This article isThis article by protected copyright. All rightsreserved. 10.1111/plb.12900 doi: differences to lead between the of thisversion citethisarticle and asVersion Record.Please cop been throughthe This article acceptedhas been for publication andundergone fullpeer review buthasnot e author’s Corresponding author Corresponding 2 Rí Bariloche, 1 C. AmicoGuillermo Forest Analysis Macroscale Byers Dr.Diane Editor: handling Paper :Research Article type 0000 ID: (Orcid AMICO GUILLERMO DR.
AcceptedIL 62901 Carbondale, University, Illinois Southern Biology, Plant Departmentof Comahu del Nacional (Universidad INIBIOMA CONICET Laboratorio Ecotono, Article
o Negro, Argentina Negro, o 1* , Daniel L. Nickrent L. , Daniel
yediting, pagination andproofreadingtypesetting, process,may which -
mail address of Mistletoe of
:
guillermo. - 0002 2
and Rominaand Vidal
Host Ranges Ranges Host - 3709 amico@ - 3111) comahue
-
Russell i n the Andean n the - conicet.gob.ar 1
- e) Quintral 1250, 1250, e) Quintral -
Patagonian Patagonian 6509
This article isThis article by protected copyright. All rightsreserved. Accepted trees shrubs and herbs, annualperennial or including habits growth different many plantsexhibit These heterotrophic onwards). 1997 12 times (Nickrent independently evolved INTRODUCTION KEYWORDS Article ABSTRACT Parasitic angiosperms Parasitic angiosperms
conversely less diverse regions would have more specialized mistletoes. mistletoes. morehave would specialized less regions diverse conversely ranges have large host also would ranges large geographic with mistletoes predicted specialists than ranges smaller geographic data Our in overlap low is there sympatric, the of mistletoe are species many families. and genera several species from host six more than parasitizing Notanthera (Loranthaceae) All specificity. degrees of varying these that results show Our distribution geographical By Santalaceae). and Misodendraceae contains 55˚S, Fuego Andean The regions. for many featurearelacking lifehistory this of analyses macroecological theof parasite overall distribution and virulence prevalence, influences mistletoea by species infected host of numberThe
: Andes, Andes,
show that that show
co (Loranthaceae) and (Loranthaceae) and - Patagonian forest, found along thealong forest, found Patagonian mpetitive exclusion, exclusion, mpetitive constitute are specialists that that are specialists in in twelve the southern South American bioregion, generalist mistletoes have have mistletoes generalist SouthAmerican bioregion, the southern
over 4700 species in 277 genera and this nutritional mode has mode nutritional has this generaand 277 species in 4700 over s
of these mistletoe these of parasites occur on parasites occur
mistletoe species in three families (Loranthaceae, families (Loranthaceae, three in mistletoe species Antidaphne use Misodendrum host
Nothofagus tabulating herbarium records, herbarium records, tabulating specificity . This
and and s
w 43 plant 2 43 species in ere
southern Andes from Andes southern 3 Lepidoceras contrast contrast
species and and species , parasitic plants
as their primary as theirhosts. primary explored. explored. (host range) is critical in that it that iscriticalin range) (host with a with
Desmaria mutabilis Desmaria (Santalaceae) are generalists generalists are (Santalaceae)
previous hypothesis that hypothesis that previous (Kuijt, 1969) (Kuijt, , South America , South 4
host use host
families but with families with but the host range host the ; 5
˚S to Tierra del Tierra to ˚S however,
Even though though Even Tristerix .
. All
s and and
, and and and and This article isThis article by protected copyright. All rightsreserved. Accepted6% and (15%) plants lineages mixture austral, of a represents species that woody with of flora forests. The continental proposed forest genus Chi and Argentina in range mountain Andes the sides of is Patagónico) Andino forest (Bosque Patagonian fewer in occur significantly tropical rainfores and seasonal tropical in of occur mistletoe species hundreds mya) (50 Loranthaceae Article and mya) most rece (53 Santalaceae mistletoesin eremolepidaceous mya), (72 Viscaceae by Misodendraceae, followed inlineageleadto the that mya ca.80 evolved order the parasitism in (7 Loranthaceae ofmajority mistletoe spe vast The Viscaceae. and Eremolepidaceae) former (the part in Santalaceae Misodendraceae, Loranthaceae, families: Amphorogynaceae, mistletoespecies 1670 as mistletoes referredto these aregenerally this Within species. 2400 genera over 179 and with species. Sa among considerably utilizedvaries hosts of called haustoria modified roots through stems roots host’s or tissues the in to conductive connect parasitic plants America South Antarctica. In of exception the with all continents presenton are Mistletoes others in the Neotropical biogeographic realm Neotropicalbiogeographic inthe others s Nothofagus
(Moreira (Aizen & Ezcurra, 1998) &Ezcurra, (Aizen that this forest represents a biogeographic island because of its isolation from other from isolation its other because of island representsabiogeographic that forest this - 6 (Kuijt, 1969; Press 1969; (Kuijt, Muñoz, 2011) Muñoz,
genera/104 Blume
are have been named been have (Vidal
. ae
It is composed of of composed It is rial parasites rial parasites the southern South American bioregion. The temperate Andean temperate The American bioregion. South southern the 4 -
Russell & Nickrent, 2008b; Liu 2008b; Nickrent, Russell & species) and Viscaceae (7/570). Previous studies aerial studies that Previous estimated (7/570). Viscaceae species) and .
this ecoregion this T . Most species are shrubs (57%), followed by treesclimbing followed by (22%), (57%), are shrubs species. Most he latter of which is which of he latter
et al.
