BRIT Press

DISTRIBUTION AND MORPHOLOGICAL CHARACTERISTICS OF ARCEUTHOBIUM HONDURENSE

AND A. NIGRUM (VISCACEAE) IN MEXICO
Author(s): Robert L. Mathiasen, Shawn C. Kenaley and Brian P. Reif
Source: Journal of the Botanical Research Institute of Texas, Vol. 6, No. 2 (23 NOVEMBER 2012),
pp. 599-609
Published by: Botanical Research Institute of Texas, Inc.
Stable URL: http://www.jstor.org/stable/41972447
Accessed: 23-02-2016 07:17 UTC

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 DISTRIBUTION AND MORPHOLOGICAL CHARACTERISTICS OF
ARCEUTHOBIUM HONDURENSE AND A. NIGRUM (VISCACEAE) IN MEXICO

Robert L. Mathiasen Shawn C. Kenaley Brian P. Reif

ofForestry
School ofPlant
Department Pathology ofForestry
School
Arizona
Northern University andPlant-Microbe
Biology Arizona
Northern University
86011U.S.
Arizona
Flagstaff, A. Cornell
University Flagstaff, 86011U.S.
Arizona A.
NewYork
Robert.Mathiasen@nau.edu Ithaca, U.S.A.
14853 Brian.Reif@nau.edu
sck26@cornell.edu
ABSTRACT
The and
geographic host ofArceuthobium
distributions and
hondurense A.nigrum(Viscaceae) Mexico
insouthern andCentral have
America
remained intheir
duetodifficulties
unclear This
identification.study the
toclarify
wasconducted morphology, distribution,
phenology,
andhostaffinities dwarf
ofthese mistletoes.
Morphological were
measurements madeforthese across
species their distributions
geographic
and were
nrITSsequences andcompared
generated fromselected inMexico.
populations subtle,
Although interspecific inplant
differences
were
morphology found, and
A.hondurense A.nigrum bythe
canbedifferentiated oftheir
dimensions staminate staminate
spikes, flowers,
andfruits.
Ourdata
alsoindicated and
A.hondurense
that A.nigrumwere
not Arceuthobium
sympatric. from
isdistributed
hondurense north-
ern tonorthern
Nicaragua Oaxaca, and
Mexico A.nigrum from
isdistributed tonorthern
Veracruz A.hondurense
Although
Durango. andA.
nigrum in
floweredthe A.
fall, hondurense
consistently
peakedin and
September A. peaked
nigrum inOctober, into
extending in
January
Aspring
Mexico.
central period
flowering for
previously
reported wasnot
A.nigrum Additional
observed. onthe
information host
distribu-
andmolecular
tion dwarf
ofthese
differences isalsopresented.
mistletoes
KeyWords:Arceuthobium Arceuthobium
hondurense, dwarf
nigrum, mistletoe, ITS,molecular
hosts,
geography, identification,
parasitic
plants
RESUMEN
Ladistribución
geográfica yA.nigrum
hondurense
deArceuthobium (Viscaceae) enMexico
ydesushospedadores yCentro soninci-
América
ertas alosproblemas
debido Eneste
ensuidentificación. trabajo, lamorfología,
seestudió fenología, dehospeda-
yafinidades
distribución
deestas
dores enanos.
demuérdagos
dosespecies Lasmediciones
morfológicas hechas
fueron Mexicanas
depoblaciones ambas
para espe-
cies
ysegeneraron denrITS.Aunque
secuencias
ycompararon existen
ligeras, diferencias
interespecíficas delasplantas,
enlamorfología
yA.nigrum
A.hondurense sepuedendistinguir
por delasespigas
lasdimensiones flores
estaminadas, Nuestros
yfrutos. indican
datos que
estas nosesolapan
especies ensudistribución
geográfica. hondurense
Arceuthobium desde
sedistribuye deNicaragua
elnorte elnorte
hasta de
México,
Oaxaca, mientras desde
sedistribuye
queA.nigrum Veracruz elnorte
hasta México.
deDurango, Aunque florecen
lasdosespecies en
A.hondurense
elotoño, tiene
supicodefloración yA.nigrum
enSeptiembre supico
tiene enOctubre,
defloración hasta
extendiéndose Enero
deMéxico.
enelCentro Elperiodo quefue
defloración A.nigrum
para
previamente
reportado nofue
enlaprimavera observado
paraestaes-
pecie. adicional
información
Sepresenta sobreloshospedadores moleculares
lasdiferencias
ysobre entreestas demuérdago
especies enano.
Clave:
Palabras Arceuthobium Arceuthobium
hondurense, dwarf
nigrum, mistletoe, ITS,
hosts,
geography, molecular
identification,
parasitic
plants
ThegenusArceuthobium Viscaceae)
(Santalales: consistsof42species(Hawksworth & Wiens1996)thatare
aerialparasitesofPinaceaeorCupressaceae. Manyofthespecies, commonly knownas dwarf are
mistletoes,
recognized as seriousforest
pathogens (Hawksworth & Wiens1996;Mathiasen etal. 2008).Morphological
charactersconsistentthroughoutthegenusinclude smallflowers
produced onmaleandfemale leaves
plants,
reduced tosquamate scales,andmorphologicallysimilar fruits
bi-colored (Hawksworth & Wiens1996).The
genushaslongbeenconsidered difficult
a taxonomically groupbecauseoftheextreme reduc-
morphological
tionassociated withtheparasitichabitandthemorphological between
similarities species(Hawksworth &
Wiens1996).Factors thatcomplicate include
andidentification
classification a largeamount in
ofvariation
morphology andgeographic as wellas flowering
distributions periods thatoccasionally Twospecies
overlap.
thatexemplify theproblems associatedwithfield ofmorphologically
identification similar dwarfmistletoes
occurinsouthern andcentral Mexico:Arceuthobium Hawksw.
hondurense & Wiens(Honduran dwarfmistle-
toe)andA.nigrum Hawksw. & Wiens(blackdwarf mistletoe).

