Harvard University Herbaria

THE AVICENNIACEAE IN THE SOUTHEASTERN UNITED STATES

Author(s): Roger W. Sanders
Source: Harvard Papers in Botany, Vol. 1, No. 10 (April 1997), pp. 81-92
Published by: Harvard University Herbaria
Stable URL: http://www.jstor.org/stable/41761528
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 THE AVICENNIACEAE IN THE
SOUTHEASTERN UNITED STATES1

Roger W. Sanders2

AVICENNIACEAEEndlicher, Bot. 314. 1841,"Avicennieae,"

Enchiridion nom.cons.
(Black MangroveFamily)
Mangroveshrubsand trees; root systems subcapitate[or spicate]unitsthatare arranged
composedof horizontally radiating, cable-like in terminal and axillarypaniculateclustersdis-
extension rootsthatbeardescending, anchoring tallyon twigs;basal axes subtended by foliage
roots and erect,pencil-likepneumatophores; leavesanddistalaxes bytriangular bracts;usu-
trunk simplebelow,withaerialstiltrootsocca- ally onlya singlenode (one or bothflowers)
sionally developed low on trunk,much perunitin anthesisat a time.Flowersperfect,
branchedabove; vegetativeextensiongrowth hypogynous, protandrous, modifiedpentamer-
sympodial(fromdormantbuds in leaf axils ous andzygomorphic [toseemingly tetramerous
belowinflorescences); budsenclosedby petio- and weakly zygomorphic or actinomorphic],
lar groove of subtendingleaves, bud scales subtendedby single,triangular bract and 2
developed on lateral buds, terminalbud smallerlateralbracteoles, the3 structures imbri-
enclosedbytheterminal leafpair.Leavesoppo- catelyencasingthebudbase,closelyappressed
site,decussate, persistent, exstipulate, petiolate; to and nearlyequallingthesepals. Calyx of 5
bladessimple,entire, withpinnatevenation, the sepals,veryshortly connateat base, imbricate.
secondary veins brochidodromous; both sur- Corolla sympetalous, tubularin proximalhalf,
facesbearing,in minutepits,subsessileglands expandedand dividedinto4 [teratologically 5
thatexcretea hypersaline solutionthatrapidly or 6] prominentlobes in the distal half.
driesto formsalt (sodiumchloride)crystals; Stamens4 [teratologically 5 or 6], ascending
upper surface glabrous; lower surface with a under the adaxial (upper) lobe and didyna-
uniform,dense palisade-likearrangement of mous,withtheabaxial (lower)pairlonger[or
microscopicdavate hairs, these sometimes radiating in two equal pairs],alternating with
deciduousinpatchesandgenerally exposingthe and insertedbelow thelobes; anthersbilobed,
salt-gland pits.Inflorescences of pedunculate, dorsifixed, dehiscingintrorsely bylongitudinal
'PreparedfortheGeneric Flora oftheSoutheasternUnited a
States,long-term initiated
project, and continued
byCarroll
E.Wood, Jr.,madepossible bygrants fromtheNational Science andatthis
Foundation, writingsupportedbyDEB-9419940
(WalterS. Judd,principal andDEB-9419952
investigator) (Norton G.Miller,principal Thistreatment,
investigator). the
146thintheseries,followstheformat inthefirst
established one(Jour.ArnoldArb.39:296-346. 1958)andcontinued tothe
Theareacovered
present. bytheGeneric FloraincludesNorth andSouth Carolina,
Georgia,Florida,Tennessee,
Alabama,
andLouisiana.
Arkansas,
Mississippi, Thedescriptionsarebased ontheplants
primarily ofthisarea,withinformationabout
members
extraregional ofa family orgenusinbrackets[ ].Thereferences I have
that aremarked
notverified with anasterisk.
I thanktheprincipalinvestigatorsfortheinvitationtoprepare thiscontribution, with
forassistance and
theliterature,
Thestaff
guidance. oftheBotanical ResearchInstitute
ofTexas, Barney
especially Lipscomb,Assistant facilitated
Director,
myextensive useofthelibrary.I alsoconsultedthelibrariesoftheUniversityofTexasatAustin,theUniversityofTexas at
Arlington,TexasChristianUniversity,andFairchild Tropical Garden. Specimenshoused intheherbariaoftheBotanical
ResearchInstituteofTexasandthePlantResources Center, ofTexasatAustin
University (includingtheMoldenke
aswellasliving
Collection), andherbarium specimens atFairchildTropicalGarden,wereusedinthis BillieL.Turner
study.
hostedmyvisit tothePlant Resources Wilma
Center. Campbell, W.S.Judd, N.G.Miller,P.B.Tomlinson, C.E.Wood, Jr.,
andW.B. Zomlefer provided numerous helpfulcomments.
Theillustration
wasdrawn byRachel A.Wheeler in1967under anearlier
grantfromtheNational Science
Foundation for
research
ontheGeneric Flora (C.E.Wood, Jr.,principal Thedissections
investigator). werepreparedandtheillustration
super-
visedbyG.K.Brizicky andWood. Thematerials usedwere collected
byR.B.Channell (a)andWood andK.A.Wilson (b-f)
inFlorida;byWood inPuerto Rico(h);andbyC. L. Lundell inBelize(g,from Lundell7009, gh).
2ResearchAssociate,Botanical Research Institute
ofTexas, 509PecanStreet, FortWorth,Texas76102-4060, U.S.A.;
e-mail:
rsanders@mesquite.brit.org
Harvard
PapersinBotany,
No.10,1997,
pp.81-92.
andFellows
©President ofHarvard 1997.
College,