, 1999) (Aizen & Ezcurra, 1998; Aizen & Ezcurra, 2008) Aizen &Ezcurra, 1998; (Aizen &Ezcurra, and these are classified by classifiedby theseare and (Mathiasen two
shows greater affinity with those in New Zealand than than inNewZealand those with shows greater affinity ; however, the degree of host dependence and number and dependence host of degree the ; however,
main located between 3 located
b (Wardle clade oreal, endemic (24%), neotropical and tropical tropical and neotropical (24%), oreal, endemic
eco more ntalales is the largest largest ntalales isthe
et al. le
are parasites that occur on host branches and host branches and on occur that are parasites regions: regions: , and the , and
bio et al. , 2008)
et al. diverse ,
the the
2001) dominant trees are members of the the of members are dominanttrees . A total of 87 genera and atlea and genera of 87 total . A 5 Nickrent , 2018) cies reside in two families,two in cies reside °S and 55°S latitude on both on 55°S latitude °S and Magellanic . Armesto . It is composed of 185 composed is . It 185 of . clade
et al. t biomes whereas whereas t biomes
et al.
and of parasitic plants parasiticplants of
(2010)
the the (1996) ntly in in ntly
Valdivian Valdivian . in
-
five
hav ,
e st This article isThis article by protected copyright. All rightsreserved. Accepted host with of the dealing literature majority artefacts sampling by are differences impeded range causeshost for underlying determine the overalldistribution and virulence influences it prevalence, that parasite) aparticular by species infected and specificity. preference, selectivity perspectives host the parasitize and are These achenes staminodes. (Mathiasen branches host afterdispersal to attachment theirseeds facilitates that viscin on sticky fruits and fleshy & Nickrent, bioregion 2014) central the and Vidal 1985; Kuijt, ArticleMart. found monophyletic are they family, Eremolepidaceae a distinct considered present in Antidaphne of genera 11 of composed Misodendraceae area 1 (Table northern The relationship between mistletoe species and their hosts hosts their and mistletoe species between relationship The Andean The . , however, only species, ,one only however, in the the Andean in Desmaria embedded within Santala within embedded . Misodendraceae the the
et al. et
Poepp. &Endl. Poepp.
2007) and from these ha fromand these Andean by S
-
ierra in Argentina Argentina ierra in , 2008) and Santalaceae and Patagonian forests Patagonian and and Der & Nickrent (2008) Der &Nickrent -
all of which are all of which Russell & Nickrent, 2008a) &Nickrent, Russell - Patagonian temperate forests Patagonian Notanthera - , Fig . Patagonian temperate forests. The temperate forests. Patagonian
. In contrast, contrast, . In neotropical neotropical .
, Lepidoceras with a single genus genus asingle with 1 ). These mistletoes belong to three families: three to These mistletoes). belong ve dispersed by wind by dispersed
are monospecific and endemic and monospecific are (Fig emerged various terms ash such various emerged ceae s. str ceae s. T. corymbosus T. (Kuijt, 1988; 1988; (Kuijt, endemic to the Andean the endemic to harbour harbour Misodendrum .
root a As 2
) . is crucial when examining life history factors for parasites in parasitesin for factors examininglife history is crucialwhen Nickrent in asdefined . Santalaceae, For Hook.f. discussed - mistletoe relationships report lists of various combinations combinations of lists various report mistletoe relationships . The nd stemnd parasites 12
Loranthaceae, . (Kuijt & Hansen, 2015) &Hansen, (Kuijt
Misodendrum mistletoe species, some of which which of mistletoe some species, Tristerix Amico
“eremolepidaceous” mistletoes we “eremolepidaceous” ,
(L.) Kuijt (L.)
and : and
Desmaria
species have dry fruits fruits species dry have by ,
Eubrachion after Watson
et al.
se has 13 species distributed along the the Andes along species distributed has 13 -
Patagonian forest. Most mistletoes have have mistletoes Most forest. Patagonian three genera genera three ,
entangl only three species in three genera are genera three in three species only has a range extending south intothis south extending has arange , 2007; Amico & Nickrent, 2009; Kuijt, Kuijt, 2009; Nickrent, Amico, 2007; &
Tiegh but only three are mistletoes: three only but DC
, but comparative approaches to approaches , but comparative has been examinedhas been fro
(2017) to , contains ost
Chile Hook.f. ing on ing . , Notanthera range, range, , , however, molecular data show show molecular data , however,
host range have previously been previously have
(Barlow & Wiens, 1973; 1973; & Wiens, (Barlow Loranthaceae, Loranthaceae,
tree provided with long feathery long feathery provided with
The 8 species8 choice, et al.
