
Fig. 1.External form ofthe Hydnophytinae. a.Hydnophytum moseleyanumBecc.; b. H. myrti-
foliumMerr.&Perry; c.H. guppyanum Becc.; d.Myrmecodiatuberosa Jack;e.M.brassii Merr.&
Perry; f.M.platytyreaBecc.; g.AnthorrhizarecurvispinaHuxley&Jebb;h.A.caerulea Huxley&
Jebb;i.SquamellariamajorA.C.Smith. DrawnbyRosemary Wise.
C.R. Huxley & M.H.P.Jebb: The newsubtribe Hydnophytinae 3
parenchyma cutting out volumesoftissuewhichdie, leaving cavities.Ants usually
occupy these cavities and through theirdebrisprovide the plant with a source of
macronutrients(Huxley, 1978).The five generawiththese tubershave undergone
considerablespecialization andspeciation (Huxley, 1981; Jebb,1985).
Rumphius first describedtheseplants in 1750,butLinnaeusdid nottake up the
work and Jack(1823) gave the namesto thetwo main genera:Hydnophytum and
Myrmecodia. OdoardoBeccari (1884-86) describedafurtherthreegenera:Myrme-
phytum, Myrmedoma, andSquamellaria, although hehadno detailsofthetubersin
the lattergenus. SinceBeccari's work, species havebeenaddedpiecemeal except for
Valeton'sefforttomakeacomprehensive survey, buthediedwhilethiswas inprog-
ress (see Huxley, 1976, 1978, 1981).A new genusAnthorrhiza hasnow beende-
scribed(Huxley & Jebb, 1990, 1991a) whichis definedoninflorescence, floral,and
tuber cavity characters, but variableinits vegetative appearance.Myrmedoma has
nowbeen sunkintoMyrmephytum on account ofitsfloralandinflorescencesimilari-
ties (Huxley & Jebb, 1991b).
Itis nowapparentthatthetuberandcavitiesofallthesegeneraarealmostcertain-
ly homologous; coupled withsimilaritiesininflorescencestructure,floralcharacters,
andchorological evidence,thissuggests thatthesegenerahavehada single origin.
Thegroupis also homogeneous inits vegetative morphology, ecology, and distribu-
tion(figs. 1 & 2). We thereforeproposethat these generaare unitedas a subtribe,
the Hydnophytinae.
OurstudiesoftheHydnophytinae havecoveredtheecology, morphology, taxon-
omy,tubers andant-interactionsofMyrmecodia, Hydnophytum, Anthorrhiza, and
Squamellaria (Huxley, 1976, 1978, 1981; Jebb, 1985). Myrmephytum (including
Myrmedoma) hasbeenexaminedtaxonomically inthelightoftheseothergenera,but
only onespecies was availableformorphological study. Revisionsofthegeneraare
published inthis volumeor are inpreparation.
During thelate 19thcentury, studiesandspeculations weremadeontheformation
ofthetubersandtheroleoftheants (Treub, 1883,1888;Beccari, 1884-86;Karsten,
1895).Miehe(191la& b)madedetailedstudiesofthe ant-associationdemonstrating
absorption by certainofthecavity surfaces. Interestthenfocusedon 'physiological'
explanations forthe tubers(Spanner, 1939),untilJanzen'secological study ofthe
plants andtheirants (1974). Isotope tracer studieshavenow shownthat nurtrients
brought by theants, canbeabsorbedby theplants (Huxley, 1978).
THE GENERA
Hydnophytum, with some50 species, is thelargest genusinthe group,and some
species shareunderivedcharacter states with muchofthePsychotrieae. InHydno-
phytum several shrubby stemsarise from thetuberapex (fig. la-c). Thetuberis
roundedand most species lack spines. The tuber cavities ofthis genus show the
greatestrangeofformofall thegenerain theHydnophytinae (fig. 3a-c), butthey
are notascomplex as inMyrmecodia andSquamellaria (fig. 4).Infourspecies the
inflorescenceis sympodial andterminal,andfallsshortly afterflowering andfruiting
(fig. 5a), which is the commonconditionin the Psychotrieae. Intheremaining spe-
ciestheinflorescenceis delayedanddoesnotappearterminally,butarisesinoneaxil
4 BLUMEA VOL. 36, No. 1, 1991
HYDNOPHYTUM MYRMEPHYTUM ANTHORRHIZA SQUAMELLARIA
MYRMECODIA
Hydnophytinae.
the
of
genera
five
the
of
Distribution
2.