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82 HARVARDPAPERS IN BOTANY
slits but retainingadherentpollen. Gynoecia
bicarpellate,syncarpous,seated on a flat
hypogynousdisk (nectary?);style branches
2, moreor less equal; ovaryuniloculateabove,
2 [or 4] loculatebelowtheincomplete central
axis with2 [or4] basal buttress-likepartitions,
theplacentation seemingly ovules
free-central;
4, pendent from cap of central axis, more or
less orthotropous, micropyles enclosedin the
partialbasal locules. Fruitscapsule-like,thin
walled, leathery, smooth(or becomingwrin-
kled in age) [or pitted],laterallycompressed;
thecalyx,bracteoles, andbractpersistent; fruit
oftenfallingunopened;pericarpsplitting open
alongabaxialand adaxialsuturesbygrowth of
embryo.Embryo1 (rarely2), closelyinvested
by pericarp,oftenviviparous,endospermand
seed coatabsent;cotyledons 2, fleshy,cordate-
reniform,conduplicate and encirclingthe
somewhatcurved plumularaxis; hypocotyl
exposed,investedwith non-absorptive hairs;
germination phanerocotylar.Base chromosome
number18. Typegenus:AvicenniaL.
A small tropicalfamilyconsistingof the
single genusAvicenniawith probablyfewer
thantenspecies,one extending intotheUnited
Statesalongcoastssouthof 30° N; apparently
absent from Hawaii. This genus is often
includedintheVerbenaceae, usuallyas thesub-
family Avicennioideae Briq.
As an important memberof the mangrove
formation, or mangal,all speciesofthisfamily
exhibitadaptationsconvergent withthose of
othermangroves (fora moredetailedsummary
of the following,consultTomlinson,1986).
Specializederect,lateralrootsaredevelopedas
pneumatophores, andlongitudinal airchambers
developinthecortexofthepneumatophores, as
wellas intheextension, anchoring, andabsorb-
ingroots(Chapman,1944; Metcalfe& Chalk,
1965,1983).The plantsaretolerant ofhighsalt
concentrations and excretehypersalinesolu-
tionson bothleafsurfacesvia subsessileglan-
dular hairs. Leaves exhibitsome xerophytic
suchas a well-developed
specializations, hypo-
dermis,abundant terminal tracheids,andscler-
ifiedbundlesheaths(Metcalfe& Chalk,1965).
The moreorless viviparous fruitsaresea-water
The
dispersed. hypocotyl of theembryo catches
in softmud,allowingimmediate growth of the
seedling.The successionofmangrove commu-
nitiesis truncated;primarycolonizers(man-
groves) almost directlygenerate a highly
unusual edaphic climax community.As a
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No. 10
result,thespeciesare r-adapted reproductively
butareK-adaptedintermsofcommunity struc-
tureandvegetative growth. The Avicenniaceae
are usuallycodominant withRhizophoraceae,
thetwobeingthemostsalt-tolerant ofthevari-
ous mangroves. Whether theAvicenniaceae are
moreseaward(as in Queensland)ormoreland-
ward(as inSouthFlorida)thanRhizophoraceae
dependslargelyon the coastal physiography
andtherelativesizes of theseedsofthepartic-
ular species involved.The Avicenniaceaeare
also themostfrosttolerantof themangroves.
Atthelatitudinal extremes, multiple lateralreit-
erativeshootsdevelopnearthestembase after
frosthas killedthe shoottips,forming short,
dense-crowned shrubs.
Otherspecializationswith respectto pre-
sumedrelatives involvestemandrootanatomy,
pollen morphology, gynoecialanatomy,and
embryology. Thesespecializations mayor may
notbe relatedto themangrove habit.The stem
and root wood (Carlquist; Görts-vanRijn;
Krishnamurthy & Sigamani;Metcalfe& Chalk,
1965, 1983; Tomlinson,1986; Zamski) has
veryregularanomalousgrowthringsthatare
producedby successivecambia.Aftergenerat-
inga broadbandof xylemto theinsideandup
to tencell layersof parenchyma to theoutside,
each cambiumbecomesinactive.Some of the
parenchyma cells further (re)differentiateinto
strandsof phloem,an outerlayerof sclereids,
or a new continuousringof cambium.The
wood of theAvicenniaceaeis diffuseporous
and consistsof radial files of comparatively
small vessels withsimpletransverse perfora-
tions,homogeneousuniseriateto multiseriate
rays,and nonseptate libriformfibers.The pro-
ductionof growthringsis notcorrelated with
age or seasonal patternsbut is controlledby
endogenous factors.Crystalline lapachol,a yel-
low-colored quinone,oftenaccumulatesin the
heartwoodvessels. Parenchymacells often
containcubiccrystals.
Pollenis spheroidal andtricolporate, withthe
ora protruding and colpi deeplyintruded. The
exineis moreor less reticulate, withthemuri
broadandtheluminasmall(Tomlinson, 1986).
The gynoecium of theAvicenniaceaeis best
understood by comparisonwiththatfoundin
theVerbenaceaeand Labiatae(Lamiaceae).In
thelattercase, themarginsof thetwocarpels
notonlymeetto forma septumbetweenthe
carpels,butbend at rightangles,intrudeinto
thechambers, and abutthemedialdorsaland
ventralovary walls to formfour separate
1997 SANDERS, AVICENNIACEAE 83

Figure1. Avicennia.a-h,A. germinans : a, branchlet

withyoung x 1/2;b,nodeofinflorescence
fruits, with
flower andbud(atleft),
(atright) x 4; c,openedcorolla,x 3; d,anther,
x 10;e,gynoecium insectiontoshow
modified axileplacentation;
f,placenta withfourpendulous ovules,x 20; g, mature x 1; h, young
fruit,
x 1.
seedling,

locules. The partitionsseparatingthe carpels as inotherspecies).The apexofthecentralaxis

are, thus, true partitionsor septa, and the
intrudedmarginsare consideredto be false
ones. The ovules in the Verbenaceae are
attachedto the false partitions only,and are
usuallybasal to medial,erect,and anatropous
to hemianatropous. In the Avicenniaceaethe
twoor fourlocules,whichare separatedat the
base of the ovary,are confluent above intoa
singlelocule.The buttresses of thecentralaxis
consistof twowell-developed lateralpartitions
and two falsepartitions,whichare developed
eitheras mereridgeson thecentralaxis (i.e.,
two basal locules, as in certainspecies) or
acrossthecarpelfloors(i.e., fourbasal locules,
formsa cruciform umbonatecap, itsarmscor-
responding to the fourbasal partitions. The
umboprojectsintobutdoes notclose thestylar
canal. The partialpartitionsat thebase of the
ovaryandthearmsofthecap ofthecentralcol-
umnare directlycomparableto thecomplete
partitionsdividinga verbenaceous/lamiaceous
ovary.Althoughthe ovules of theAvicennia-
ceae are apical, pendulous,and moreor less
orthotropous, theytoo are attachedlaterallyon
each side ofthetwomedialarms,whichcorre-
spondto thefalsepartitions. These gynoecial
peculiaritiesare essentiallyidenticalto those
occurringin the threegeneraconstituting the

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84 HARVARDPAPERS IN BOTANY No. 10