J.
Bot. Inst.
Res. Texas 599
6(2): -609.
2012

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All use subject to JSTOR Terms and Conditions
600 oftheBotanical
Journal Institute
Research ofTexas
6(2)

Arceuthobium hondurense wasoriginally described fromcentral Honduras (Hawksworth & Wiens1970)

andthought tobeextremely rare, evenontheverge ofextinction duetorapidandextensive ofits
harvesting
pinehosts(Hawksworth & Wiens1972).However, Honduran dwarf mistletoewaslaterfound tooccurfrom
northern Nicaragua,through muchofHonduras intoChiapas,Mexicoandasfarnorth ascentralOaxaca(Ma-
thiasen etal.2001;Mathiasen etal.2002a;Mathiasen etal.2003;Mathiasen etal.2006;Mathiasen & Melgar
2006).Although itlikely
occursinGuatemala, A.hondurense hasnever beenconfirmed there(Hawksworth &
Wiens1977;Mathiasen etal. 2003).Another dwarf mistletoe,originally describedas A.hawksworthiiWiens
andC.G.Shaw(Hawksworth's dwarf mistletoe),wasrecombined as a subspeciesofA.hondurense (Mathiasen
2007).Therefore, A.hondurense presently consistsoftwosubspecies: A.hondurense subsp.hondurensewhich
occursfrom Nicaragua northtoOaxaca,Mexico(Mathiasen etal.2010)andA.hondurense subsp.hawksworthii
(Wiens& C.G.Shaw)Mathiasen whichis primarily distributed in theMountain PineRidgeareaofBelize
(Mathiasen 2007),butalsohasbeenreported from centralHonduras (Mathiasen etal.2002b).
BecauseplantsofArceuthobium hondurense subsp.hondurense (hereafterreferredtoasA.hondurense)are
similar insizeandcolortothoseofA.nigrum , determining thegeographic distributionofthesespeciesin
southern Mexicohasbeendifficult (Hawksworth & Wiens1989,1996;Mathiasen etal. 2001,2002a,2003,
2010).Although A.nigrum wasthought tobedistributed from northern Durango, Mexicointosouthern Mexi-
co (Hawksworth & Wiens1996),itisnowthought tobedistributed onlyas farsouthas centralMexico(Ma-
thiasen etal.2010).Further,bothA.hondurense andA.nigrum produce redflowersthatbloominthefall.We
havecollected additionalmorphological dataforA.hondurense andA.nigrum since1998.Herewereport our
findings anddiscussthedistribution ofthesedwarf mistletoesinMexicobasedonourfield observations
and
morphological measurements. Becauseprior studies(Mathiasen etal.2003;Nickrent etal.2004)havesuccess-
fullyusedribosomal DNA(rDNA)sequenceinformation todiscriminate between A. hondurense andA. ni-
grum i,weconducted additionalanalyses oftheinternal transcribed spacer(ITS)region forseveralpopulations
ofbothspecies, particularly
populations incentral Mexicowhere thesespeciesmaybesympatric (Nickrentet
al.2004).Inaddition, becauseA.vaginatum (Willd.)Presisubsp.vaginatum (Mexican dwarf isalso
mistletoe)
morphologically similartoA.hondurense aswellasA.nigrum ,andoften confusedwiththem, wehaveprovided
information onhowtodistinguish thesespeciesfrom A.vaginatum. Theprimary objectiveofthisstudy,
how-
ever,wastoprovide additionaldataonhowtodiscriminate A.hondurense from A.nigrum - andviceversa -
andinso doing, better determine theirgeographic andhostranges. Morphological dataandITSsequences for
A.vaginatum weretaken from Hawksworth andWiens(1996)andobtained from GenBank, respectively.
ANDMETHODS
MATERIALS
Morphology andPhenology
To compare morphological characterswesampled16populations ofArceuthobium hondurense (twofrom
Oaxaca,Mexico, onefrom Nicaragua, and13from previous work byMathiasen (2007))and14populations of
A.nigrum from throughout itsgeographicrange(Fig.1).Plantsweremeasured from thetypelocality forboth
mistletoespecies(Hawksworth & Wiens1965,1970,1977)(Fig.1;locations 6 and23).Fromeachpopulation,
10-20maleand10-20female plantswerecollected
andthedominant shootfrom eachinfection wasusedfor
morphological measurements. Charactersmeasured werethoseusedbyHawksworth andWiens(1996)for
taxonomie classification
ofArceuthobium: basaldiameter,
height, thirdinternodelengthandwidth, andcolor
ofmaleandfemale plants;mature fruit width,
length, andcolor; seedlength,width andcolor;length andwidth
ofstaminate spikes;staminate flowerdiametersfor3-and4-merous flowers;
length andwidthofstaminate
flowerpetals;and,anther diameter andanther distancefrom thepetaltip.Plantsweremeasured within 24
hoursafter collectionusinga digital
caliperanda BauschandLomb7Xhandlensequipped witha micrometer.
Staminate spikeandflower measurements weremadeduring thepeakofanthesis andfruitandseedmeasure-
ments weremadeduring thepeakofseeddispersal.One-way ofvariance
analysis (ANOVA) wasusedtoexam-
inethevariance intheabovecharacters forA.hondurense andA.nigrum andsignificantdifferences between
meansweredetermined usinga Tukey's honestly difference
significant (HSD)post-hoc test(a = 0.05).Allsta-
tistical
analyses wereperformed usingJMP8.0.2software (SASInstitute,Cary,NC).