Fig.
C.R. Huxley & M.H.P. Jebb: The new subtribe Hydnophytinae 5
at eachnodeandis paired, onepart lying toeach side oftheleafaxil (fig. 5b). In
several species theinflorescenceis pedunculate, whileintheremainderitis sessile,
generally longlived,andoccasionally coveredby persistentbracts.
Myrmecodia has fewerspecies (c. 25), but occupies asimilarrangeto Hydno-
phytum (fig. 2).InMyrmecodia the stems arefewin number,thickwithshortinter-
nodes, andrarely branched(fig. Id—f). Bothstemandtubersbearspines. Thetuber
cavities ofMyrmecodia are sharply differentiatedintosmoothandabsorptive cham-
bers.InMyrmecodia theinflorescenceis alwayspaired, andsunkeninalveolieither
sideoftheleafaxil(fig.5d). Thepartialinflorescencesare larger thanthoseofHydno-
phytum, oftenexceeding one centimeterindiameter.Theseinflorescencescontinue
toproduce flowersthroughoutthelifeof theplant. ThegenusAnthorrhizacomprises
eight species, andexhibits arangeofvegetative morphological variety whichencom-
passes thatseenin bothMyrmecodia andHydnophytum (fig. lg, h). This situation
obscures theformerly clearcutmorphological distinctionbetweenthespiny, pachy-
caulousMyrmecodiaandthenon-spiny, leptocaulous Hydnophytum. InAnthorrhiza
thesingle, large, axillary inflorescenceliesmoreorless centraltotheleafaxil(fig.5d).
Withtheexception ofMyrmephytum (including Myrmedoma) all thegenerahave
4-merousflowers. Myrmephytum has6-merous,blue flowers,andtheinflorescence
is solitary andbractenclosed(Huxley & Jebb,1991b). MuchlikeAnthorrhiza,Myr-
mephytum demonstratesarangeof vegetative morphology, which is explicable in
ecological andevolutionary terms. Thesetwo small generainhabitnon-overlapping
areaswithintherangeofHydnophytum andMyrmecodia (fig. 2).
Squamellaria consistsofthree species withelongated stemsandsparsely spined
tubers (fig. li) (Jebb, 1991).Theinflorescenceissolitary and slightly displaced la-
terally intheleafaxil. Stemsariselaterally as well as apically onthetuberofSqua-
mellaria.Thegenus was originally recognised by Beccari onthestrength offloral
characters, especially the squamules inside thecorollatube andthecapitate,fringed
stigma (1886). Thetubersofthis genushave adifferentcavity structure, whichhas
greatly strengthened thegeneric distinction.Squamellaria isgeographicallyisolated,
inFiji, lyingoutsidetherangeofMyrmecodia, anddemonstratesseveralparallels to
Myrmecodia, Myrmephytum, andAnthorrhizainNewGuinea.
COMPARATIVE MORPHOLOGY
TUBER
Externalfeatures
The tuberis formedby thehypocotyl of theseedling whichswells, even in the
absenceofants (Forbes, 1880;Treub,1883).Insmallspecies typical tubersmay be
8 x 15 cmbutinmostcases thetubercontinuesto grow andmayreach 50 cmacross
in someHydnophytum species. Inonly onespecies (H. normaleBecc.) is thetuber
reported to be facultatively absent(Beccari, 1884-86), although thisis doubtful.
Theexactnature ofthisabsenceis uncertain;forexample stemsofHydnophtum can
takerootby layering or through cuttings, andthendo notform atuber.