verbenaceoussubfamilySymphorematoideae him by Leon Croizat (quoted in Moldenke,

(Bentham)Briq.,whichsometimestoo is rec- 1960a),althoughno character supportis given
ognized as a separatefamily on the basis of in the letters. A santalalean-celastralean rela-
these characters. The gynoecia in the tionshiphas been suggestedon the basis of
AvicenniaceaeandVerbenaceaeareconsidered embryological features (vanTieghem,see com-
hereto be homologous. mentsabove;Dahlgren,1975a,b, butremoved
Ovule structure is highlyunusual.Although byhimin 1980 andalso fromlaterpublications
the ovules have been interpreted as lacking withoutcommentor alternateplacement).
integuments and a nucellus (van Tieghem), Otherwise, Avicenniais treatedas an atypical
moreconvincing studiessupportthefollowing memberof theVerbenaceaeand placed in its
inference(Briquet;Davis;Junell; Padmanabhan, own subfamily(Briquet;Cronquist;Erdtman,
1960,1964): the nucellus is a small nipple-like 1966; Hegnauer; Melchior; Reddy et al.;
projectionon thetip of the more or less undif- Thorne,1976).
ferentiatedtissue representingthe single Whether theAvicenniaceaeare alignedwith
integument. The integument nevergrowsup theLamíales(heretreated as fullysynonymous
overthenucellustoforma micropylar canal,but, withthe Scrophulariales following G. Dahlgren;
as themegagametophyte develops, its chalazal Judd et al., Thorne, 1992; and Wagenitz)or
endpenetrates theintegumentary tissue,andall another orderis resolvedbydetermining which
exceptthemicropylar endbecomesenveloped. ordinallevelsynapomorphies occurin thefam-
The gametophyte remainsin theapical portion ily.Of thetenputativesynapomorphies listed
oftheovuleandis linear-cylindric or fusiform. by Juddet al. for the Scrophulariales, the
Although it is and
monosporic initiallyeight homologous state is known with certainty in
nucleate (Polygonumtype), the antipodals Avicenniaforonly six. However,all six are
degenerate quickly.Endosperm development is apomorphic:stipulesabsent;leaves opposite;
ab initiocellular,witha single,saclike,cha- stornatapredominantlydiacytic (Cantino,
lazal haustorialcell and two much-enlarged 1990); corollasbasicallyzygomorphic and bi-
micropylar haustorialcells. The largerof the labiatewiththe upperlip two lobed and the
two becomes multinucleate and producesa lowerthreelobed (here interpreted to be the
highly branched haustorial tube that penetrates ancestral state in Avicennia); stamens didyna-
thefulllengthoftheintegument, thefuniculus, mous, with the lower pair longer(likewise
andthecentralaxisoftheovary.Embryodevel- interpreted); embryogeny onagrad; and
opmentconforms totheonagradpattern. As the endospermwith conspicuous chalazal and
endosperm tissue develops, it and the embryo micropylar haustoria.Because flavonoidsare
the
expandbeyond apical region of the integu- poorly studied inAvicennia(onlyfourflavones
mentand continuedevelopingdirectlyin the identified; Reddyetal.; Hegnauer),theabsence
ovarychamber. Eventually, theembryofillsthe of 6-oxygenated flavonesis nota clearindica-
entirefruit,and the witheredremainsof the tionof theplesiomorphic state.These six apo-
centralaxis, integument, and endospermare morphies,as well as the occurrence of
pressedagainsttheembryo'saxis.The embryo non-seco-iridoids, unitegmicand tenuinucel-
is spatulate(Martin)but withthe cotyledons late ovules,spatulateembryosand degenerate
conduplicately folded,one insidetheother, and endosperm,and synsepalous, sympetalous
withtheplumular axiscurveddownward some- flowersare inconsistent and nonparsimonious
whatbringingthe marginsof the cotyledons with placementsnear the Dipterocarpaceae,
down over the hypocotyland radical(Duke, Santalaceae,or Celastraceae.Any presumed
1969; Tomlinson, 1986). synapomorphies withthesefamilies,such as
These unusualvegetative, physiological, and cellular endospermdevelopment(Dahlgren,
reproductive characters have led manyrecent 1975a, b) or ategmic,anucellarovules (van
authors(Carlquist;Erdtman,1945; Takhtajan; Tieghem),arelikelytobe misinterpretations (as
Thorne,1992) to recognizeAvicenniaas a dis- suggestedby Junellor vanTieghem),conver-
tinctfamilyrelatedto Verbenaceae,although gences,orsymplesiomorphies.
otherrelationships havebeensuggested. Inpartic- Determining theexactrelationships withthe
ular,Moldenke(1960a; Moldenke& Moldenke) Verbenaceae is complicated byproblems within
championed a dipterocarpaceousancestry, thatfamilyas it is traditionally conceived.
apparently on thebasisoftwoletters written to Recentstudiesshowthefamilytocomprisetwo

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1997 SANDERS, AVICENNIACEAE 85

distinctclades. One is subfam.Verbenoideae, data matrix (1992) and added Avicennia,

whichis diagnosedby the followingsynapo- CongeaRoxb.(Symphorematoideae), PhrymaL.
morphies: ovules attachedto the margins of the (Phrymaceae), and Lantana L. and Verbena L.
falseovarypartitions, inflorescences racemose, (Verbenoideae), anda fewadditional characters.
pollentricolporate, exinethickened adjacentto Althoughthe resultsprovedinappropriate for
theaperatures, stylebranches replacedbya two- publicationin thatpaper,theyillustrated the
lobedmassofstigmatoid tissue,andabsenceof difficultyof the familial disposition of
uniseriatemulticellulartrichomes(Cantino, Avicennia.I foundthatAvicenniaand Congea
1992; Chadwellet al.; Juddet al.). The other alwaysformeda clade unitedby the synapo-
clade encompassesnot only the Viticoideae morphiesof ovulesfullyapical (and pendent),
(Dumort.) Briq., Chloanthoideae(Bentham) ovarylocules confluent, fruitan indehiscent
Briq., and Caryopteridoideae (Bentham)Briq., capsule, and pollentricolporate. The topologi-
butalso theentireLabiatae,as subcladespoly- cal positionofthiscladewas labilebasally.The
phyletically dispersedamongthethreesubfam- positionswere 1) sistergroupto all remaining
ilies.This clade is delimitedby thefollowing taxa,2) sistergroupto theLabiataesensulato,
synapomorphies: ovules attachedlaterallyto 3) coordinatewith the Phrymaceae,Verbe-
the false ovarypartitions and inflorescences naceae sensu stricto(i.e., Verbenoideae),and
basically cymose. Furthermore, themolecular Labiataesensulato, or4) embeddedamongthe
evidence(Olmsteadetal., Olmstead& Reeves) lowerclades of theLabiataesensu lato. With
indicatesthattheVerbenoideae and thesecond the Labiatae sensu lato, the Avicenniaceae/
clade are derived separately within the Symphorematoideae clade shares the ovules
Lamíalessensulato. The twoclades,therefore, reducedtotwopercarpelandlaterally attached
arenotsistergroups.Thus,thecorrelated char- to the false partitions. WiththeVerbenaceae
actercomplexpreviously thought to unitethe sensustricto , itsharesracemoseinflorescences,
Verbenaceae (plusLabiatae),i.e.,ovules reduced ovules reduced to twopercarpel,and tricolpo-
totwopercarpel,carpelsdividedbyfalseparti- ratepollen. In bothcases, it lacks a schizo-
tions,fruitsbasicallyschizocarpic, andpericarp/ carpicfruitand a reticulate pericarp/endocarp.
endocarpsreticulated, represents convergence. From a cladistic perspective,the numerous
Thus,theVerbenaceae sensustricto consistonlyof peculiarities of theAvicenniaceaecitedabove
theVerbenoideae, whereas,theLabiataesensu can be viewedas autapomorphies ofAvicennia
latoareradicallyexpandedto includetheclade or of the Avicenniaceae/Symphorematoideae
withlaterallyattachedovules,i.e.,Viticoideae, clade. However,underlying thesepeculiarities
Chloanthoideae, Caryopteridoideae, andLabiatae are othercharactersin wood anatomy,floral
sensustricto (Cantino,1992;Cantinoet al.; Judd anatomy, embryology, pollenmorphology, and
etal.; Thorne,1992;Zomlefer, 1994). the chemistry of iridoids,flavonoids, triter-
Because theAvicenniaceaeare peripheral to penes,and quinonesthatare consistent witha
the relationship of the Labiatae and Verbe- placementnear the Labiatae sensu lato or
naceae,as thesefamilieshavebeentreatedtra- Verbenaceae sensustricto(Carlquist,Kooiman,
ditionally,the Avicenniaceae have notyet been et
Reddy al.). Clearly, moremorphological,as well
sampledinanypublishedfamilial/ ordinallevel as molecular,comparisons,analyzedcladisti-
cladisticanalyses(Cantino,1992; Olmstead& cally,areneededto resolvetherelationships of
Reeves). While a
preparing paper on cladistic the Avicenniaceae (and Symphorematoideae)
patterns amongfamilypairs(Juddetal.), I sub- to theVerbenaceaesensustrictoand Labiatae
sampledthetaxa and characters of Cantino's sensulato.