branches first two genera aregenera first two
are sympatric in the the are sympatric in G.Don
(the number of host host of number (the
(2010), is is (2010), re shown to be be to shown re susceptibility, susceptibility, m many mmany (Vidal ,
germinate germinate and
- Russell Tristerix . The The
This article isThis article by protected copyright. All rightsreserved. Acceptedavailable species, (i.e. label voucher the on present information the with matrixwas constructed Adata mistletoe. with the together was regis species host Aires, Argentina) (Buenos SI and Argentina) (Corrientes, Andean METHODS also ranges). Andean the in that depauper mistletoes in be whereas host to generalists, tend diverseregions mistletoes in that hypothesize studies Article species. number each host for total the with are associated mistletoe species from different void summarized previously been not specificity. and generality host measure of a this provide metric can and effort sampling wellas (species as range richness) host on information range mistletoe host such however, and occasional,rare secondary, mistletoes dwarf( for reported host listsof detailed example,For data. quantitative lack but Several herbaria were visited to record the host ranges of all mistletoe species that grow in the in grow speciesthat rangesmistletoe all theof record host to werevisited Several herbaria ranges host The . In addition, we will examine wewill . Inaddition, have larger host ranges (i.e., are generalists). are generalists). (i.e., ranges largerhost have - Patagonian forest Patagonian addition In ). ate regions tend to be host specialists tobehost tend ate regions
Duplicate specimens were excluded from the matrix from the excluded were specimens Duplicate
rankings do not measure the frequency with which a host species is parasitized. speciesisparasitized. a host which with frequency the measure not do rankings - Patagonian Patagonian ,
of we predict, that that we predict, statistic(K diversity tered if this information was available information wasavailable if this tered
the the ,
CORD (C : 12 host, host, BCRU (Bariloche, BCRU (Bariloche,
mistlet Arceuthobium forest mistletoes will tend to be host specialists specialists to behost mistletoes willtend forest immune
collector, date, locality, altitude locality, date, collector, and this study will study this and . ó Each voucher was examined and identified to to species level identified wasexamined and Each voucher whether rdoba, Argentina), MA (Madrid, Spain), MO USA) Louis, (Saint Spain), (Madrid, MA Argentina), rdoba, oe species oe species those
(Hawksworth & Wiens, 1972; Hawksworth & Wiens, 1996) &Wiens, Hawksworth 1972; & Wiens, (Hawksworth Q
) introduced by by ) introduced
Patagonian mist Patagonian
the the
M.Bie Argentina) (Barlow, 1977; Norton & Carpenter, 1998) & Carpenter, Norton 1977; (Barlow, latitudinal latitudinal occurring within occurring
b. provide macroecological data useful in filling that that filling in data useful macroecological provide ) where hosts are classified as principal, as principal, areclassified hosts ) where ,
Kavanagh & Burns (2012) Kavanagh &Burns range and number of collection vouchers collection numberof and range CONC (Concepci letoes with large with letoes - o mistletoe combinations have been been have mistletoe combinations n the label or if the host was collected wascollected host the if the or n label
; however, records from the same from the records ; however,
and the Andean
geog raphic raphic coordinates r
- ó geographic range geographic Patagonian forestha Patagonian n, CTES n, Chile), (i.e., (i.e., with small host host small with
incorporates . We expect Previous Previous when when . T s The The
will he ve
; This article isThis article by protected copyright. All rightsreserved. model car as herbarium labels exotichost when weregistered species; however, host native restricted to hostspecies among distribution even andan generality records islow, collection numberredundant of the and range and is host richnes index) Shannon (e.g. the diversity species between differences sample effort addition specificity. mistletoe will determine ranges, host with together analyses, These mistletoe species. forest. range between host relationship bias methodological To detect reported. 1999) & DeLange, region geographical can be herbariumwith data analysis. for considered temperatewere the forest within collected ( in Andean the found mistletoe species and wereincluded locality Accepted Article corymbosus Tristerix For each mistletoe species we calculated host range (richness)range host we calculated mistletoe species each For very very W use s . ,
e old coll We obtained obtained We we d also also
as
ried out inR out ried calculated the calculated the a good approximation for general patterns and and patterns general approximationfor a good analysed the relationship between host range and maximum latitudinal range forall range maximum and latitudinal range host between therelationship analysed . Al ections α
is redundant collection records collection is redundant . .
l variables were l variables exist This
. and and K One of the eight species of eight One the of
(before 1870) (before Q ,
(RCoreTeam, 2017) (RCoreTeam, approach for the species and genus level with this formula: level this with genus and species the for e.g., collector e.g., Notanthera heterophylla Notanthera K Q
proposed by by proposed and , incorporates
has been used in other mistletoestudies other in has beenused the number of herbarium records for all mistletoe species in the the in mistletoe all species for the number herbariumof records log log - , Patagonian forest are endemic; for the two that are not arenot that two the for forest areendemic; Patagonian thus
associated associated transformed bias .
The The
Kavanagh & Burns (2012) &Kavanagh Burns this species this
(Garcillán & Ezcurra, 2011) &Ezcurra, (Garcillán .
K information information Q .
Misodendrum value with When the number of recorded host species is high species ishigh host recorded of number the When
(Ruiz & Pav. G.Don &Pav. (Ruiz
and t and
K (Kavanagh & Burns, 2012) &Burns, (Kavanagh
herbarium vouchers herbarium was , Q equivalent to other measures of host host othermeasuresof equivalent to
he data were fit to a simple regression regression asimple were to he data fit will take high values, indicative of host of indicative values, high will take
on exclud as a first approximation for as afirstapproximation
relative abundances
(
M.
as the number of host species host numberof as the It is known known It is ed macrolepis
from to to ) s , take into consideration take intoconsideration ;
only thespec were however, herbarium data however, herbarium data
this study. study. this K (Downey, 1998; Norton 1998; (Downey, , we analysed the the , weanalysed Q that
=
mention
Phil. β .
biases associated biases associated
/( The analyses were The and α ) Ten of the 12 Ten the of 12 + 1), where where + 1), had onlyhad
imens imens species species ed on ed on
a
a In In few β
This article isThis article by protected copyright. All rightsreserved. Accepted wasdistribution range of similar that to narrow species a wide species have Populus corymbosus h exotic Patagonia northwest In Kuijt (Molina) region study the 22 of species in atotal parasitizing species generalist is ahighly Article 1). (Table families and several genera species host from six than Tristerix D.Don two mainly generalist species are four remaining species. Host angiospermsgymnosperms. orders and of 21 families spanning Andean RESULTS The latitudinal latitudinal The Among W rare host combinations rare host
but notsignificant but e found that mistletoes parasitize 43 43 that mistletoes parasitize e found er
(Cunoniac parasitize - ( osts:
Eight Patagonian forest Patagonian , Table L.
distribution Notanthera
and
Patagonian mistletoes, there are two cases of epiparasitism: epiparasitism: cases of two arethere mistletoes, Patagonian was found to parasitize more than 10 exotic species( 10 more than to parasitize was found Cytisus scoparius
mistletoe species are specialist mistletoe are species 1 parasitizing parasitizing Salix . ) significantly . Misodendrum
eae) Nothofagus Except for Except geographic range geographic
(more than 8 degrees 8 than (more
al , L.
