Towards an understanding of the distribution of Ilex L.(Aquifoliaceae) on a World-wide scale

BS 55 501

Towards an understanding of the distribution ofIlex L. (Aquifoliaceae) on a World-wide scale

PIERRE-ANDRÉ LOIZEAU, GABRIELLE BARRIERA, JEAN-FRANÇOIS MANEN AND

OLIVIER BROENNIMANN

LOIZEAU, P.-A., BARRIERA, G., MANEN, J.-F. & BROENNIMANN, O. 2005. Towards an understanding ofthe distribution of Ilex L. (Aquifoliaceae) on a World-wide scale. Biol. Skr. 55: 501-520. ISSN 0366-3612. ISBN 87-7304-304-4.

Almost 600 species of Ilex L. (Aquifoliaceae) are now recognized and most of them occur in trop-ical America and eastern Asia. Only c 30 species are known from North America, four species arefound in Europe, a few on Pacific islands, one in northeastern Australia and one in sub-SaharanAfrica. Fossil data shows that this genus previously had a much wider distribution. Fossils havebeen found in Alaska and Iceland, western North America and southern South America, Siberia,New Zealand and southern Australia. Floral morphology of Ilex species is very uniform at an inter-specific level, whereas leaf morphology often shows great variability at an intra-specific levelresulting in difficulties of discriminating between the different species. We compared recon-structed phylogenies based on chloroplast and nuclear DNA sequences, and morphological char-acters from 47 Ilex species. The plastid phylogeny is strongly correlated with the geographic dis-tribution of extant species. However the plastid and nuclear phylogenies are not congruent. Thismay be due to frequent inter-lineage hybridization events, a process which could explain the highcomplexity of this family (i.e. at morphological, genetic, geographical distribution levels). We didnot obtain a resolved phylogeny based on morphological characters. A world-wide distributionmodelling map has been computed by an Ecological Niche Factor Analysis (ENFA) based on 826Ilex occurrences in tropical America and 12 GIS layers describing the environment. The map ofthe potential distribution obtained is consistent with the distribution of the genus at present.However the model has less predictive probability for the northern hemisphere. Data of pollenfossil records for all Ilex over the world were mapped at world scale at various geological periods.Analyses of extant and past distributions of the genus, and phylogenetic results integrated withclimatic patterns have been used to tentatively explain the current distribution pattern of Ilex.Some hypothesis assuming Bering and North Atlantic land bridge connections, Tertiary relict flo-ras, long distance dispersal or morphological stasis are congruent with the current disjunct dis-tribution of the family.

Pierre-André Loizeau, Conservatoire et Jardin botaniques, Chambésy/Genève, Switzerland. E-mail: [email protected]

Gabrielle Barriera, Conservatoire et Jardin botaniques, Chambésy/Genève, Switzerland. E-mail:[email protected]

Jean-François Manen, Conservatoire et Jardin botaniques, Chambésy/Genève, Switzerland. E-mail: [email protected]

Olivier Broennimann, Université de Lausanne, Institut d’écologie et de géobotanique, Dorigny/Lausanne,Switzerland. E-mail: [email protected]

Introduction

Diversity and distributionAquifoliaceae, the holly family, was once repre-sented by four genera: Ilex L., NemopanthusRaf., Phelline Labill. and Sphenostemon Baill.(Cronquist 1981), but today it includes onlythe genus Ilex (Judd et al. 1999; Powell et al.2000; Loizeau et al. in press), which is com-posed of almost 600 species. Although cos-mopolitan, it is very unevenly distributed interms of the number of species occurring ineach continent. Ilex occurs mostly in the trop-ics but extends into temperate regions withoceanic climates up to 63°N (America, Eura-sia) and down to 35°S (America, Africa). Thereare c 300 species in tropical America (Loizeau1994), c 250 species in south-east Asia, c 30species from North America, four species inEurope (including the endemic species of theCanary Islands, Madeira and Azores), a fewspecies in Pacific islands, one in northeast Aus-tralia and one in sub-Saharan Africa. TropicalAmerica and south-east Asia are the importantcentres of species diversity for this genus.Species of Ilex are found from lowland to mon-tane forest (disturbed or primary) up to 4000meters elevation in the Andes and in theHimalayan region. The family is usually foundin humid habitats (Martin 1977) and is totallyabsent from very dry areas.