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Mathiasen
etalvArceuthobíum andA.nigrum
hondurense inMexico 601

1.Approximate
Fig. ofpopulations
locations sampledfor
Arceuthobíum
hondurense hondurense
subsp. (open inHonduras
circles) andMexico
andAnigrum
(dark inMexico.
circles) that
Populationsarenotnumbered
arelocations inHawksworth
reported andWiens(1996).Plant
material
from
locations
inbold
wereused nuclear
toobtain ribosomal
DNAinternal
transcribed
spacer
sequences A.hondurense
for andA.nigrum 2).Arceuthobíum
(Fig. hondurense
:
HONDURAS.Department 1- Cusuco
Cortes: National
Park;
Department 2- Celaque
Lempira: National
Park;DepartmentFrancisco
Morazan:
3-Lepa-
4- LaEstancia;
[RLM0136];
terique 6- 22km
5- Tatumbla; SEofTegucigalpa
onPan American
Hwy [RLM98107]; 7- 2kmSofValle
deAngeles;
8- 7.5kmSofValle
deAngeles;
Department 9- SanLucas.
ElParaiso: NICARAGUA.Nueva 10- Mozonte.
Segovia. 11- Chiapas:
MEXICO. SanCristobal
12- Oxchuc;
delasCasas; 13- 32km
Oaxaca: EofIxtlan 14- 15km
[RLM0994]; EofOaxaca [RLM0993];
City 15- Suchixtepec 16-21
[RLM0998];
km NEofTeotitlan - Arceuthobium
[RLM1086]. MEXICO.
nigrum: 17- Cofre
Veracruz: dePerote
[RLM0764];18- 3km SofSierra
deAqua[RLM1082];
19- Los
Puebla: 20- Tetla
Hermanos; deOcampo; 21- Los
Hidalgo: 22- Metepec;
Duraznos; Durango:23- 50km EofElSalto 24- 11
[RLM0778];
km EofElSalto 25- 3km
[RLM0779]; EofElSalto
[RLM11 26-23km
05]; NofRoute40onroadtoSanMiguel deCruces ];27- 102km
[RLM0781
NofRoute40onroadtoSan 28- Otinapa;
deCruces;
Miguel 29- 30kmWofSantiago 30- 18km
Papasquiaro; WofTepehuanes.

Becausethetimesofflowering
andseeddispersalforArceuthobium andA.nigrum
hondurense arepoorly
known(Hawksworth & Wiens1996),additionalobservations
ofthephenology ofthesetaxaweremadedur-
andfallof1999,2003,2005,2007,2008,and2010aswellas during
ingthespring theearly of2011.
spring
DNAExtraction andITS Sequencing
SamplesofDNAwereobtained from fiveandsixspecimens,eachrepresentinga geographically
separatepopu-
ofArceuthobium
lation, hondurenseandA.nigrum , respectively.
Localityandvoucher number foreachspeci-
men(boldprint)arepresentedinFig.1.Foreachspecimen, totalDNAwasextracted usingtheDNeasy™ Plant
MiniKit(Qiagen,Valencia,CA)according tothemanufacturer's DNApurity
instructions. andconcentration
foreachsampleusinga NanoDrop
werequantified ND-1000(Thermo Fischer Scientific,
Wilmington, DE).
ITSsequences
Full-length, (comprisingITS1,5.8SrDNAgene, andITS2)werePCR-amplified usingtheprimer
pair18S1830for
and26S40rev(Nickrent etal. 2004).PCRamplificationswerecarriedoutin25 pLreaction
mixturescontaining12.5pLof2XAmpliTaq Gold® Mix(Applied
Master Foster
Biosystems, CA),0.5pL
City,
ofeach20pMprimer, 11.25pLnuclease-free water,and-2-18ng(0.25pL of8-78ng/pL) ofgenomic DNA.

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602 Journal
oftheBotanical
Research
Institute
ofTexas
6(2)