Antidaphne and and
, ranges
(Salicaceae). Misodendrum brachystachyum Misodendrum
(Fig (Table 1, 1, (Table Desmaria mutabilis Desmaria
Tristerix corymbosus Tristerix were fou .
T. negative species (Nothofagaceae) and thus are considered specialist are considered thus and species (Nothofagaceae)
3 and
. (L.) Link Link (L.) a, R corymbosus The geographic distribution was distribution geographic The
and and the number of host species parasitized per mistletoe species is mistletoe species per species parasitized number the host of 2 Table S Table
nd, nd, s s
= 0. . All . All between
(Fig. 3b, R 3b, (Fig. Lepidoceras Misodendrum brachystachyum Misodendrum 233 (
latitude Fabaceae Misodendrum host , 1). These mistletoe species parasitize a wide range of of awiderange parasitize mistletoespecies These 1). , s species within within species P , parasitizing , parasitizing
Patagonian mistletoes are different. different. mistletoesare Patagonian o = 0. plant species in plant n , and , and ) 2 Weinmannia trichosperma Weinmannia
distributional range and and range distributional = 0.
) 273 are allgeneralist are
and and T. corymbosus T. 396
). was the only species in the genus parasitizing parasitizing genus the species in only was the
Castanea sativa Castanea At species species , mainly P Loranthaceae and Santalaceae have Santalaceae Loranthaceae and the the = 0.
34 genus level, genus level, 21 Tristerix corymbosus Tristerix and and negatively negatively 033 Table
genera and 24 families genera 24 and one plant genus, while the the genus, while one plant genera and 18families and genera
mistletoe range ) parasitizing parasitizing Desmaria mutabilis .
DC S Lepidoceras chilense Lepidoceras
2 Mill. Mill. ), the most frequent being mostthe), frequent
mistletoe among differed primarily primarily on associated with host host associatedwith the geographic geographic the
Cav. Cav. s that parasitize more parasitize s that
Caldcluvia paniculata Caldcluvia ( Fagaceae). Fagaceae). Desmaria mutabilis Desmaria (Cunoniaceae). Misodendrum parasitize parasitize
(Loranthaceae) (Loranthaceae) s
; Tiegh. Tiegh.
i h just within within just n the the n Tristerix Tristerix owever, owever,
few
. This article isThis article by protected copyright. All rightsreserved. ( species foundthat three They Zealand. New speciesin loranthaceous others range host larger have some species where here, wereport as theone asimilarpattern have the then species. to only applies statement this Okubamichael 1999; &DeLange, Norton 1998; Carpenter, species or fewhost genus one specificto tobe arelikely mistletoes forests temperate thesemistletoes useby host in overlap waslow there are sympatric, species punctulata Antidaphne specialist mistletoes Eight families. 23 species in D lowest the a also to mostfrequent two the collected. an considered can be m that show mistletoe the species eachof for with associated not was specimens voucher of Thenumber 1). (Table each specimens 35 less than with collected least were the punctulata Antidaphne corymbosus Tristerix
AcceptedISCUSSIO Article A T hree mistletoe species, hree mong the 185 woody species available in the Andean the species in woody 185 mong available the (Norton & De Lange, 1999) &DeLange, (Norton However; if each if However; less diverse less diverse Misodendrum ,
K while the remaining four species( remaining the while being Q
N of the Patagonian mistletoe Patagonian the of
M. punctulatum M
exception were frequently collected (>50 specimens) collected(>50 frequently were Misodendrum ,
agellanic forest agellanic (Clos) Kuijt (Clos) and M. of the two the of
gayanum Lepidoceras chilense Lepidoceras Misodendrum punctulatum Misodendrum Mis
since it uses a large number of host species and has been frequently has frequently and been species host of usessince it alargenumber
and and odendrum . These parasite ,
Lepidoceraschilense species ( ecoregions within the temperate forest are temperate forestare within the ecoregions Tiegh. M. linearifolium
contains contains (seven to species level species level to authors evaluated the host specificity for the five five the for specificity host the evaluated authors
host host (Table 1). (Table spp. and and spp. Tristerix corymbosus Tristerix ost use less than 10 host species. 10 than use less ost M. punctulatum Misodendrum only specialistmistletoes.only range (Fig range ) are generalists. generalists. ) are Desmaria
and the highest highest the and K
Banks ex DC ex Banks Q varies from 0.
at the at the and the remaining the and . -
Patagonian forest, m forest, Patagonian 3 et al.