SystematicsA world-wide treatment of the genus was doneby Loesener (1901, 1908, 1942). Floral mor-phology of Ilex species is very uniform at ainter-specific level whereas, leaf morphologyoften shows great variability at an intra-specificlevel, resulting in difficulties in discriminatingbetween different species. Ilex is composed ofdioiceous shrubs or trees with simple and alter-nate leaves, and small, usually 4-5-merous flow-ers gathered in cymose inflorescences. Speciesare mostly recognized on whether they are

deciduous or evergreen, the size and shape ofleaves, complexity of the cymose inflores-cences, and the number of floral parts. The fol-lowing large-scale anatomical studies empha-sise some of the difficulties encountered whendiscriminating between different specieswithin the genus. Baas (1973) published anextensive treatment on the wood anatomy ofIlex. He concluded that Ilex species were impos-sible to separate using wood anatomy alone.He made the same conclusion based on a studyof leaf anatomy (Baas 1975). Lobreau-Callen(1975) studied the pollen of more than halfthe species included in Loesener’s works(1901, 1908) and concluded that Ilex speciescould not be separated based on pollen charac-teristics. Loizeau and Spichiger (1992) pro-posed a classification based on the structuresof the inflorescence in Ilex. They included anevolutionary character for the first time intothe classification of Ilex.

Ancient and extant pollenThe pollen of Ilex is very characteristic (Martin1977) and no other known pollen type couldbe confused with it (Fig. 1). The closest pollengrain morphology to Ilex is that of Coprosmanertera F. Muell. (Rubiaceae), which has other

502 BS 55

Fig. 1. Ilex teratopis pollen grain (photo J.Wuest).

features that readily distinguish it. The othertaxa with a pollen ornamentation resemblingthat of Ilex can easily be separated using otherpollen morphological characters. Ilex represen-tatives produce low amounts of pollen, they areinsect-pollinated and very little pollen is foundin the atmosphere (Hyde 1961; Clot pers.comm.). Moreover they have a relatively lowpollen dispersal capacity (Behling et al. 1997).The oldest findings of pollen attributed to Ilexoriginate from the Turonian or earliest upperCretaceous in Australia, 90 million years ago(mya) (Martin 1977). But the genus was appar-ently already cosmopolitan by the late Cre-taceaous, since pollen grains of Ilex dated at 70-85 mya have been found in Africa, westernNorth America, and South America (Lobreau-Callen 1975; Martin 1977; Muller 1981). How-ever, few data (pictures) of these very old fossilpollens of Ilex have been published.

Molecular analysesThe phylogenetic history of the genus basedon DNA analyses has been studied by Cuénoud(1998), Cuénoud et al. (2000), Setoguchi andWatanabe (2000), and Manen et al. (2002).The chloroplast atpB-rbcL spacer has beensequenced for 116 taxa represented in mostparts of the world (Cuénoud et al. 2000). Theplastid phylogeny showed four major cladesthat were poorly supported and lacked anyresolved hierarchy between them (i.e. anAmerican, two Asian/N. America, and aEurasian clade). Manen et al. (2002) compareda three-gene plastid phylogeny with a two-genenuclear phylogeny based on 47 species selectedamong the taxa studied by Cuénoud et al.(2000). They observed an incongruencebetween the two phylogenies, which they con-sidered due to the probable expression of astrong inter-specific and interlineagehybridization, making phylogenetic studiesvery complex. The same conclusion was madeby Setoguchi and Watanabe (2000) based on

Asian Ilex of the Bonin and Ryukyu Islands.These two studies both demonstrated naturalinter-specific hybridization in Ilex. In horticul-ture, inter-specific hybridization is achievedrelatively easily between different species of thegenus (Galle 1997).

Finally, a relative test of the rate ofnucleotide substitution made by Cuénoud et al.(2000) gave the age of the common ancestor ofthe extant species as 50 million years old. Thisage is far from the 90 mya indicated by the fos-sil records. According to these authors this dif-ference could be explained by extinction ofthe basal branches of extant species, whichthen do not represent the entire lineage.Moreover they consider the Eocene (54-36mya) as an important era for diversification inthis genus.

Two questions that this paper attempts toclarify are: (1) Can contradictions between thepast and present distribution of Aquifoliaceaebe explained using a comparative analysis offossils and the current distribution of Ilex, thatalso integrates the different theories involvingthe earth’s history (continental drift, migra-tory pathways, climate fluctuation) from 90mya? (2) Can a phylogeny of Ilex, based onmorphological characters, improve the under-standing of the different migration patterns inthe genus?

Materials and methodsMorphological analyses For the 47 Ilex species from all over the world,for which plastid and nuclear phylogeny wasavailable (Manen et al. 2002), morphologicaldescriptions including vegetative (leaves, ram-ets, etc.) and sexual (inflorescence, flower andfruit) characters were made. Descriptions werebased on herbarium specimens from BM, BR,COL, F, G, K, MBM, NY, P, S, US, and W. Whennecessary, the descriptions were supplementedwith information from literature, mostly Loe-

BS 55 503

sener (1901) and Galle (1997) (Appendix 1).Within the framework of our research onNeotropical Aquifoliaceae, 126 morphologicalcharacters were chosen to infer phylogeneticrelationships among the 47 species included inthe present study.