1. AvicenniaLinnaeus,Sp. Pl. 1: 110. 1753; Gen. PI. ed. 5. 49. 1754.

Slender[or spreading]trees10-15[-30] m flaking];branchlets and twigsslender,moreor
tallor reducedto dense-crowned shrubsabout less tetragonal [to hexagonalor terete]becom-
1 mtallwhenkilledbackbyyearlyfrosts; pneu- ingteretewithage,jointedwithswollennodes,
matophores to
projecting 30 cm above the sub- brownish, glabrousor minutelygrayishtomen-
strate;bark rough, fissuredor checkered, tose [to finelylanate],oftenshiny,sparsely
blackishwithlightergrayfissures[to grayish lenticellate. withpetioles1-3 cm
Leavespetiolate,
and lenticellate, or
pustulate smooth,pale and long,denselygray matted,minutely tomentose

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86 HARVARDPAPERS IN BOTANY
to glabrous,witha deep basal adaxialgroove
containing gray[black]marginal hairsthatcon-
tinueas a lineacrossthenode;bladesmoreor
less subsucculent to coriaceous,withvenation
obscured(whenfresh)exceptmidrib prominent
below,narrowlyoblong ellipticto lanceolate
elliptic[broadlyoblong-elliptic, ovate, obo-
or
vate, linear-elliptic], apex obtuse to acute(or
or
acuminate)[rounded attenuate], base acute;
uppersurfacegray-green, brightgreen,or deep
green,denselypunctulateby salt gland pits;
lower surface pale gray-greenor silvery
[yellowish or olive], matted tomentulose
(sometimes bothsurfacesnigrescent upondry-
ing). Inflorescence axes denselygraymatted
tomentulose;floweringunits composed of
2-10(-15) decussateflowerpairs.Flowerswith
subtendingbractsand bracteolespuberulent
[and ciliate]; calyx light green, densely
appressedpubescent[or glabrous] outside,
glabrous within [marginallyciliate]; lobes
ovate to triangular; corolla whiteor cream,
becomingwhiteor throatinfusedwithyellow
[whitewitha distinctly yellowthroat, yellowor
orange],rotate-subbilabiate [rotatecampanu-
late],puberulent [toglabrous]outside,puberu-
lent-tomentose [glabrousor minutely capitate
glandular in tube]inside;corollalobesexceed-
ing or equalling [or shorterthan]the tube,
slightlyimbricate[valvate] at first,widely
spreadingand becomingreflexed withage [or
erect-ascending, sometimesthetipsreflexed],
withthe marginsrecurved[straight], unequal
[or equal], the abaxial and two laterallobes
roundedor slightlyemarginate, spatulateor
broadlyclawed[oblongto deltate,acutish],the
adaxiallobe broadlyoblonganddistinctly two-
lobed at apex [oblongto triangular, acutish,
unlobed].Stamensexsertedfromtube[moreor
less included];filaments slender,inserted near
baseofcorollatube[nearlyobsolete,inserted at
corollamouth];anthers agingblackish,dehisc-
ing introrsely by longitudinal slits.Gynoecia
spherical-conic, more or less puberulentor
tomentose, unilocular
bicarpellate, above,2 [or4]
loculate below, the placentationseemingly
free-central,but actuallymodifiedaxile,with
4 pendulous ovules; style elongate, about
equallingstamens[moreor less obsolete,with
style-branches sessile, not reachinganthers],
puberulent glabrous.Fruitscapsule-like,
or flat-
tenedovate [to elliptic],oftenobliquelyso,
witha prominent, persistent stylarbeak; peri-
carp thin,lightgreen,and variouslyinfiised
withanthocyanin, denselywhitetomentulose
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No. 10
[to glabrescent],suturelines impressed.Seed
one; endospermand seed coat absent; ripe
embryo brightgreen [often anthocyanic];
cotyledonsand plumulemoreor less glabrous
[puberulent];hypocotylwith short,straight
[longandwavyorhooked]hairs.Typespecies:
A. officinalisL., the only species listed by
Linnaeus;see W. T. Stearn,Kew Bull. 13: 35.
1958. (Named in honorof Abu Ali Alhosean
Ben Sina, better known as Avicenna,
980-1037, a Persianphysicianand naturalist.)
- Black Mangrove.
A smallgenusof abouteightspeciesoftrop-
ical and subtropical salinecoastalswampsand
brackishwetlandsof bothhemispheres, with
one species,Avicenniagerminans(L.) Stearn
(A. nitidaJacq.,A. tomentosa Jacq.nonWilld.),
blackmangrove, nativetotheUnitedStatesand
ourarea alongthecoastsof theFloridapenin-
sula and panhandle(northto St. JohnsCounty
along theAtlanticCoast and to Levy County
alongtheGulfCoast,withdisjunctlocalitiesin
Taylorand Franklin counties),theRio Grande
Delta,and in protected sitesin theMississippi
Delta regionand Coastal Bend of southern
Texas(Clewell;Johnston; Little,1976; Long&
Lakela;Moldenke,1980; Sherrod& McMillan;
Small;Wunderlin et al.). Avicenniagerminans
is the most widespreadof the Neotropical
species, occurringthroughout the Caribbean
basin,northern Brazil, and along the Pacific
coastfromcentralMexicotoPeru(Duke,1991;
Little, 1976; Moldenke, 1973; Tomlinson,
1986). If thespecies is interpreted to include
A. africana Beauv. (Compère; Duke, 1991;
Tomlinson, 1986),italso extendsalongthetrop-
icalAtlanticcoastofwestern Africa.Avicennia
is
germinans easilydistinguished fromall other
species by its largecorollas(10-15 mmlong
and wide). These are whitishwith a yellow
throat,tomentulose adaxially, andthemostcon-
spicuouslyzygomorphic. styleandstamens
The
areexserted. Avicenniagerminans occurssym-
patricallywithtwo otherNeotropicalspecies,
also withwhitishflowers:A. bicolorStandley
at scatteredlocalitiesfromsouthern Mexicoto
Colombia (corollas conspicuouslyzygomor-
phic and tomentuloseto glabrousadaxially
[less thanhalfthe size of thoseof A. germi -
nans],styles and stamens notexserted) andA.
SchaueranaStapf& Leechmanex Moldenke
fromthe Lesser Antilles,Brazil to Uruguay
(corollassimilarin size toA. germinans butnot
strongly zygomorphic [the lobes less distinctly
1997 SANDERS, AVICENNIACEAE 87

differentiated], glabrousadaxially,stylesand ers yellow,ovarypartiallyfourlocular) and