species and and species c
and and , R
, but not for the other mistletoe othermistletoe for the not , but
genus genus whereas , 2016) 2 , Even though many of the mistletoe the many of though Even
M. linearifolium = 0.307, = 0.307, Notanthera heterophylla Notanthera . , Antidaphne punctulata Antidaphne Alepis flavida Alepis level
0 M. linearifolium . According to our results, . According 6 Desmaria mutabilis Desmaria Desmaria mutabilis Desmaria
New Zealand mistletoes New Zealand to 2.0, the lowest were 2.0,to the . P varies from 0.0 varies from It has been proposed that that proposed been It has Misodendrum = 0.061 Tristerix corymbosus Tristerix examined istletoes parasitize 43 43 parasitize istletoes ) and the highest highest the ) and
Tiegh ) (Norton & (Norton . The vouchers . Thevouchers
DC.
separately ,
s 1 , species Peraxilla Peraxilla
than than
) were . and and to ,
0.78, 0.78, for for
,
This article isThis article by protected copyright. All rightsreserved. Accepted have tree host per infections linearifolium site corymbosus Tristerix relation no by biased sampling. not parasitize Moreover, mistletoes, is specialist the parasitized by because issurprising This mistletoes. specialist and between generalist that parasitize hosts dispersed. Article dispersal: specialization. Andean related families. mistletoe establishment for required properties The parasitize hostspecies. of range a wide parasitize spe colensoi cies of
(García three for explored been has mistletoe parasitism of intensity The Andean the in generalists arehost mistletoesthat the Among t that interesting It is reason for this is unknown but may may i but isunknown this for reason greater infection intensity intensity greater infection -
Patagonian (Hook.f.) Tiegh. Tiegh. (Hook.f.) Nothofagus Nothofagus the fruits of of fruits the Nothofagus
ship Tristerix corymbosus
et al. et ,
were studied at three si three at were studied
These two m These two between dispersal mode and hostrange. mode and between dispersal Misodendraceae includes those mistletoes with the widest latitudinal ranges in the the in ranges widestlatitudinal the mistletoes with those includes Misodendraceae , 2009)
share recent common ancestors common share recent forest and these were the ones with the smallest host ranges, thus indicating thusindicating ranges, smallesthost the with ones the forest thesewere and , a host generalist, , ahostgeneralist,
, whereas (or Cunoniaceae). These observations also These Cunoniaceae). observations (or spp. Misodendrum (Vidal
. All he two The mistletoe host specialist, host The mistletoe and and
but for both genera, rare hosts are found in the same family, Cunoniaceae same the in family, genera,arefound rarehosts for both but
istletoe genera, that show restricted hosts, have different mode different have restrictedhosts, show that genera, istletoe host generalist host - P. tetrapetala P. Russell & Premoli, 2015) Premoli, Russell & than generalists. Tupeia antarctica Tupeia host host , the most, the
specialist are wind dispersed while dispersed are wind tes. These mistletoes These tes.
showed showed ndicate that ndicate the dominanttree the collected mistletoes are dispersed by animalsby mistletoes aredispersed
(L.f.) Tiegh. (L.f.) mistletoes that that
less than 2 mistletoe infections per host tree host per mistletoe infections 2 less than
Cham. & Schltdl. Cham. &Schltdl. . Interestingly, there is no overlap in host use host overlapin there isno . Interestingly, are met by bothhost metare by
mistletoe species, is a host generalist that does not not does that generalist isahost mistletoe species, certain anatomical, physiological or biochemical or physiological certain anatomical,
Misodendrum punctulatum Misodendrum
. ) are host specific and parasitize mainly mainly parasitize specific and ) arehost
According to thesestudies to According (
Misodendrum showed higher number higher showed in the Andean the in
those those of
- support thefact support Patagonian forest,none Patagonian and and species
Desmaria Nothofagus s, despite being from distantly fromdistantly s, despite being
and and Ileostylus micranthus Ileostylus - Patagonian forests. forests. Patagonian of the temperate forest. temperateforest. the of Desmaria
and there appears to be be appears to there and
that our results a our that are s (from 3 to 8) to 3 s (from
and and , the host genus genus host , the ,
host specialist host animal animal ) M. primarily primarily
appear appear to s
of of
at one at one
Tiegh. Tiegh.
of of re s
. This article isThis article by protected copyright. All rightsreserved. 42 to wit species numberhost of the with new record. reported in this study caseswe found the of subtropics ofmistletoes infieldsurveys employed statistic This sample size. of that surpass thefor 47 tobeless than have would collections of number species. The of instead genera K corymbosus Tristerix despite lower, Another gayanum study this mistletoe in the inflates This were seen. example, by specificity on the disregard 5.0 to 0 mistletoe for Australian reported Q
sampl
Accepted as distributions restricted h Article value is in the range of range the isin value The geographic range width of Andean of width range geographic The worldw epiparasitism occurs Mistletoe K The ˚
South, specialists( the while
across undesirable (Wilson & Calvin, 2016) &Calvin, (Wilson e
Misodendrum drops by an order of magnitude order of an dropsby
Q size size (Wilson & Calvin, 2016) &Calvin, (Wilson
values ; K
comparatively comparatively however Antidaphne all Australia (here number of of number (here Q
of 2.0 for for 2.0 of
for for
aspect of the the of aspect
that is clearly the the most general isclearly that
(Table 1) mistletoes ,
gayanum these numbers have to be be to have these numbers might
. Our study sho . study Our M. gayanum the . In . In K high numbers high of Q
Misodendrum was predicted. The distributions ofgeneralist distributions The predicted. was
the value to 2.0 to value . If one . If
herbarium and genera and be improved by incorporating stopping rules similar to those rulesstopping those similar to byincorporating be improved (Kavanagh & Burns,2012) (Kavanagh
of the of , but the, but case parasitizes four different different parasitizes four K
Andean Lepidoceraschilense Misodendrum . E Q
statistic is that high numbers of high statistic isthat piparasitism also occur piparasitism also
, the highest value. Hence, , thehighest considers only considers Andean (Watson
and and ws that the use of the use the the of ws that
- ide; however, it is most common in the tropics and and tropics the in common ismost it however, ide; records
- Patagonian forest Patagonian giving the false impression that this is the this isthe that the falsegiving impression they parasitized they Patagonian Patagonian
specialists. This artefact is not corrected by by corrected is not artefact This specialists. is more comparable to comparable is more different different of T. corymbosus T. of -
Patagonian forest Patagonian et al. ) have a larger distributional ) have alargerdistributional ) considered with caution considered with and and ist , 2017)
the number of host genera, the value for for genera, value the numberhost the of
parasite among the mistletoes parasite among host forest mistletoes mistletoes forest how the diversity of of hosts diversity iscalculated the how
on Nothofagus . s Tristerix corymbosus
. Specialist mistletoes were not the ones ones mistletoes the werenot Specialist
, . parasitized. This is best seen with seenwith isbest This parasitized.