The shapeofthetubersresults from theway inwhichnew cavitiesareadded. In
Hydnophytum growth is usually all overthe surfaceor lateral, andthe tubersare
6 BLUMEA VOL. 36,No. 1, 1991
Fig. 3.Tubercavity structure inHydnophytumandAnthorrhiza. a.H. moseleyanum;b.H. myrti-
folium;c.H.guppyanum; d.Anthorrhiza caerulea.Drawnby RosemaryWise.
globose, flattenedor clasping (fig. la). In somespecies growthis apical,producing
elongated tubers(fig. lb,c). InMyrmecodia apical growth produces amoreregular
ovoid, cylindrical tuber(fig. Id, f).Rarely thereis a distinct lowerand upperpor-
tion(fig. le).In Anthorrhiza thetubersvary fromconicaland globoseto flattened
(fig. lg, h).Squamellaria hasrelativelylarge obovoidtocylindrical tuberswhichare
bilaterally symmetrical (fig. li).
Thecolourofthetuber surfacevariesbetweenspecies fromdarkbrownthrough
fawnto grey. Young areasofthetubermay be greenish. Thefleshofthetuber is
normally buffor green,but is magentainseveral species ofHydnophytum andMyr-
mecodia.Longitudinal ridges are commoninMyrmecodia (fig. If), butabsentfrom
C.R. Huxley & M.H.P.Jebb: The newsubtribe Hydnophytinae 7
theothergenera.Squamellaria tubers are 'hooped', being swollenbetweentherings
ofentrance holes. ThetubersurfaceinsomeHydnophytum andAnthorrhiza species
isoftenareolate, whileintheremaining generaitisgenerally smooth.In somespecies
ofMyrmecodia small(1-2 mm)swellings similarin structure totheinternalwarts
(see below) are sometimespresentexternally (Spanner, 1938). In Squamellaria
ratherlarger(3-4 mm) swellings arepresentwhich, atleastinS. majorA.C.Smith,
are associatedwith fungal hyphae (Jebb, 1985). Theseswellings have not been in-
vestigated anatomically.
Formation of the tuber cavities
Thetubercavitiesaremadeby phellogens, meristematiclayers whicharise denovo
intheparenchyma oftheswollenhypocotyl andenclose volumesofparenchyma. In
someMyrmecodiae andHydnophyta thephellogens sometimescutthrough vascular
bundles.Following suberizationofasingle layer ofcellwalls, theenclosedtissue
diesandshrivels(Treub, 1883, 1888; Huxley, 1978).This process is similarin all
five genera,andmaybe unique tothis groupof plants. Thefirstcavity is initially a
simple hookshape inallthegenera,except somemembersofMyrmecodiawhere the
apex is bifid.During subsequent growth ofthetuber thefirstcavity expands only
slightly, exceptinAnthorrhizawhereitgrowsconsiderably (fig.3d),andtoalesser
extentinsome species ofHydnophytum andMyrmephytum. Thefirstcavity always
hasasingle basal opening totheoutside.Thisholeis initially coveredby theepider-
misof thetuber which is usually torn open,either as the tubergrowsor by ants or
otherinvertebrates.
Thecavity system develops by furtherdiscretephellogens eachforming a new
cavity. Theirpositionandstructure isoftencomplex and highlycharacteristic butis
difficulttoexaminebecauseeach cavity is formedamongexisting ones.Latercavi-
tiesmayhavenone, one, fewormanyentrance holestotheoutside, Theseholesare
scattered or maybe arranged in arcs,rings, or two parallel rows along thetuber
(fig. lc).
Latercavities mayormaynot connectwithexisting cavities, though notwiththe
initialcavity. Interconnectionswithothercavitiesare formedinasimilarway toen-
trance holes,with thenew phellogen fusing tothe earliercavity's wall.In certain
species ofMyrmecodia andAnthorrhiza, cavities mayopen atthebaseofthestem
(figs. 3d,4a), andinsomeMyrmecodiae formwithinthe stem.
Smallerholestotheoutside,referredtoas pores,toosmalltoadmitan ant,arealso
foundin manyspeciesofMyrmecodia (fig.4b) andinsomeMyrmephyta. They are
located in small groupsor rings over particularareas ofthecavities (see below).