stamensincluded).UnlikeA. germinans, both sect.Hilairanthus(vanTieghem)Briq.(flow-
A. bicolor and A. Schauerana have spicate ers whitish,ovarypartiallytwo locular).My
inflorescence unitswithwell-separated nodes. observationssuggestthat the Indian-Pacific
AlthoughA. germinanscan be foundinter- species belongto the former, while all three
mixedwitheitheroftheotherspeciesat certain Neotropical-Atlantic speciesbelongtothelatter.
localities, no hybridshave been reported As an alternative, Tomlinson(1986) recog-
(Tomlinson, 1986). nized three informal groupsbased on flower
Geographically, the species ofAvicennia fall morphology: (1) the germinans type - distinctly
intotwo discrete,stronglyallopatricgroups: zygomorphic, withspatulatelateralandabaxial
theaforementioned Neotropical-Atlantic group lobes and a secondarily bilobedadaxial lobe,
(interpreted A.
broadly, germinans amphi- is lobes adaxially tomentulose, stamensandstyle
Atlantic) and an Indian Ocean-southwestern (branches) exserted or not and ascendingunder
Pacificgroup.All species of the lattergroup the uppercorollalobe (Avicenniagerminans ,
haveyellowororange,weaklyzygomorphic or A. bicolor,A. Schauerana)',(2) theofficinalis
actinomorphic, adaxially glabrous corollas. type - weaklyzygomorphic, withovate(basally
The most widely distributed species of this narrowed) lateral and abaxial lobes and a very
group are A. alba Blume (Pakistan to the weakly bilobed ovate-oblong adaxial lobe,
SolomonIslands),A. marina(Forsskâl)Vierh. lobes glabrousadaxially,thickand coriaceous,
(East Africa and the Red Sea, east to the stamensexsertedor not and erector weakly
SolomonIslands,and southto New Zealand), ascending(i.e., moreor less radiating), style
and A. officinalis (Pakistanto New Guinea) (branches)exserted ornotandascendingunder
(Duke, 1991; Tomlinson, 1986). uppercorolla lobe (A. officinalis and related
Avicenniais clearlydelimitedand somewhat Asian species); (3) the marinatype - actin-
isolated.However,species limitsare not as omorphic, lobes broadened basally (more or
clearcut.Moldenke(1960a,b, c) recognized 27 less deltate),glabrousadaxially,thickandcori-
taxa in 12 species,diagnosedlargelyby leaf aceous,stamensand style(branches)erectand
andinflorescence shape.However,in a detailed not exserted.The systematicsignificanceof
morphometric analysisof theAustraliantaxa, theseflowertypesis notclear,sincethetransi-
N. C. Duke (1990) reported leafshapeto vary tionseriesis notcorrelated directly withlength
withlightintensity andsalinity, andTomlinson of thestyleand degreeof insertion and exser-
(1986) had alreadyfoundMoldenke's criteria tionofthestamens.However,Tomlinson 's ger-
to be inconsistent and difficult to apply.Thus, minanstypecorresponds to sect.Hilairanthus,
Tomlinson (1986) andDuke (1991) recognized andthetworemaining typesto sect.Avicennia.
only ten and eleven taxa, respectively, in eight Detailed phylogenetic analysesareneededto
species.Further populational andmonographic evaluatethe relationships of the species. It
studiesareneeded,especially forthe neotropi- should be noted that the choice of outgroups
cal Atlanticspecies. vs.
(zygomorphic actinomorphic) will likely
Variousinfrageneric classificationsusing dif- have a profound effecton the rooting of any
ferentcriteriahave been proposed.Sections suchanalysisandsubsequentinterpretation.
Donatia (Loefl.) Schauer (= Avicennia)and Floral biologyvariesamongspecies and is
Upata (Rheede) Schauer are separated ori the characterized bya flexiblebreedingsystem. All
basis of stylelengthand internalcorolla-lobe speciesaredichogamous as a resultofprotandry,
pubescence (Schauer; Moldenke, 1960). haveflowersthatremainopenforseveraldays,
However, thesecharacters do notcorrelate well and offernectar.In Tomlinson 's germinans
withone another, withothercharacters, orwith flowertype(1986), andsomewhat less so inhis
and
geography, they have not been applied con- officinalistype, theanthers dehisce shortly after
sistently.Schauerplaced the typespecies,A. the corollaopens,and the lowercorollalobe
, in sectionUpata(perhapsfromcon- servesas a landingplatform
officinalis forstereo-orienting
fusionof thespecieswithA. marina),whereas short-tongued insects(presumably beesandwasps
Moldenkeplaced in it in sectionDonatia (= thatnestinthemangrove forest;theintroduced
Avicennia).Variation in thedevelopment ofthe honeybee is also thoughtto workmangrove
falsepartitions at thebase of theovarywas the flowers).The insect'sback is dustedwiththe
primarybasis for Briquet's classification. somewhatadherent pollen.The stylebranches
SectionEuavicenniaBriq.(= Avicennia ) (flow- subsequently spreadand becomereceptive. In

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88 HARVARDPAPERS IN BOTANY No. 10

theactinomorphic marina-type, a widerangeof ofa terminal hookthatreorients thegrowing tip

generalistpollinatorsis apparentlyattracted horizontally. Afterhorizontal growth is reestab-
(Clarke & Myerscough).The pollen is dis- lished,theybehaveas normalradialroots,pro-
playedonlyafterthefourcorollalobes reflex. ducingpneumatophores and anchoringroots.
Being strongly adherent, massesof pollenare The function of thesespecializedrootsis not
pickedup,presumably on theinsect'sabdomen. well understood (McCuster).
Thepollenreleaseandstigmareceptivity arealso The mechanisms bywhichthepropagulesare
moredistinctly separated in time (Tomlinson, dispersedby sea water have been studiedin
1986). Pollen:
ovule ratios are high
relatively detail in Avicennia germinans.Generally, the
(at leastinA. marina; Clarke& Myerscough). diasporeconsistsoftheentirefruit, thepericarp
Seed set is usually frequentin all species. of whicheitherremainsindehiscent or is par-
Althoughoutcrossingmechanismsare well tiallyforcedopenby thegrowthof thesingle,
developedin all species,thedata also suggest large, germinatingembryo.The fruitsfall
thattheplantsareself-compatible. Reducedfruit directly belowthetreeontomudor intobrack-
setoccursevenin theabsenceof geitonogamy. ish water,wherethe tidal fluxescarrythem
Wheretwoor morespeciesofAvicenniaoccur away.The pericarpis shedinoneortwoweeks.
together,floweringseasons are separated. Free-floating seedlingsoftenremainviablefor
Otherwise,flowering may extend year-round, 16 weeks or more. Rootingoccursin shallow
witha peakin thewetterorwarmerseason. water that is free of tidal disturbancefor
The genus is poorlyknowncytologically. 5-20 days (McMillan; Rabinowitz;Ridley;
Chromosomecounts are available only for Tomlinson, 1986).
Avicenniamarina(2n = 36, Subramanian; 2n = The community andappliedecologyofman-
64, 96, Dawson) andA. alba (2n = ca. 66). grovesin theUnitedStates(and in thecircum-
Mostof thesecondarycompoundsidentified Caribbeanregion)is reviewedby Craighead,
in Avicenniahave been extractedfromthe Walsh et al ., and West, and globally by
widespreadAsian species A. marina and A. Chapman.Mangrovehabitats aremostsensitive
officinalis.
Currently, thespeciesofAvicennia to andendangered byurban/industrial develop-
are known to synthesizeiridoids(aucubin, ment(Gill). However,local and regionallaws
geniposide, lamiide, and harpagide types; now regulateremovalof mangrovesin many
Königet al, Reddyet al.); freeand esterified areas,including southernFlorida.
triterpenic acids; triterpenesaponins; fatty The major economic benefit of Avicennia
acids;alkanes;a diversity ofphenolicacidsand derivesfromitscodominance withRhizophora
relatedcompounds;theflavones,velutin,lute- in mangroveswampswhereit stabilizescoast-
olin, orientin,and quercetin; quinones as lines, providesnutrients to nearshore environ-
idioblasticcrystals(lapacholand relatedstruc- ments, andservesas a nursery forcommercially
tures)and as phytoalexins; and quinolizidine important fishand shellfish.Presumably, it is
alkaloids(Hegnauer,Reddyet al.). also themajorsourceof nectarfor"mangrove
In additionto the anatomicalpeculiarities honey."In subsistence economies,itis used as
notedin the discussionof the family,"knee a sourceofpoles,charcoal,andtanning chemi-
roots"developin at least Avicenniamarina. cals. Extracts fromthebarkofA. germinans are
These arise vertically fromtypicalhorizontal used medicinally, primarilyforintestinal and
roots,and initiallytheyare indistinguishable vasculardisorders. The cookedseedsareeaten,
externally from pneumatophores. However, though said to be toxicwhenraw (Görts-van
unlikepneumatophores, theyelongatebymeans Rijn;Morton;Tomlinson, 1986).
References:
Alam,M. K., & B. M. R. Khatun.Avicenniaceae. Bessedik,M. Une mangrove à AvicenniaL. en
Fl.Bangladesh 31: 1-11.1986.* Méditerranée
occidentale
au Miocèneinférieur
et
Bâillon, H. Avicennieae.
Hist.PI. 11: 120, 121. moyen.Compt.Rend.Acad.Sci. Paris.II. 293:
1891. [One of five tribes("series") in the 469-472.1981.*
Verbenaceae; seealso88-90,92,93.] Bigazzi,M. The occurrence
of intranuclear
inclu-
Bakhuizenvan den Brink,R. C. Revisiogeneris sions in the Labiatae, Verbenaceaeand
Avicenniae. III. 29:
Bull.Jard.Bot. Buitenzorg Scrophulariaceae. 37: 269-292.1984.
Caryologia
199-226.1921. [Accordingto Wagenitz,
below,theseinclusions
Bentham, Gen.PI.
G.,& J.D. Hooker.Avicennieae. arerestricted
to theScrophulariales
(= Lamíales
2: 1160.1876.[Oneofeight ofVerbenaceae.] sensulato)anda fewother
tribes scattered
groups.]