s T
the valuesthe for
hat study in thein Andean K
parasitizing parasitizing Q
t are within the the within are
he K index is subject to bias issubject to index
values values records
species Q
show show show
values values
because
seenin K mistletoes reach only up only reach mistletoes
- Desmaria mutabilis Desmaria push the the push range. Patagonian Patagonian Q ed , negative
but only five five only but we if low, are
give similar result give ranges those of
that has been previously previously has been
they areaffected they other species other At least for the the At leastfor
K studied mostgen K
Q relationship relationship Q
using range
forest. One
value value K based on on based Q , yet its , yet records
value to to value
d . eralist host M.
For For . from
is a s
This article isThis article by protected copyright. All rightsreserved. Tristerix Accepted mistletoe species and of reinforcement process that of consequence We where non onsuch establish to seedsfail inoculated artificially when place, especially is taking competition no mustthat one assume Amazonian is competition that suggesting thus mistletoe species, atleast two by host usage in isoverlap mistletoes,there dwarf Arceuthobium mistletoe be could families fromdifferent speciesare the Article speciesw hosts between potential interaction the that Loranthaceae two Santalaceae, (two mistletoefour species generalist wefound however, t Because (2012) & Burns speciali tobehost tend regions depauperate ranges geographic specialists. SouthAmerican bioregion southern
can Africa, South In in Mistletoes Desmaria host specificity specificity host Tristerix corymbosus Tristerix , however,
- an example of competitive exclusion an example competitive of and and he Andean host interactions host contrast In Psittacanthus Lepidoceras .
in North America North in currently currently The The
provide a may lead to non to lead may floristically floristically
hypothesize that competitive exclusion exclusion competitive that hypothesize (Grenfell & Burns, 2009) &Burns, (Grenfell host interaction interaction is not - mistletoe Patagonian Patagonian
to to - - parasite d taking place. In other mistletoes, such as the three sympatric species of of species sympatric three asthe mistletoes,such taking other place. In host trees. This appears to be the situation in the Andean the in situation the be to appears host trees.This our res
evidence supporting this hypothesis for severalAustralia for this hypothesis evidence supporting related only to the diversity of potential host species available but but host speciesavailable potential of diversity tothe related only studied in the temperate forest. forest. temperate the in .
Competitive exclusion Competitive
does not not does is that no is that diverse regions tend to be host generalists whereas mistletoes in mistletoes in whereas to behostgeneralists tend diverse regions
s dynamics pecies ults
coevolutionary arm race leading to host specificity in in specificity to host arm leading race coevolutionary forest is not very very forestdiverse, isnot (Hawksworth &Wi (Hawksworth - by overlapping host use host overlapping , generalist mistletoes have smaller geographic ranges than than ranges smallergeographic have , generalistmistletoes , host ranges of Australian mistletoes are not associated with their their with associated mistletoes arenot Australian of , hostranges Fadini (2011) share hosts with share with hosts
host overlap host overlap rarely share the same primary host primary thesame share rarely (Okubamichael between potential hosts species hosts between potential sts .
, aprocess (Barlow, 1977; Norton & Carpenter, 1998) & Carpenter, Norton 1977; (Barlow, ith the mistletoe, and also with with mistletoe competition. also mistletoe, and the ith Even mistletoe species in the same family same family the speciesin mistletoe Even
has been has been , no exists ens, 1972; Jerome & Ford, 2002) Jerome&Ford, 1972; ens,
Misodendrum et al.
overlap in host use was detected. hostusewasdetected. in overlap patterns as is currently see is currently as patterns
that contributes to a geographic mosaic of of mosaic a geographic to contributes that today. This process could have actedas have This processcould today. may have we expected to find specialist mis specialist find to we expected , 2016) impl
icated for icated .
The authors authors The
happened in the past and and thepast in happened species and and species
and several several and in a local area, especially if area, especially alocal in
other mistletoesother speculated Desmaria mutabilis - n Patagonian forest Patagonian n
with mistletoes. mistletoes. sympatric sympatric . Misodendrum For theseFor
) In this case, this In Antidaphne . . It appears It appears
Kavanagh Kavanagh such as such that this this that also tletoes; tletoes; thata
to to a
, .