Wartsare small (c. 1 mmdiameter)pale protrusions on certainofthecavity sur-
faces. Although describedas lenticel-liketheydonot have airspaces betweenthe
smallcytoplasm-filled cells(Huxley, 1978).Thepale surfaceofthewart is unsuber-
izedandalmost certainly highly absorptive. Wartsare probably adapted fromroot
tips, in Hydnophytum guppyanumBecc. andH. kajewskii Merr.& Perry they ap-
pearliketiny roots (Beccari, 1884-86). Theinitialcavity is usually waited, as are
some blind-endedextremitiesoflatercavities. Cavity walls withoutwarts arere-
ferredto assmooth. As arulethecavitywallsofsuperficialcavitiesare more darkly
pigmentedthan deeper-lying cavities.
8 BLUMEA VOL. 36,No. 1, 1991
Fig.4.Tuber cavity structure inMyrmecodiaandSquamellaria.a.M. tuberosa;b. M.platytyrea;
c.M.schlechteri;d& e.Squamellariaimberbis. DrawnbyRosemaryWise.
Structure andposition of the cavities
Thestructure ofthecavities andtheposition in whichthey areaddedare impor-
tantcharacters atspecific and genericlevelandin understanding thewholegroup.
Broadly thereare twokinds ofarrangementofthecavities: a) cavitiesoftwo major
types: someproduced early, whichare for themostpartwaited, andlatercavities
C.R. Huxley& M.H.P.Jebb: The new subtribe Hydnophytinae 9
whichare smooth,or only slightly warted;andb)allthecavities(afterearly devel-
opment) are essentially the same(repeatcavities) andare internallydifferentiatedinto
chamberswithdistinctshapes andpresence orabsenceofwarts. Thetwo-cavitytype
andtherepeat-cavity typeappeartobetwomorphological solutionstotheproblem of
maintaining abalance ofthefunctionally distinctwartedandsmooth-walledsurfaces
as thetuberdevelops. InAnthorrhiza thetwo cavity-type system is developed and
the early wartedcavitiesareabletoexpand not only insizebut alsoincomplexity,
becoming branched(fig.3d). InMyrmecodia andSquamellaria therepeatcavitiesare
differentiatedintochambers withdistinct shapes andsurfacecharacteristics, these
cavitesare addedattheapexofthetuber(fig.4). Intheonly species ofMyrmephy-
tum studiedacombinationoccurs, thefirst cavities growwhilelatercavitiesformre-
peatunitsincorporating both wartedandsmoothchambers. InHydnophytum some
species have two-cavity types, while in othersrepeatcavity unitsareadded either
laterally (fig. 3a) or apically (fig. 3b). The differenttypesofarrangementare not
sharply distinguished inHydnophytum, andtherepeatcavitiesare notascomplex as
those ofMyrmecodia andSquamellaria.
ROOTS AND SPINES
Roots
Theradicalis soonjoinedbytwo tofourotherroots arising fromaroundthebase
oftheswollenhypocotyl. Theseroots growandattachtheplanttoitshosttree. Some-
timesamatureplant isblown looseandmay hang suspended fromitshostby roots
uptoameterlong. Rootsare only veryrarely produced withinthecavities.Theroots
ofotherepiphytes (e.g. Dischidiaspecies, Asclepiadaceae) oftenenter thecavities,
andmaybemistakenforthoseofthe mbiaceousant-plant (Janzen, 1974;pers.obs.).
Spines
Spines arepresentinall five genera.They havea vascular structure whichindi-
cates they aremodifiedadventitiousroots, newly grownspineshaveroot caps(Treub,
1883), andthereis alsoa gradationfrom spines toroots. Spines are most common
on the tubers,especially aroundtheentrance holes. They are alsocommon around
the inflorescence,and densely clothethestems inmany species ofMyrmecodia.