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All use subject to JSTOR Terms and Conditions
1997 SANDERS, AVICENNIACEAE 89

Bird,E. C. F.Theconservation ofmangroves innorth- in southeastern Australia. Austral. Jour. Bot.39:

ernQueensland. N. Queensl. Nat.39: 6-8. 1971.* 283-293.1991.[Reproductive phenology, pollen:
Briquet,J. Verbenaceae. In: Engler & Prantl, ovuleratios, seedset.]
Nat. Pflanzenfam. IV. 3a: 133-182. 1895; Clewell,A. F. Guideto thevascular plantsofthe
Ergänzungsheft I (Nachträge II zumII-IV Teil): Floridapanhandle. 605 pp.Tallahassee, Florida.
64-67. 1900; Ergänzungsheft II (Nachträge III 1985.[Avicennia germinans , 252.]
zum TeilenII-IV): 307, 308. 1908. [Avicen- Compère, P. Thecorrect nameoftheAfro- American
nioideae, oneof sevensubfamilies, 181,182;A. blackmangrove. Taxon12: 150-152.1952.[Avi-
germinans(as A. tomentosa)illustrated; in cenniagerminans (L.) L. accepted ascorrectcitation
Nachträge II,Avicennia divided intotwosections.] forthisspecies, whichis broadly circumscribed.]
Cantino,P. D. The phylogenetic significance of Corner, E.J.H.Theseedsofdicotyledons. Vol.1.xii+
stornataand trichomes in the Labiatae and 311 pp. Vol. 2. (illustrations) viii + 522 pp.
Verbenaceae. Jour.ArnoldArb. 71: 323-370. Cambridge, London,NewYork,andMelbourne.
1990.[Avicennia withmostly diacytic andsome 1976.[Characters ofAvicennia notedin a brief
anomocytic stornata, subsessile glandswithhead characterization oftheVerbenaceae, 1: 276.]
composed mostly of morethanfourcells,non- Correll,D. S.,& H.B. Correll.FloraoftheBahama
glandular trichomes eitherunicellular oruniseriate Archipelago. Frontisp. + (50) + 1692pp.Vaduz.
multicellular.] 1982.[Avicennia germinans (illus.),1252,1253,
. Evidencefora polyphyletic originof the treated inAvicenniaceae.]
Labiatae. Ann.Missouri Bot.Gard.79: 361-379. Craighead,F. C., Sr. The treesof SouthFlorida.
1992. [Evidencefortwo separateclades,i.e., Vol.I.Thenatural environments andtheir succession,
Verbenoideae (= Verbenaceae sensustricto)vs. xviii+ 212pp.CoralGables, Florida. 1971.[Black
Viticoideae + Chloanthoideae + Caryopteridoideae mangrove, passim ; manyecologicalillustrations;
+ Labiataesensustricto (= Labiataesensulato).] extensive bibliography, including sectiononselected
, R. M. Harley,& S. J.Wagstaff. Genera of papers byJ.K. Small;Vol.II. notcompleted.]
Labiatae:status andclassification. Pp.511-522in Cronquist, A.Anintegrated system ofclassification
R. M. Harley& T. Reynolds, eds.,Advances in offlowering plants. Frontisp. + xviii+ 1262pp.
Labiatescience.Kew.1992.[GeneraofLabiatae NewYork.1981.[Verbenaceae subfam. Avicen-
sensulato(i.e.,including Verbenaceae withlater- nioideae, 920-924.]
allyattached ovules)listed, withindication ofsub- Dahlgren,u. ine lastDañlgrenogram. systemoi
family oralsotribe.] classification ofthedicotyledons. Pp.249-260in
Carlquist,S. Woodanatomy of thesympetalous K. Tan, ed.,The Davis and HedgeFestschrift.
dicotyledon families: A summary, withcomments Edinburgh. 1989.[Posthumous publication ofR.
on systematic relationships and evolution of the Dahlgren's most recent alterations of his
woodyhabit.Ann. MissouriBot. Gard. 79: angiosperm system;Avicenniaceae not listed;
303-332.1992.[Tabular summary ofcharacters of Lamialescombined withScrophulariales.]
woodanatomy; Avicennia marina(figs.44, 45); Dahlgren,R. A systemof classification of the
phenetic for
argument recognition of Avicennia- angiosperms tobe used to demonstrate thedistrib-
ceae on thebasisof woodanatomy andnarrow utionof characters. Bot. Not. 128: 119-147.
family concepts.] 1975a. [Avicenniaceae, 130;placedinCelastrales,
Chadwell,T. B.,S. J.Wagstaff, & P. D. Cantino. neartheSantalales.]
Pollenmorphology ofPhryma andsomeputative . The distribution of characters withinan
relatives.Syst.Bot.17:210-219.1992.[Avicennia angiosperm system. I. Someembryological char-
pollen illustrated and described; does not support acters. Ibid. 181-197. 1975b.
a closerelationship withPhryma .] . A revisedsystem of classification of the
Chapman, V.J.1939Cambridge University Expedi- angiosperms. Bot. Jour. Linn. Soc. 80: 91-124.
tionto Jamaica. - Part3. The morphology of 1980.[Avicenniaceae removed fromCelastrales
Avicennia nitida Jacq.andthefunction ofitspneu- butnotplacedelsewhere.]
matophores. Bot.Jour. Linn.Soc. 52: 487-533. Davis, G. L. Systematicembryology of the
1944.[Detailed description (illus.)ofstructure and angiosperms. x + 528 pp.NewYork,London, &
development of seedlings androotsystem; gas- Sydney. 1966.[Avicennia, 271,272; included in
exchange physiology ofroots.] Verbenaceae butitspeculiarities noted.]
. Ecosystems oftheworld. Vol.1.Wetcoastal Dawson,M. I. Contributions toa chromosome atlas
ecosystems, xi + 428pp.Amsterdam, Oxford, New of the New Zealandflora - 30 miscellaneous
York.1977.[Avicennia mentioned throughout.] species.New ZealandJour.Bot. 27: 163-165.
Chen,C.-F.,& H.-C. Lo. Pollenmorphology of 1989.[Avicennia marina, 2n = 64,96.]
mangrove species endemic to Taiwan. (InChinese; Duke, J.A. Keys for the identification ofseedlings
English summary.) Quart.Jour. Chin.Forestry 20: ofsomeprominent woodyspeciesofeightforest
85-89.1987.[Illustrations.] typesin PuertoRico.Ann.MissouriBot.Gard.
Clarke,P. J.,& P. J.Myerscough. Floralbiology 52: 314-350.1965.[Avicennia germinans, 315,
andreproductive phenology ofAvicennia marina fig• 166.]