This article isThis article by protected copyright. All rightsreserved. RVR and specimen ACKNOWLEDGEMENTS hostr understanding for consider factors to important be might parasites and mistletoes morehave would specialized regions large with mistletoes component CONCLUSIONS parasitize instead but parasitizing of capable mistletoes not are In these casesthe origin. moreis of recent host whereasthe others history for theirevolutionary in early arose adaptation 1999) Lange, level ( genus the at specialists by species host predominant the explained that collect empiric the in hosts samearea. different use (Loranthaceae)
Accepted ArticleNothofagus We thank the curators of the various herbaria we herbaria thevarious of the curators We thank Andean The genus The mistletoes in depauperate regions tend to specialists to behost tend depauperate regions in mistletoes
were supported by supported were data by the presence of presenceby the mistletoes. We provide evidence that contradicts a previous hypothesis that predicted predicted hypothesis that aprevious evidencethatcontradicts provide mistletoes. We . This observation may be evidence that for some mistletoes some for that evidence maybe . observation This
used in used al data to directly address the causes of this observation. this causes of the address directly to al data Misodendrum forests of New Zealand, Chile and Argentina are that some mistletoe species are host host are species mistletoe some arethat Argentina and Chile Zealand, New of forests - Patagonian
geographic ranges would also have large host ranges and conversely less diverse less diverse conversely and ranges have host also large would ranges geographic other species from the community. the species from other
this paper. Special thanks go to Javier Puntieri for comment for to go JavierPuntieri thanks Special this paper.
temperate forests show unique host utilization patterns amongits patterns utilization host unique show temperate forests Consejo Nacional de investigacion Científicas y Técnicas (CONICET). y Científicas investigacion de Nacional Consejo selection selection
(Barlow, 1977; Dean 1977; (Barlow, (with 8 species) 8 (with Nothofagus favouring ) whereas others parasitize parasitize others ) whereas that only parasitizes only that . Host abundances and biogeographic history of hosts hosts of history biogeographic and abundances . Host
close physiological adaptations of the mistletoes to mistletoes to the of adaptations close physiological
et al. This lack of overlap suggests field studies to studies field suggests overlap of lack This visited , 1994; Downey , 1994;
for their assistance in collecting the the collecting assistance in their for
. This This Nothofagus multiple evolutionary outcome can be outcomecan be evolutionary
et al. , strong physiological co physiological , strong ange in this biome. this in ange
genera , 1997) -
supports the concept concept the supports mistletoe combination mistletoe combination s . Authors . Authors
Nothofagus (Norton &De (Norton .
Features shared GCA
trees -
This article isThis article by protected copyright. All rightsreserved. Accepted of Santalaceae (Santalales). phylogeny Amolecular (2008) D.L. Nickrent, and Der, J.P. Africa: South ofmistletoes in The distribution W.D. (1994) J.J.,Stock, Midgley, Dean, W.R.J., Host (1977) B.A.a.D.W. Barlow, of segregates the generic of The classification D. Wiens, (1973) and B.A. Barlow, León J.J., Armesto, Vidal Amico, G.C., Article Schinus on verticillatus Tristerix Mistletoe ofthe Report First (2009) D.L. Nickrent, and Amico, G.C. C. Ezcurra, and Aizen, M.A. plant Highincidence of (1998) C. Ezcurra, and Aizen, M.A. REFERENCES Botany choice. host and species richness of patterns . mimicry. Notanthera M. & Villagran C. Armesto, (J.J. de Chile. bosques nativos delos Ecología In isla biogeográfica. hosts. and mistletoe the in speciation fasci awarmerpast? America reflect significance. and present ecological origin biogeographical America: South of temperateforest the T.K. Arroyo, eds), Editorial Universitaria, Santiago: pp 23 pp Santiago: Universitaria, Editorial eds), Arroyo, T.K. culatus from the Sierra de San Luis, Argentina. Argentina. Luis, deSan Sierra from the culatus , 33
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Accepted species diversity in patterns spatial macroecology: Mistletoe (2012) Burns,K.C. and P.H. vanagh, Article and host use across Australia. use across Australia. host and angiosperms. americanum Arceuthobium Servi USDA Forest (Arceuthobium) Biotropica Science Vegetation effectiveness mistletoe apopulation. of scale thespatial shapes Brasilica Botanica Acta specialization. extreme generalization to host savanna: Amazonian an in mistletoe species Example an from. Colonization: Australia. in Viscaceae) , 41 of herbarium data against vegetation sampling in an oceanic island. sampling vegetation data against herbariumof - Molecular Ecology Molecular , 656 Cabal, M.A., Cabal,
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This article isThis article by protected copyright. All rightsreserved. Accepted on patte insights Metadata provide C.L.(2016) Calvin, C.A. and Wilson, to estimators ofspeciesrichness Novelapplication A.(2017) K.V.,Leigh, Milner, D.M., Watson, of the vegetation of flora and Comparison (2001) S. Wagstaff, Ramírez, C., C., Ezcurra, P., Wardle, Vidal ArticleVidal Vidal Vidal computing. statistical for and environment A language R: (2017) RCoreTeam. interactions ecological and physiological Parasitic(1999) plants: J. Watling, J., Scholes, Press, M., - - - - Russell, R. and Premoli, A.C. (2015) Nothofagus trees show genotype difference that influence influence differencethat genotype trees show (2015) Nothofagus A.C. Premoli, and R. Russell, T (2008b) Nickrent, D.L. and R. Russell, mistletoe family thein showy relationships Evolutionary (2008a) Nickrent, D.L. and R. Russell, mistle feathery the of phylogeny Amolecular (2007) Nickrent, D.L. and R. Russell, mistletoes (Santalales), an overlooked topic in forest biology. biology. forest topic in overlooked an mistletoes (Santalales), parasites. of hostrange the predict NewZealand. and Andes southern the mistletoes, Misodendraceae by infection Santalales. (Loranthaceae). Misodendrum. Austria Vienna Computing Statistical hosts. their with Molecular phylogenetics and evolution and phylogenetics Molecular Systematic Botany Systematic American journal botany of journal American Physiological plant ecology plant Physiological , International journal for parasitology for journal International 32 , 560 .