A matrix of characters was built up for the 47representative species (available at the addressof the first author) and was used to generatemorphological trees with PAUP 4.0b3a (Swof-ford 2000). The trees were arbitrarily rootedwith Ilex canariensis Poir., which is claimed to bethe most basal taxon (Manen et al. 2002), tocompare their topology with the molecularphylogenetic trees.

The plastid and nuclear trees (Manen et al.2002) were used to analyse the charactermatrix. Consistency indices (CI) of each char-acter were tabulated using MacClade (Maddi-son & Maddison 1992).

Distribution modellingIn the classical approach, distribution model-ling (e.g., GLMs, McCullagh & Nelder 1989;GAMs, Hastie & Tibshirani 1987) requires bothpresence and absence data. The available Ilexdata do not allow us to use this kind of modelbecause, as is often the case with herbariummaterial, the absence of herbarium collectionsfrom a given place may indicate that taxa areabsent or that there are no collections fromthat region. To overcome this problem ofabsence data, several modelling techniqueswhich incorporate presence data only havebeen developed in recent years (e.g., BIO-CLIM, Austin et al. 1994; GARP, Peters &Thackway 1998; ENFA, Hirzel et al. 2002). Inthis paper, the distribution modelling map hasbeen computed by ENFA (Ecological NicheFactor Analysis) using the software Biomapper(Hirzel et al. 2002). The distribution modellingmap is then called habitat-suitability map.

ENFA allows us to compare the distributionof ecological values for a presence data set to

the distribution of ecological values for thewhole study area. Species distribution based onthe ENFA factors is then used to compute ahabitat-suitability map (Hirzel et al. 2002).Model validation is achieved in Biomapperthrough a jack-knife cross-validation process(Fielding & Bell 1997) with presence pointspartitioned in ten subsets of equal sizes.

The study area comprises the world-wideland area, excluding Antarctica. All analyseshave been performed within a raster-map datastructure based on the latitude/longitudecoordinate system with a 0.5 decimal degreeresolution. The Ilex presence dataset origi-nated from a tropical American Aquifoliaceaedatabase (Conservatoire et Jardin botaniques,Geneva) based on herbarium specimens. Thestudy included 3506 individuals and each wasdescribed by its geographic coordinates. Onlyone location occurring in the same 0.5 x 0.5degree grid cell was kept, the final sample sizewas thus reduced to 826 occurrences. The sec-ond type of data required for the ENFA is a setof quantitative raster maps describing the envi-ronment. A mean monthly climate dataset(CRU global climate dataset, New et al. 1999)was used to create annual climatic predictors.Monthly data consisted of data to 0.5 degreelatitude/longitude resulting from an interpola-tion from worldwide meteorological stations.Annual data have been produced through GIScalculation, resulting in 12 GIS layers.

Pollen fossil distributionA database of the pollen fossil records for Ilexfrom all over the world has been compiledfrom published sources cited by Martin (1977),Muller (1981) or directly from Wijninga andKuhry (1993). The data were mapped at worldscale (Scotese 2003) at various geological peri-ods with for each period the correspondingposition of the continents. The object was toanalyse the distribution of fossil records in anattempt to determine the origin and phytogeo-

504 BS 55

BS 55 505

Fig. 2. Strict consensus of 22 most parsimonious trees(820 steps, CI = 0.20, RI = 0.42) obtained from thematrix of characters using the heuristic search (TBR,100 random taxon additions) of PAUP. Bootstrap values(if > 50) are indicated below the branches. Abbrevia-tions of the geographic distribution are alphabetically:Afr = Africa, And = Andes, Bra = Brazil, Cam = CentralAmerica, including South Mexico, Can = CanaryIslands, Car = Caribbean Islands, Eas = East Asia, Eur =Europe, Gui = Guiana, Haw Tah = Hawaii/Tahiti, Mac =Macaronesia, Nam = North America, Sam = SouthAmerica, Sea = South-East Asia.

graphic relationships of modern Ilex distribu-tion. The macrofossils were not retainedbecause they are not considered a reliable datasource unless they are identified throughautapomorphies shared with extant species(Hill 2001).

ResultsMorphological analysesThe morphological tree (Fig. 2) is incongruentwith either the plastid or nuclear tree. TheConsistency Index (CI) of each character wascalculated on the plastid and nuclear trees todetermine any correlation between morpho-logical characters and molecular trees. No cor-relation was found with any of the moleculartrees (results not shown).

Distribution modelling map The genus Ilex shows a global marginality valueof 0.939 and a global tolerance value of 0.292,indicating as expected that its habitat differsfrom the world average conditions and that itsecological niche is relatively restricted. Thefirst four ENFA factors account for 92% of thevariance. The marginality factor alone explains72% of the variance. Its coefficients show thatIlex distribution is essentially linked to indicesof precipitation (0.49 for the year, and 0.41 forboth the driest and wettest months) and to alesser extent temperature during the coldestmonth (0.33) and number of frost days (- 0.31). The suitability map is based on all theENFA factors. The jack-knife cross-validationshows that predicted suitability exceeds 0.5 in69.6% of the validation cells, which proves thatthe model is well supported.