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All use subject to JSTOR Terms and Conditions
90 HARVARDPAPERS IN BOTANY No. 10

. On tropicaltree seedlings.I. Seeds, Judd,W. S., R. W. Sanders,& M. J.Donoghue.

seedlings, systems, and systematics. Ibid. 56: Angiosperm family pairs:Preliminary phyloge-
125-161.1969. [Germination and seedlingsof neticanalyses. Harvard Pap.Bot.5: 1-51.1994.
Avicennia briefly described, 160.] [Verbenaceae sensustricto andLabiatae sensulato
Duke,N. C. Morphological variation in theman- (Cantino,1992) accepted;Avicenniaceae sug-
grovegenusAvicennia in Australia: systematic gested as member ofLabiatae.]
andecological considerations. Austral. Syst.Bot. Junell,S. ZurGynäceummorphologie undSystem-
3: 221-239.1990.[Multivariate analysis ofgenet- atikderVerbenaceen undLabiaten.Symb.Bot.
icallyand ecologically (lightintensity, salinity) Upsal. 4: 1-219. 1934. [Detailedcomparative
induced morphological variation.] anatomy ofgynoecia ofall tribes ofVerbenaceae
. A systematic revisionof the mangrove and Labiatae;Avicennia , 140-146,drawings of
genusAvicennia (Avicenniaceae) in Australasia. sections through ovaries, ovulesanddeveloping
Ibid.4: 299-324.1991.[Eight speciesrecognized, embryos; treated as subfamily ofLabiatae.]
fiveinAustralasia; maps,illustrations.] Khatum, B. M. R.,& M. K.Alam.Taxonomie stud-
Erdtman, G. Pollenmorphology andplanttaxon- iesinthegenus Avicennia Linn,from Bangladesh.
omy.IV. Labiatae,Verbenaceae, andAvicenni- Bangladesh Jour. Bot.16: 39-44.1987.*
aceae. Sv. Bot. Tidskr.39: 279-285. 1945. Kooiman, P.Theoccurrence ofiridoid glycosides in
[Avicennia illustrated; briefarguments forits theVerbenaceae. ActaBot.Neerl.24: 459-468.
placement ina separate familv.l 1975.[Survey of30 percent ofgenera; closesimi-
. Pollenmorphology and planttaxonomy. larity in iridoid typesamongtribes andwiththe
Angiosperms. (Corrected reprint ofthe1952edi- Labiatae; Avicennia notsampled.]
tionwithaddendum.) Frontisp. + xiv+ 553 pp. König,G., & H. Rimpler.Iridoidglucosides in
NewYork.1966. [Avicennia briefly described, Avicennia marina. Phytochemistry 24: 1245-1248.
treated under Verbenaceae, 448.] 1985.[First report forAvicennia ; phytochemistry
Everett, J. New combinations in the genus ofAvicennia reviewed.]
Avicennia (Avicenniaceae). Telopea5: 627-629. , , & D. Hunkler. Iridoidglucosides in
1994.[Twoatsubspecies rankunder A. marina .] Avicennia officinalis.Phytochemistry 26: 423-427.
Fahn,A., & C. Shimony. Development oftheglan- 1987.[Geniposide, lamiide, andharpagide iridoids
dularandnon-glandular leafhairsofAvicennia found.]
marina(Forsk.)Vierh.Bot.Jour. Linn.Soc. 74: KRISHNAMURTHY, K. v., & K. SlGAMANI. Wood
37-46. 1977. [Developmental pathways to the anatomy oftwoSouthIndian speciesofAvicennia.
subsessile saltglandsandthedavatetrichomes FeddesRepert. 98: 537-542.1987.[Verifies ear-
diverge lateinontogeny.] lierreports forother species.]
Gill,A. M. Mangroves: Is thetideofopinion turn- Little,E. L.,Jr.AtlasofUnited Statestrees.Vol.4.
ing?Fairchild Trop.Gard.Bull.26: 5-9. 1971. Minoreastern hardwoods. U.S. Dep. Agr.Misc.
[Economic significance and needforconserva- Pubi. 1342. v + 17 pp. + 230 maps. 1976.
tion;illustration.] [Avicennia germinans , maps17N& 17SE.]
Görts-vanRijn,À. R. A., ed. Verbenaceae. Fl. . Ibid.Vol.5. Florida.U.S. Dep.Agr.Misc.
Guianas.A. Phanerogams 4(148): 1-99. 1988. Pubi. 1361. vi + 22 pp. + 262 maps.1978.
[Floristics byM. J.Jansen- Jacobs,including A. [Avicennia germinans , map168.]
germinans ; woodanatomy byB. J.H. terWelle . Checklist ofUnited Statestrees(native and
& D. Détienne; Avicennia germinans, 88,89,figs. naturalized). U.S. Dep. Agr.ForestServ.Agr.
18-20.] Handb.541.iv+ 375pp.1979.[Avicennia germi-
Hegnauer,R. Verbenaceae. Chemotaxonomie der nans, 59.]
Pflanzen.6: 658-681. 1973. Addenda in & F. H. Wadsworth.Commontreesof
Nachträge6: 775-559, 792, 297. 1973; 9: PuertoRicoandtheVirgin Islands.Vol.1. U.S.
731-753.1991.[Systematic review ofsecondary Dep.Agr.ForestServ.Handb.249. x + 548 pp.
chemistry withinfamilyby chemicalclass; 1964. [Avicennia germinans (as A. nitida)in
Avicennia mentioned throughout.] Verbenaceae, illustrated,476,477.]
Howard,R. A. Avicenniaceae. FloraoftheLesser Long,R. W.,& O. Lakela. A floraof tropical
Antilles,Leewardand Windward Islands 6: Florida, xvii+ 962 pp.Miami.1976.[Avicennia
211-213.1989.[Avicennia germinans (illus.),A. germinans , 732.]
Schauerana .] Martin, A. D. Thecomparative internalmorphology
Jafri,S. M. H. Avicenniaceae. In: E. Nasir& S. I. of seeds.Am. Midi.Nat. 36: 513-660.1946.
Ali, eds.,FloraofWestPakistan 49: 1-4. 1973. [Avicennia, 608;embryo spatulate.]
[Avicennia marina illustrated.] McCuster,A. Knee rootsin Avicennia marina
Johnston, S. A.,Jr.Preliminary reportonAvicennia (Forsk.)Vierh. Ann.Bot.II. 35: 707-712.1971.
germinans communities locatedon Ile de Chien [Description of rootsthatarisevertically, bend,
(Dog Island),Franklin County, Florida.Trop. descend, andcontinue horizontally.]
Ecol.India24: 13-18.1983.[Coldtolerance inthe McMillan, C. Environmental factorsaffecting
likely northernmost population ofA. germinans .] seedling establishment oftheblackmangrove onthe