PCRswereperformed inanEppendorf prothermal

Mastercycler® cycler(Eppendorf,Westbury, NY)withthe
following
cycling parameters: holdfor6 min.at95°C;5 cycles
initial at94°Cfor30s,55°Cfor30s,and72°Cfor
1min.;33cycles at94°Cfor30s,48°Cfor30s,and72°Cfor1min.;and,a final extensionstepof72°Cfor10min.
Blankreactions(i.e.,minusgenomic DNA)wererunconcomitantly tocheckforcontamination ofthereagents.
ThesizeofeachPCRproduct (bp)waschecked byultraviolet
separately fluorescence after1.2%agarose
gelelectrophoresisin0.5xTAEbuffer andstainingwithGelRed™ (PhenixResearch Products, Candler,
NC).
products
Amplification werepurified
directlyfromreactions
usingExoSAP-lT (0.4pLper''L ofreactionprod-
uct;USBInc.,Cleveland, OH)andnormalized to130ngpersequencing reaction.Sequencing wascarried out
DNA kit
usinga BigDyeterminators sequencing (Applied Biosystems),ABI3730 DNA sequencer, the
and
aboveforward andreverse primers.PCRproducts in
weresequenced bothdirections. Sequences wereproof-
readandassembled in CodonCode Aligner (CodonCode Corporation,Dedham, MA).Boundaries tothe5-
and3'-region
ofITS1andITS2,respectively, werepreviously
identifiedbyNickrent etal.(1994).ITSsequences
A.hondurense
for (n=5)andA.nigrum (n=6)produced inthisstudy
weredeposited inGenBank.
Phylogenetic Analysis
ITSsequences forArceuthobium hondurense andA.nigrum obtained inthisstudy andfrom GenBank (A.hondu-
renseAY2888263 and A. nigrum AY288271) as well as A. vaginatum subsp.vaginatum (AY288286and
AY288287) and A. douglasiiEngelmann (L25687;outgroup) were included in the dataset.
Sequences were
alignedusingClustalX ver. 2 etal. and
(Larkin 2007) visually edited as necessaryin CodonCodon Aligner.
Maximum Likelihood(ML)trees wereconstructed usingPAUP* 4.0bl0(Swofford 2003).TheDNAsubstitu-
tionmodelTIM2andtheparameter estimates fortreereconstructionweredetermined usingtheAkaike Infor-
mation Criterion(AIC;Akaike1974)as implemented injModelTest 0.1.1(Posada2008).Allnucleotides were
includedinthephylogenetic analysis;gapsweretreated as missing characters.Heuristic
searches wereper-
formed with200replicates ofrandom sequence additionandtreebisection-reconnection(TBR)branch swap-
ping.Branch supportwasevaluated using 1000 bootstrap and
replicates 10 random additionsofsequences per
Inter-
pseudo-replicate. andintraspecificgenetic distanceswerealsoexamined usingKimura's two-parameter
model(K2P;Kimura 1980)forbasesubstitution asimplemented inPAUP*.
Bayesian was
analysis also performed 3.1.2
usingMrBayes (Huelsenbeck & Ronquist 2001).Thebest-fit
model forDNA was
substitution determined as describedpreviously;however, Hasegawa-Kishino-Yano (HKY;
Hasegawa etal. 1985)modelandparameter estimatesweredetermined usingtheBayesian Information Crite-
rion(BIC;Schwarz 1978).Onecoldandthree heated Markov were and
chain(s) run, samples taken were every
100generations over5.0x 106generations. Thepotential scalereduction factor(PSRF)foreachofthemodel
parameterswas>1.0 whentheprogram wasterminated. wasaccessed
Stationarity byexamining theaverage
standard of
deviations splitfrequencies and likelihood values. Burn-in value(10%) was determined using
Tracervl.5(Rambaut & Drummond 2009).Theremaining treeswereusedtocalculate a 50%majority rule
consensus treeandtodetermine theposteriorprobabilities.
ANDDISCUSSION
RESULTS
Arceuthobiumhondurense
Ourmeasurements ofArceuthobium
hondurense indicateitforms largerplantsthanpreviouslyreported by
HawksworthandWiens(1970,1996);they reportedplantheightsaveraged approximately14cmwitha maxi-
mumheight of21 cm,butwemeasured plants(maleandfemale combined) thataveraged22 cm.Wefound
somemaleplantsinChiapas,Mexicothatwereover65cminheight (Table1).Thediscrepancyinmaximum
is
heights probably to
related Hawksworth and Wiens onlymeasuring specimens from centralHonduras
where were
plants generally smaller
than in southernMexico etal.
(Mathiasen 1999; Mathiasen 2007).The
meanbasaldiameterofdominantshootswasthesameas reported by Hawksworth andWiens (1996);ap-
5 mm.However,
proximately wemeasured someshoots withbasaldiameters ofnearly13mm,whileHawk-
sworth a maximum
andWiens(1996)onlyreported of9 mmforthischaracter. Themeansandranges formost
oftheremaining characters
morphological were similarto those
previously (HawksworthWiens
reported &

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Mathiasen
etal.,Arceuthobium
hondurense
andA.nigrum
inMexico 603

Table
1.Morphological
measurements
for
Arceuthobium and
hondurense
A.nigrum.
Dataare
listed
asmean Means
[n].
(range) followed
different
by capital
inthe
letters same
row
were different
significantly aTukey's
using HSD (a= 0.05).
test
post-hoc Lower
case inbrackets
letters indicate sizes
sample listed
already
inthe
same
column.
Plant incm
heights and
allother inmm.
measurements
Character A.hondurense A.nigrum
Plant
Height
Male 24.9A(11.5-66.4)
[160a] 24.3A(10.3-53.5)
[130a]
Female 18.6A(9.1
-33.1
) [a] 19.6A(9.3-37.2)
[a]
Basal
Diameter
Male 5.1A(2.8-1
3.4)[a] 7.0B(4.4-1
2.5)[a]
Female 5.4A(2.8-1
2.8)[a] 7.8B(4.1
-13.1) [a]
LengthofThird
Internode
Male 16.1A(6.6-34.0)
[a] 16.8A(11.6-28.7)
[a]
Female 13.8A(6.3-32.0)
[a] 16.5B(11.8-31
.8)[a]
WidthofThird
Internode
Male 3.8A(2.0-8.0)
[a] 4.9B(4.0-7.8)
[a]
Female 4.0A(2.0-1
0.0)[a] 5.5B(4.4-9.6)
[a]
Staminate
SpikeLength 14.3A(6.1
-17.9)[1
20b] B
20.6 (8.1
-33.3)
[200
b]
Staminate
SpikeWidth 1.7A(1.3-2.4)
[b] 2.9B(2.4-3.3)
[b]
MeanFlowerDiameter
3-merous 2.5A(2.0-3.0)
[80] 3.2B(2.7-4.0)[100c]
4-merous 3.1A(2.8-3.4)
[40] 4.8B(3.6-5.4)[c]
Petal
Length 1.3A(1.0-1
.6)[b] 1.7B(1.3-2.3)[b]
Petal
Width 1.2A(0.8-1
.4)[b] 1.4B(0.8-1
.9)[b]
AntherDiameter 0.5A(0.4-0.6)
[b] 0.8B(0.5-1
.1) [b]
AntherDistance
from
Tip 0.3A(0.2-0.6)
[b] 0.5B(0.3-0.6)[b]
Fruit
Length 5.3A(5.0-6.0)
[100c] 6.9B(5.2-8.8)[c]
Fruit
Width 3.4A(2.8-4.2)
[c] 4.1B(3.4-5.0)[c]
SeedLength 3.1A(2.8-3.5)
[c] 3.1A(2.7-3.9)[c]
SeedWidth 1.5A(1.3-1
.7)[c] 1.5A(1.3-1
.9)[c]