New Zealand Journal of Botany of Journal New Zealand he first mistletoes: origins of aerial parasitism in aerialparasitism of in he first mistletoes: origins . Australian Journal of Botany of Journal Australian - 568. , , 175 95
, 1015 - 197. , 47 - , 523
1029. - 537.
Botany
rns of epiparasitism in epiparasitism in of rns , 95 R Foundation for R Foundation , , 39 63 , 259 , 47 , 69 , 541 , 31 - - 269. 108. - - 548. 39. toe toe
This article isThis article by protected copyright. All rightsreserved. records of sizerange Fig remain the Glatzel, Gerhard linearifolium corymbosus Tristerix mutabilis B. shoots. prefloral (Santalaceae) Fig ( Collections forest Fig LEGENDS FIGURE Accepted Article Matorral Chilean . . .
3. 2 1 . . .
Green Distribution mapDistribution of F Andean Representativesmistletoes fromthe of or
(Loranthaceae) at anthesis. D. D. anthesis. at (Loranthaceae) and and and and
the 12 mistletoe species of Andean temperate forest Andean of mistletoe species the 12
of of
(Misodendraceae) shoots with fruits bearing plumose bearing staminodes. fruits with shoots (Misodendraceae) shading Notanthera heterophylla Notanthera number of species numberhost the of )
are not shown (seetext). shown are not
(Loranthaceae), the quintral the (Loranthaceae), represents
host species host the three three the ing G. Amico. G. Amico. ing
the the Lepidoceraschilense Valdivian Valdivian mistletoe families
( C
and and Notanthera heter Notanthera )
. (A)
Tristerix corymbosus Tristerix
,
geographic range size range geographic forest forest ,
in full flower with snow. E. E. snow. in full with flower and and -
Patagonian forest.A. Patagonian
within the within (Santalaceae) with young fruits. C. fruits. young with (Santalaceae) tan shadingtan ophylla
, r
elationships elationships
(Loranthaceae) inflorescence. E. E. inflorescence. (Loranthaceae) Andean from
and and the the outside the temporal forest temporalforest the outside Magellanic forest host host - Patagonian Patagonian Antidaphne punctulata Antidaphne between genera (B) Misodendrum Misodendrum
Photo credits: A. Photo temperate geographic geographic
and . Desmaria
number
This article isThis article by protected copyright. All rightsreserved. Accepted Article Table APGIV follows orders and Families forests. temperate Andean Table article the online in found Information maybe Supporting Additional INFORMATION SUPPORTING
S S 2 1 . . Exotics species used by by used Exotics species the in themistletoe species 12 by species used eachhost for Number observations of Tristerix corymbosus
.
supporting information tab for this for tab information supporting
( 2016 ) .
Accepted isThis article by protected copyright. All rightsreserved. Misodendrum oblongifolium Misodendrum linearifolium Misodendrum gayanum Misodendrum brachystachyum Misodendrum angulatum Misodendrum Misodendraceae chilense Lepidoceras punctulata ArticleAntidaphne Santalaceae Species 1. Table
Mistletoe species present in present in species Mistletoe
36 36° 15' 37° 15' limit (S) Northern 36° 3 35° 2 35° 15' 37° 35° 2
° 32 25 1 1 1 ' ' ' ' '
52° 2 42° 30' 42°15' limit (S) Southern 55° 0 45° 5 46° 2 54° 3
2 ° 16 33 2 3 2 1 Andean
' ' ' ' ' '
0 0 0 0 0 0 0 0 range (m) Altitudinal
- Patagonian temperate forest temperate Patagonian ------
1700 2000 2500 1300 1500 1350 2000 1350
(degrees) range Latitudinal
18.02 17. 19.19 1
9.91 8.97 6.22 5.03 5 . 94 80
hosts
No. 6 4 6 4 6 3 9 7
genera
No. 1 1 1 1 2 1 8 7
families
No. 1 1 1 1 2 1 6 5
orders
No. 1 1 1 1 2 1 5 5
records
No. 101 31 80 30 18 23 15 5
species K
Q
0.06 0.14 0.08 2 0.24 0.19 0.6 0.78 .00 0
genera K
Q 0.01 0.03 0.01 0.2 0.07 0.06 0. 0.78
60 0
Accepted isThis article by protected copyright. All rightsreserved. matorral, the Chilean in occur Species that * + Northern mutabilis Desmaria Articleheterophylla* Notanthera corymbosus* Tristerix Loranthaceae quadriflorum Misodendrum punctulatum
limit in the temperate forest the limit in
35° 20' 34° 26'+ 33° 30'+ 36° 30'
41° 20' 42° 25' 42° 25' 54° 0
4 '
0 0 0 0 Tristerix corymbosus Tristerix - - - -
1800 1500 2400 1500
17.
5.98 8.07 8.91 55
at to 30° 9' S and 9'and 30° S to at
22 3 5 8
21 1 2 8 Notanthera heterophylla Notanthera
19 1 2 5
17 2 4 1
at to at to 167 2 34 34 8
32° 19' S 32° 19'
0.2 0.3 0.15 0.09 1 0
0.07 0.3 0.14 0.03 0
This article isThis article by protected copyright. All rights reserved. Accepted Article
This article isThis article by protected copyright. All rightsreserved. Accepted Article
This article isThis article by protected copyright. All rightsreserved. Accepted Article