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1997 SANDERS, AVICENNIACEAE 91

central TexasCoast.Ecology52: 927-930.1971. handbook totheflora ofCeylon 4: 125-136.1983.

[Seedling establishment andgrowth is promoted [Avicennia marina , A. officinalis, colorphotos,
bywater depths lessthan5 cmandreduced turbu- extensive synonymy.]
lence,butnotbysalinity orhightemperatures.] Moran,R.Avicennia marina var.resinifera (Forst,f.)
Melchior,H. Avicennioideae. In: H. Melchior,A. Bakh.(Verbenaceae orAvicenniaceae). Madroño
Engler's Syllabus derPflanzenfamilien, ed.12.2: 437, 27: 143. 1980. [PlantsfromAuckland,New
438.1964.[Oneofeight subfamilies ofVerbenaceae.] Zealand(36°52' S) wereplanted ina wildlife pre-
Metcalfe,C. R., & L. Chalk. Anatomy of the servein MissionBay, San Diego, California,
dicotyledons. 2 vols,lxiv+ 1500pp.Oxford. (Cor- where they fruitedandformed a reproductive pop-
rected reprint.)1965.[Avicennia inandmentioned ulation ofabout100individuals, whichwerelater
throughout Verbenaceae, 1030-1053.] eradicated.]
& . Anatomy ofthedicotyledons, ed. Morton,J.F. Atlasofmedicinal plantsof Middle
2. Vol.2. xi + 297 pp. + 11 pls. Oxford. 1983. America, BahamastoYucatan, xxviii+ 1420pp.
'Avicennia pneumatophores, 134;wood, 46,86,198.] Springfield, Illinois.1981.[Avicennia germinans,
Moldenke, H.N.Materials toward a monograph ofthe 731,732.]
genus Avicennia. - I. Phytologia 7: 123-168. 1960a; Muller, J. Fossil pollen recordsof extant
-II. Ibid.179-232.1960b;-III. Ibid.259-293. angiosperms. Bot.Rev.47: 1-142.1981.[Earliest
1960c.[Lengthy forthe
argument recognition of the known record ofAvicennia from lowerMioceneof
Avicenniaceae; descriptions,key, extensivesynonymy thewestern Pacific.]
listsandcitation ofliteratureandspecimens.] Olmstead,R. G.,K. M. Scott,& J.D. Palmer.A
. Additional notesonthegenus Avicennia. - chloroplastphylogenyfor the Asteridae:
I. Ibid.14: 301-320.1967a;-II. Ibid.326-336. Implications fortheLamíales. Pp.19-25inR. M.
1967b;-III. Ibid.15: 71,72. 1968a;-IV. Ibid. Harley & T. Reynolds,eds., Advancesin
470-478.1968b;-V. Ibid.32: 343-370.1975a; Labiatescience.Kew.1992.[Verbenaceae sensu
-VI. Ibid. 436-457. 1975b;-VII. Ibid. 33: strictoandLabiataesensulatooccuron different
238-279.1975c;-VIII. Ibid.34: 70-94.1976a; cladeswithin theScrophulariales.]
-IX. Ibid. 167-203. 1976b; -X. Ibid. 36: & P.A. Reeves.Evidence torthepolyphyly
408-412.1977a;-XI. Ibid.439-450.1977b;- oftheScrophulariaceae basedonchloroplast rbcL
XII. Ibid.40: 406-413.1978;-XIII. Ibid.46: andndkFsequences. Ann.Missouri Bot.Gard.82:
193-199. 1980a; -XIV. Ibid.226-228. 1980b; -XV. 176-193.1995.[Additional samples support con-
Ibid 308-317.1980c. [Descriptions, synonymy clusions ofOlmsteadetal.]
listsandcitation ofliterature andspecimens.] Padmanabhan, D. The embryology of Avicennia
. Avicenmaceae. In: R. E. Woodson,Jr.,& officinalis. I. Floralmorphology and gameto-
R. W. Schery,Fl. Panama.Ann.Missouri Bot. phytes. Proc.IndianAcad.Sci. B. 52: 131-145.
Gard.60: 149-154.1973.[Avicennia bicolor, A. 1960.[Illustrations ofserialtransections offlowers;
germinans (illus.),andA. Tonduzii Moldenke (= A. development of micro- andmegagametophytes.];
bicolor).] - II. Endosperm. Phytomorphology 14: 442-451.
.A fifthsummary oftheVerbenaceae, Avicenni- 1964. [Illustrations of endosperm development
aceae,Stilbaceae, Dicrastylidaceae, Symphorema- andwhole,isolated micropylar haustoria, someof
ceae,Nyctanthaceae andEriocaulaceae oftheworld thelargest haustoria ofangiosperms.]; - III. The
as tovalidtaxa,geographic distribution andsyn- embryo. Jour. MadrasUniv.B. 32: 1S-19.1962.
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1971. [Lists of namesof taxa acceptedby identificación decampodelosprincipales arbores
Moldenke, andofsynonyms, including all ortho- tropicales deMéxico,vii+ 413pp.México.1968.
graphic variants anderrors, withcrossreference to [Avicennia germinans (illus.),368,369.]
correct names;distributions listedunder thepolit- Rabinowitz, D. Dispersaiproperties of mangrove
ical subdivisions fromwhichcollections were propagules. Biotropica 10: 47-57. 1978.[Flota-
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Avicenniaceae, Stilbaceae, Chloanthaceae, Sympho- Reddy, M. S.,C.VitayaKumari, & M.Radhakrish-
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synonymy. Phytologia Mem. 3: 1-629. 1980. chemistry, anatomy, embryology, andpalynology
[Distribution listreplacesandtheotherinforma- ofAvicennia-, phenetic argument forinclusion in
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& A. L. Moldenke.Avicenniaceae. In: M. Rico-Gray, V.Antsandtropical flowers. Biotropica
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All use subject to JSTOR Terms and Conditions
92 HARVARDPAPERS IN BOTANY No. 10

theabsenceofantsvisiting flowers ofspeciesof mentioned throughout, treated systematically as

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Stearn,W. T. A keyto WestIndianmangroves. Weiss,H. PrésenceďAvicenniaSchaueranaen
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Subramanian, D. Cytological studies ofsomeman- des palétuviers antillais.Biol. Écol. Méditer. 5:
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