1970,1996)withtwoexceptions: thefruits andpetals.Themeansforeachofthesecharacters weregreater

thanthatfound by Hawksworth and Wiens (1996).The means formale and female thethird
plantheights,
internodelength ofmaleplants,and seed length andwidth were not significantly but
different, the means of
theremaining characters
wemeasured (e.g.,width of thethird internode and staminate spikelength and
width)weresignificantlydifferent between A. hondurense andA. nigrum (Table1).Ourmeasurements of
4-merousflower diametersofA.hondurense (n=40)werethefirst reportedfor this character.
Animportant andconsistent characterexhibited byArceuthobium hondurense wasthedarkredsurface of
theadaxialsideofpetalsreported by Hawksworth and Wiens (1970,1996), which was characteristic
ofthis
speciesthroughout itsgeographic range.Another characteristicofA. hondurense thatweobserved, andre-
portedby Hawksworth and Wiens (1970,1996), was thatthelower nodes of older were
plants oftenswollen
andround, thiswasparticularly
evident onold,maleplants. Hawksworth andWiens(1970)indicated thatthe
stigmason female flowers
and fruits ofA. hondurense were exserted as much as 0.5 mm. While we observed
thischaracteronmany femaleplants,wealsoobserved manyflowers andfruits without exerted
stigmas,sug-
that
gesting thischaracteristic
was polymorphic forA. hondurense. the
Similarly, nectary ofA.hondurense was
occasionallythree-lobed
as reportedby Hawksworth and Wiens (1996),but again this was
characteristic in-
consistent.
Arceuthobium hondurenseflowered from lateAugust toNovember withitspeakflowering period inmid-
orlate-September, seed
dispersing atapproximately the same time. Thisis consistent with whatHawksworth
andWiens(1996)reported, exceptwefound thatinsomeyears itfloweredwellintoNovember, which theydid
notobserve.

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604 Journal
oftheBotanical Institute
Research ofTexas
6(2)

Previously, Mathiasen etal. (2003)listedthepinesparasitized byArceuthobium hondurensein Central

America andChiapas,Mexico. Ourobservations support their
findings,
exceptthat
A.hondurense alsoparasit-
izedPinusteocote SchiedeexSchlechtendal & Chamisso incentral
Oaxaca.Although wehaveonlyobserved
A.hondurense infectingthispineinonelocation north ofIxtlan(Fig.1,location
13),thelevelofinfection
(>
90%)indicated Pinusteocotewasa principal host.Thispopulation wasmisidentifiedas A.vaginatumsubsp.
vaginatum byHawksworth andWiens(1996),asourmorphological andITSanalyses indicated
thispopulation
wasindeedA.hondurense. Mistletoe plantsonP.teocote atthislocation
weredarkbrowntoblack,similar in
colortoA.vaginatum ,butmaleplants inthefallproducing
flowered darkredflowers. Largemaleplantsatthis
localityalsohadswollen nodesandparasitized P.tecunumanii EguiluzetJ.P.Perry,
a principal
hostofA.hon-
durense elsewhereinsouthern Mexico(Mathiasen etal.2003).Inaddition,A.hondurensewasfound parasitiz-
ingP. lawsoniiRoezlex Gordon & Glendiningin central andnorthern Oaxaca.Although Hawksworth and
Wiens(1977,1996)reported A.hondurense (butidentifiedasA.nigrum) Pinus
parasitizing oaxacanaMirovand
P.patulaSchiede exSchlechtendal & Chamisso inChiapas, wedidnotobserve thesehost-mistletoe
combina-
tionsduring ourfieldworkinsouthern Mexico.

Arceuthobium nigrum
Arceuthobium nigrum ismorphologically very similar toA.hondurense. Bothspeciesproduced relatively
large,
darkbrown toblackplantsontheir pinehosts (Hawksworth & Wiens 1996).Maleandfemale ofA.ni-
plants
grum averaged nearly 25and18cminheight, respectively,butwerenotsignificantly largerthanA.hondurense
(Table1).Itis difficult
tocompare our resultsforplantheights with thoseofHawksworth andWiens(1996)
becausethey a of for
onlyprovidedrange heights nigrum A. (15-35cm, maximum = 45 cm).However, thelarg-
estplantwemeasured forA.nigrum wasa maleover53cmtallfrom Mexico.
Puebla, We also foundthatthe
basaldiameter ofshoots averaged two-mm larger (7.6mm) than thatpreviously reported (5 mm, Hawksworth
& Wiens1996)witha maximum basaldiameter nearly twicethatdescribed byHawksworth andWiens.Mea-
surements ofthethird internode widthsalsoindicated thatA.nigrum produced thicker plants(about5 mm)
than what Hawksworth and Wiens reported 4
(about mm). The means for
the basal diameters ofmale(7 mm)
andfemale plants (7.8mm)andthird internode widths ofA. were
nigrum significantly than
greater thosefor A.
hondurense (Table1).Furthermore, themeanlength ofthethird internodeoffemale plantsofA.nigrum (16.5
mm)wassignificantly longer thanthoseofA.hondurense (13.8mm), butnotthemeanlength ofthethird inter-
nodeofmaleplants.
Theonlyflower characteristicsHawksworth andWiensreported forArceuthobium nigrum wasthediam-
eterof3-merous flowers(3.5mm),which wasslightly largerthanthemeandiameter forthe3-merous flowers
wemeasured (3.2mm).Ourobservations indicated that A.nigrum commonly produced 4-merous flowersalso,
thus,wesampled theseflowers andfound theyaveraged nearly5 mmindiameter (Table1).Collectively, the
meandiameters of3 and4-merous flowersofA.nigrum weresignificantlylargerthanthoseofA.hondurense.
Petalsizeswerealsorelatively largeforA.nigrum whencompared toother dwarf mistletoes (Hawksworth &
Wiens1996).Wefound petalslonger than2 mmandnearly aswide,bothsignificantly larger thanthosefor A.
hondurense (Table1).Another keycharacteristic ofA.nigrum flowers thatwasconsistent throughout itsgeo-
graphicrange, wasthattheadaxialsurface ofitspetalswasdarkred.Whilethischaracteristic waseasilyob-
served,andissimilar toflowers forA.hondurense, a review oftheliterature(Hawksworth & Wiens1989,1996)
onA.nigrum revealed thatthepetalcolor, as a diagnostic character, hadnever beenmentioned before. The
reasonsforthisomission remain unclear.
Fruits ofArceuthobium nigrum wereremarkably glaucous andlargecompared toother dwarf mistletoes.
Themeanfruit lengthwasnearly 7 mm,whichiswhatHawksworth andWiensreported. However, wefound
8.8mminlength
fruits compared to9.0mmbyHawksworth andWiens(1996).Incontrast, theaverage width
offruitsweexamined waslarger (4.1mm)thanthatreported byHawksworth andWiens(3.5mm).Wemea-
suredseedsthatwereshorter, butwideronaverage thanthoseexamined byHawksworth andWiens(1996).
Themeansforfruit lengthandwidth ofA.nigrum weresignificantly largerthanthoseofA.hondurense ,how-
ever,themeanlength andwidth ofseedsweresimilar forbothspecies(Table1).