Spines sometimesoccur inunexpected places: inthe spiny species ofAnthorrhiza
and Myrmecodia leafscars occasionally give rise to spines. InAnthorrhiza spines
havebeenfoundontorn andeatensurfacesoftheleaves.The spines maybesimple,
varying fromweak to very stout,orbranched.Branching maybeirregular, or stel-
lateinMyrmecodia, Myrmephytum, Anthorrhizaandonespecies ofHydnophytum.
Colourvariesfromblack to goldenor silvery.
Spines are only rarely present inHydnophytum, andin Squamellaria they are
simple andflexible.Sometimesshortadventitiousrootsmay bepresent aroundthe
inflorescenceofHydnophytum species.
Spines areusually presentonthe tuberandstemofMyrmecodia. They vary from
simple orroot-liketorepeatedly branchedorregularly stellateorclub-shaped. Onthe
stemthey areoftenwell developed roundthealveoliandclypeoli; whileon thetuber
they are mostdevelopedround theentrance holes,andon theridges.
10 BLUMEA VOL. 36,No. 1, 1991
InAnthorrhizathereis arangefromcomplete absenceofspines todense, stellate
spines. Whenspines arepresentonbothstemandtuber,thoseonthestemarelonger
andmorebranchedthanthoseon thetuber. InAnthorrhiza, butnot intheothergen-
era, spines sometimesarisewithintheinflorescences onridges oftissuebetweenthe
flowerbearing patches. They also ariseonlongitudinal ridges along thestems.The
spines ofMyrmephytum are denseron thetuber thanon thestem, and vary from
simple toirregularly stellate.
STEMS
Thestemsofthefive generaare subherbaceousto woody, andreachbetween 10
and 100cminlength. Thefirstfewnodesare sterile, andafterthestembecomesfer-
tiletheintemodesare shorterandfatter.
InHydnophytum thereare fewto many,oftenfreely branched, stems,whilein
Myrmecodia oneor afew littleor unbranchedstems arepresent, thestem is very
thickand thefertileintemodesare greatly reducedinlength. Inseveral species of
Myrmecodia thereis ashield-shaped boss from whicheach leafarises, theseclypeoli
may bespine fringed andhidethestementirely (fig. 4a).In afewspecies cavitiesare
present,making fourtunnelsalong thestemwhichopenatthealveoliandofteninter-
connect. InAnthorrhizaandMyrmephytum,bothHydnophytum- -likeandMyrme-
codia-like stemsare found.InSquamellaria stems arepresent atthe apexandlaterally
on thetuber, eithersinglyor inclusters.InS. majorone stemarisesbetweeneach
ring ofentrance holes, andtheintemodesare thickenedand contractedtowardsthe
stem apices. ThevasculartissueinHydnophytum stemsformsacylinder, whilein
Myrmecodia itispresentasfourbroadstrands.In Myrmephytum arfakianum (Becc.)
Huxley & Jebb thehighly condensed stemdoesnot begin toelongate and flower
untilthetuberhasreachedasubstantialsize.
LEAVES AND STIPULES
Leaves
Theentireleavesaretypically leathery, being sometimesratherfleshyinHydno-
phytum, and usually largerandthinnerinMyrmecodia. AthighaltitudesHydnophy-
tumandsomespecies ofAnthorrhizatendtolack antsandhavesmall, sclerophyllous
leaves (fig. lb); whileMyrmecodia andspecies ofAnthorrhizawithantshavelong,
narrow leaves(fig. le, h). Themidribandpetiole are usually greenbut maybeal-
most whiteor maroon colouredinMyrmecodia. Somespecies ofall thegeneraex-
ceptHydnophytum haveundulateleafmargins.
Stipules
Thestipules ofallgeneraformasquare-based pyramid covering thenextpairof
leaves.As theseleavesextendandthestemswells, thestipules split ina characteris-
ticway.InHydnophytum andSquamellaria they split opposite thepetioles, leaving
twotriangularpieces across thenodes.Thesestipules soonfall. In Myrmecodia the
stipules split opposite andbetween thepetioles, and usuallypersist aspairs oftrian-
gularprojections ineachleafaxil. In somespecies they areprominent andpersistent
ontheclypeoli (fig. 5d). InAnthorrhizathestipules arecaducous topersistent, and