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Mathiasen
etal.,Arceuthobium
hondurense inMexico
andA.nigrum 605

Thephenology ofA.nigrum requiresadditionalobservationsaswewereunabletoconfirm theincidence

oftwoflowering periods- oneinMarch-April andoneinSeptember-October - as reported previouslyby
Hawksworth andWiens(1989,1996).Weexamined maleplantsofA.nigrum atseveral inmid-to
localities
late-March during 2003,2005,and2007as wellas inearly April2011andnever observed openflowers. Fur-
thermore, staminate flowers didnotappeartobeapproaching anthesis inlateMarchorearly April. Ourfield
observations,however, indicated thatitflowersbeginninginmid-September andcontinued intoNovember in
Durango, Mexico, whileincentral Mexico, A. nigrum flowers inlate-September andcontinued intoatleast
January.Peakflowering wasinearly October inDurango; however, thepeakflowering periodincentral Mex-
icoisstillpoorlyunderstood. Seeddispersal inearly
initiated and
September peaked inmid-October continu-
ingtomid-November inDurango andelsewhere incentral Mexico.
Ourfield observations ofpinesinfected byArceuthobium nigrum inMexicodidnotreveal anyadditional
hosts.Theprincipal hostsofA.nigrum inDurango wereclearly PinusleiophyllaSchiede exSchlechtendal &
Chamisso, P.lumholtziiB. L. Robinson & Fernald, P.teocote
, andP.chihuahuana as
Engelmann reported by
Hawksworth andWiens(1996).Thismistletoe alsobeenreported torarelyinfectP.arizonicaEngelmann and
P.cooperiBlancoinnorthern Mexico(Hawksworth & Wiens1996),butwehavenotobserved itontheseinfre-
quent hosts.In centralMexico its host
principal was P.teocote.PinuspatulaSchlechtendal & Chamisso wasa
secondary hostat severallocationsin Hidalgo and Puebla.While we agree with the classification
ofP.pseu-
dostrobusLindley as anoccasional hostofA.nigrum (Hawksworth & Wiens1996),wewereunabletoverify
whether P.montezumae A.B.Lambert wasalsoanoccasional host.Moreover, wedidnotobserve anyP.mont-
ezumae at the locationwhere Hawksworth and Wiens reported an infestation
of A. in
nigrumHidalgo norin
Veracruzwhere wefound large, P.
mistletoe-free montezumae growing nearP.teocoteseverely-infectedA.
with
nigrum. the ofP.
Therefore,susceptibilitymontezumae nigrum toA. needs further
study.Although Hawksworth
andWiens(1989,1996)reported thatbothP.lawsoniiandP.oaxacana Mirov wereprincipal hostsofA.nigrum ,
thishostsusceptibility wasbasedoninfection
classification ofthesepinesbyA. hondurense inOaxacaand
Chiapas,respectively (Mathiasen etal.2003).
DNAAnalyses
DNAsequence analysisdemonstrated thatArceuthobiumhondurense ,A.nigrum ,andA.vaginatum occurred in
threewellsupported clades(Fig.2).Allsamples identified
morphologically as A. hondurenseandA.nigrum
yieldeda 627and623bpfragment, consisting
respectively, ofthe3'endofthe18S(4bp),complete ITS1-5.8S-
ITS2sequence (604and600bp),andthe5'endofthe26S(19bp).Fouroffive sequences forA.hondurense were
(meanK2Pvalue=0.0017);
identical however,RLM98107differed byanA/Gnucleotide change atpositions22
and40 inITS1.Similarly, ITSsequences forA.nigrumwerenearly identical(meanK2Pvalue=0.0018);except
forA/Tnucleotide changes atposition 508inITS2.Thealignment forphylogenetic analysesconsisted of649
charactersincluding thoseofA.douglasii andA.vaginatum. Ofthesecharacters, 574wereconstant, 50 were
parsimony-informative, and25wereparsimony-uninformative. Thecombined, MLandBayesian consensus
treesupported three clades(Fig.2) withbootstrap
distinct values>98%andposterior valuesequal
probability
to 1.00,respectively.Eachplantidentified accordingtomorphometric dataas A. hondurense orA. nigrum
formed a distinctcladewitheither A.hondurense (RLM0136,Nickrent etal. 2004)orA.nigrum (DLN2019,
Nickrent etal. 2004).Sequences ofA. nigrum differed
from thoseofA. hondurense andA.vaginatum byap-
proximately43nucleotides (meannucleotide = 43.07,
difference meanK2Pvalue=0.0775). Likewise,themean
number ofnucleotide changes between A.hondurenseandA.vaginatum was13.0(meanK2Pvalue=0.0224).
Nickrentetal.(2004)reported that mayoccurinVeracruz
A.hondurense basedonmolecular data(GenBank
accessionno.L25693;voucher DLN2018),butourresults didnotsupport this.Plants southofSierra
collected
deAqua(RLM1083), theapproximate location
where Nickrentcollected DLN2018(D.Nickrent, pers.comm.),
weremorphologically similartothoseofA.nigrum. Assuspected, theITSsequences generatedfromRLM1083
wereidentical toL25693(datanotshown). However,ina separate phylogenetic analysis(datanotshown),
thesecollections/sequences wereunrelated toA.nigrum (AY288271) as wellas GenBank accessionsofA.du-
rangenseHawksw. & Wiens, A.gillii
Hawksw. & Wiens,A.hondurense ,andA.vaginatum. Nickrentpreviously

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606 Research
oftheBotanical
Journal Institute
ofTexas
6(2)

Fig.
2.Fifty-percent
(50%) consensus
rule
majority treebased
onmaximumlikelihood
and
Bayesian
analyses
using ITS
nuclear ofArceuthobium
sequences
A.vaginatum
A.hondurense,
nigrum, subsp. and
vaginatum, the A.douglasii.
taxon,
outgroup Representative ofA.nigrum
sequences A.hondurense
and
usedinNickrent inbold.
etal.(2004) for
SequencesA.douglasii
andAvaginatum
ssp. were
vaginatum obtained
from
GenBank([]=accession
number).
Collector arefor
abbreviations Robert
L.Mathiasen andDaniel
(RLM) L.Nickrent and
(DLN) precede
assigned numbers
voucher followed
bylocality
(department/state *= type
- country; Numbers
locality). above branches
indicate
PAUP values
bootstrap >60% 103
(after numbers
replicates), below
areBayesian >0.90
probabilities
posterior 5.0x106
(after generations).

Table
2.Principal and
morphological characteristics
physiological Arceuthobium
distinguishing A.nigrum
hondurense,,and
A.vaginatum
subsp. All
vaginatum.
measurements
inmm
and inparentheses.
ranges Data
for
A.vaginatum
from
Hawksworth
andWiens
(1996).
Character A.hondurense A.nigrum A.vaginatum
MeanBasalDiameter8 5.3(2.8-12.8) 7.4(4.1-13.1) 7.0(4-20)
MeanWidthofThird a
Internode 3.9(2.0-8.0) 5.2(4.0-9.6) 5.0(2.8-8.5)
Swollen
nodesatbaseofolder
plants Yes No No
Staminate
Spikes
Secondary
Branching No No Yes
MeanWidth 1.7(1.3-2.4) 2.9(2.4-3.3) 2.0(1.5-2.5)
Mean Flower
Diameter
3-merous
flowers 2.5(2.0-3.0) 3.2(2.7-4.0) 3.5b
4-merous
flowers 3.1(2.8-3.4) 4.8(3.6-5.4) 4.5b
Redflowers Yes Yes No
Mean Petal
Length 1.3(1.0-1.6) 1.7(1.3-2.3) 1.6b
Mean Petal
Width 1.2(0.8-1.4) 1.4(0.8-1.9) 1.1b
Mean Fruit
Length 5.3(5.2-6.0) 6.9(5.2-8.8) 5.5b
Mean Fruit
Width 3.4(3.1-4.2) 4.1(3.4-5.0) 3.5b
Anthesis Aug-Nov Sep-Jan Mar-Apr
SeedDispersal Aug-Sep Sep-Oct Aug
a- Male
andfemale
plantscombined.
b- Norange inHawksworth
provided andWiens
(1996).

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 etal.,Arceuthobium
Mathiasen hondurense
andA.nigrum
inMexico 607

DLN2018(L25693)as either
identified A.vaginatum etal. 1994)orA.hondurense
(Nickrent etal.
(Nickrent
2004).Thespeciesidentity (RLM1083andDLN2018),therefore,
ofthismistletoe remains and
unresolved
further
requires study.
SUMMARY
Although Arceuthobium hondurense ,A.nigrum , andA.vaginatum aremorphologically similar andoften diffi-
culttodistinguish from eachother insitu,there areseveral diagnostic characteristics that canbe used to iden-
tifythem incentral Mexicowhere they maybesympatric. Ourresults support theclassification ofthesetaxa
as distinctspecies and the principal and
morphological physiological characters that can be used todistin-
guish these species aresummarized in Table 2. While the overall height of male and female plantsandtheir
colorcannot beusedtoeasilyseparate thesespecies, A.hondurense isa moreslender plant bothA.nigrum
than
andA.vaginatum. Italsohasswollen, rounded nodes, particularly near thebase of older plants.Thischaracter-
isticismostevident onolder, maleplants. Incontrast, A.nigrum andA.vaginatum lackswollen, rounded nodes
nearthebaseofplants.
Another keycharacteristic ofA.hondurense thatseparates itfrom theother dwarf mistletoes is thewidth
ofitsstaminate spikes. While the length of staminate spikes often is too variable to be of anydiagnostic value,
thewidth ofthestaminate spikesofA.hondurese arethinner (mean1.7mm)compared tothoseofA.nigrum
(2.9mm)andA.vaginatum (2.0mm).Furthermore, thestaminate spikesofA.nigrum andA.hondurense gener-
allydo notform secondary branches, while those ofA. vaginatum typically do.
Arceuthobium hondurense primarily forms 3-merous flowers, andoccasionally 4-merous flowers, butA.
nigrum A.
and vaginatum commonly form both 3- and 4-merous flowers. Although the adaxial surface ofpetals
ofmaleflowers for A.hondurense andA.nigrum isdistinctively darkred,the3-merous flowers ofA.hondurense
aresmaller (2.5mm)onaverage thanthoseofA.nigrum (3.5mm).Thecolorofmaleflower petalsofA.vagina-
tum, however, isdarkbrown togreen. Whilethefruits ofbothA.hondurense A.
and nigrum areusually mark-
edlyglaucous, thefruits ofA.nigrum arelarger thanthoseofA.hondurense aswellasA.vaginatum . Addition-
ally,A.hondurense andA.nigrum primarily flower from lateAugust through September andOctober, butA.
vaginatum flowers from Marchthrough April(Hawksworth & Wiens1965,1996).Additional observations of
A.nigrum arestillnecessary todetermine ifitflowers in thespring as reported byHawksworth andWiens
(1989,1996).Ourobservations ofA.nigrum overmultiple seasonsandyearsinDurango, Mexico, donotsup-
porta spring flowering periodforA.nigrum. Furthermore, ouranalyses confirm thatthesespeciescanbe
readily distinguished usingITS-rDNA sequences aspreviously demonstrated byNickrent etal.(1994,2004).
Thehostspecificity ofthesemistletoes mayhelpseparate them, depending onthelocality inMexico. In
Durango, Arceuthobium nigrum andA.vaginatum bothparasitize P.teocote ,butP.teocote islesssusceptible toA.
vaginatum (a secondary host)(Hawksworth & Wiens1996).Moreover, A.vaginatum doesnotparasitize P.
,
leiophylla P. lumholtzii,nor P.chihuahuana ,which are allhighly susceptible toA. nigrum. In centralMexico, the
principal hostofA.nigrum isP.teocote ,butP.patulaisalsoinfected byA.vaginatum there. NowthatA.hondu-
rense hasbeendiscovered severely infecting P. teocote in Oaxaca, Mexico, infection of this pine cannot beused
todistinguish A.nigrum from A.hondurense, sincethesemistletoes bothflower inthefall, haveredflowers, and
aresimilar insizeandcolor. Thewidth ofinternodes andstaminate spikes, therefore, arelikely thebestchar-
acters fordistinguishing between them. Thesizeof3-merous flowers, petals,andfruits willalsoassistindis-
A.
tinguishingnigrum (larger flowers and fruits) from A. hondurense (Table 2).
Basedonourfieldobservations andmeasurements ofplantcharacteristics ofthedwarf mistletoes in
southern Mexico, wedo notagreethatArceuthobium nigrum orA.vaginatum occurin OaxacaorChiapas.
Thesespecies areprimarily distributed alongtheCentral Volcanic Cordillera ofcentral Mexicoandnorth into
Durango. Arceuthobium vaginatum extends as far north as central Chihuahua in the Sierra Madre Occidental
andasfarnorth assouthern Coahuila intheSierra MadreOriental (Hawksworth & Wiens1996).However, the
geographic distribution ofA. nigrum is centered on the eastern side of the Central Cordillera and extends north
intoDurango (Fig.1).Arceuthobium vaginatum issympatric withA.nigrum incentral Mexico(Hawksworth &

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All use subject to JSTOR Terms and Conditions
608 Journal
oftheBotanical
Research
Institute
ofTexas
6(2)

Wiens1996)andsinceitalsoextends as farnorth as Chihuahua, itis probablysympatric withA.nigrum in

Durango.
Honduran dwarf which
mistletoe, wasoncethought tobenearextinction (Hawksworth & Wiens1972),
isnowknown tobedistributed
from northern Nicaragua tonorthern Oaxaca,Mexico(Fig.1).Oursurveys in
2010confirmed thatArceuthobiumhondurense occurs innorthernOaxaca(Fig.1,location 16),sowenowknow
thisspeciesoccursalmosttoVeracruz andPueblain central Mexico.Moreover, ithasonlybeenfound in
smallpopulations
widely-scattered, throughout itsgeographicrange andtherefore,should notbeconsidereda
common parasiteofitspinehosts.Itshouldalsobenotedthatthereports ofA.nigrum inGuatemala andEl
Salvador(Hawksworth & Wiens1977,1989,1996)shouldbeconsidered as reports
ofA.hondurense. Inaddi-
tion,sinceourresultsdemonstrated thatatleastoneofthepopulations ofA.vaginatum from north-central
Oaxacawasmisidentified byHawksworth andWiens(1996)andisindeed A.hondurense (Fig.1,location
13),
wesuspect thesouthern distribution
ofA.vaginatum onlyextendsinto Puebla and notOaxaca. Further
inves-
however,
tigations, arewarrantedtoassesswhether A.vaginatum occurs inOaxacaasseveral collections
ofthis
specieshavebeen made intheSierraJuárez near Ixtlan.
While allof thesewere classified
as A. vaginatum
by
Hawksworth andWiens(1996,page370),wesuspect thesecollections representadditional
populationsofA.
hondurenseinOaxaca,butthisneedstobeconfirmed.

ACKNOWLEDGMENTS
Thefield
assistance
provided
byCarolyn
Daughertyandearlier
reviews
ofthemanuscript
byCarolynDaugh-
Dan and are
erty, Nickrent, JobKuijt greatly We
appreciated. also thehelpofGustavo
appreciate Socorro
Perez,
andJuanTunGarrido
Gonzalez-Elizondo, withreviews
andSpanishtranslation
fortheResumen.

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