506 BS 55

Fig. 3. Habitat-suitability map for Ilex, as computed by Ecological-Niche Factor Analysis (ENFA). Ilex occurrences fromwhich ENFA was computed are illustrated with black dots. The habitat suitability values are represented as follows: whiteareas 0-20%, light-gray areas 20-40%, gray areas 40-60%, dark-gray areas 60-80% and black areas 80-100%. Hatched areascorrespond to the extant distribution of the genus. The model accuracy is given by the strong values of the mean (65,53)and the standard deviation (28,04) of values predicted by the model for the occurrences.

The map of potential distribution obtained(Fig. 3) is consistent with the distribution ofthe genus at present. However, due to all thegeographical occurrences being from Centraland South America, the model has a lesser pre-dictive probability for the northern hemi-sphere (sampling bias). Nevertheless, themodel is sufficiently relevant to allow an inter-pretation of the differences between potentialand observed distribution compared to thepaleo-environmental variations.

Pollen fossil distributionPollen fossil records have been plotted fromthe Mid-Cretaceous through to the Miocene.Figure 4 shows the geographical distribution ofIlex fossil records at different geological peri-ods considering continental drift.

DiscussionPast species diversityPalynological data indicate only the presenceor absence of the genus in a place at a giventime, but give no information on the specificdiversity of Ilex in the past as the species cannotbe distinguished based on pollen morphologyonly. In terms of distribution of the occur-rences in space and time, such records do notgive any information on the migratory path-ways or the centres of diversity.

As outlined by Cuénoud et al. (2000), pollenfossil records taken from the literature seem toindicate that the Ilex lineage was already cos-mopolitan long before the end of the Creta-ceous. Cuénoud et al. (2000) and Manen et al.(2002) arrived at the conclusion that the originof Ilex is c 50 mya, on the basis of phylogeneticstudy of extant taxa. They do not dispute thepossibility that older ancestors existed, butthose would belong to currently extinctbranches.

The high homogeneity of extant species ofthe genus, in spite of at least 50 million years of

evolution and a very broad distribution, sug-gests that speciation within the genus is veryslow (but see Burnham & Graham 1999).

Differentiation of extant Ilex speciesThe very complex history of the genus Ilex is re-flected in our incapacity to produce a relevantcladogram of morphological characters, whichis also underlined by the incongruence ob-served between the plastid and nuclear phylo-genies. The great potential of inter-specific hy-bridization of Ilex (Galle 1997), associated withmultiple migration pathways defined by Cué-noud et al. (2000) could explain our incapabili-ty to achieve a hierarchical arrangement of thespecies. It thus appears to be impossible to usethe evolutionary tendencies of the genus toanalyse the cladograms on a hierarchical basis.Several studies of wood anatomy (Baas 1973),leaves (Baas 1975), and pollen (Lobreau-Callen1975; Martin 1977), show that it is impossible todistinguish the different species on the basis ofthese characters. Furthermore, these authorsobserved great homogeneity within the extantspecies throughout the world.

At a morphological level, the extant speciesare often defined by continuous variation offorms and/or dimensions. Within the study ofSouth American species, the difficulty over sep-arating the different species has not beenresolved. Often, the samples can be classifiedon a gradient which passes imperceptibly fromone species to the other (e.g., Ilex kunthianaTriana, I. myricoides Kunth, I. ovalis (Ruiz &Pav.) Loes., I. rupicola Kunth, I. scopulorumKunth, I. uniflora Benth.). A biometric study inprogress on Ilex laurina Kunth, I. yurumanguinisCuatrec. and I. maxima W. J. Hahn confirmsthe existence of this gradient without the possi-bility of morphologically separating them withthe exception of the typical specimens of eachtaxon. A certain number of samples could beinterpreted as being hybrids between I. laurinaand I. yurumanguinis.

BS 55 507

508 BS 55

Fig. 4 (A-B). Ilex fossil distributions at different geological periods. Position of landmasses according to Scotese 2003. Posi-tion of pollen according to Martin (1977), Muller (1981) and Wijninga and Kuhry (1993). A) Miocene. B) Oligocene. Theperiods of time corresponding at the position of the continents are: A) 10 mya. B) 30 mya.

BS 55 509

Fig. 4 (C-D). Ilex fossil distributions at different geological periods. Position of landmasses according to Scotese 2003. Posi-tion of pollen according to Martin (1977), Muller (1981) and Wijninga and Kuhry (1993). C) Eocene. D) Paleocene. Theperiods of time corresponding at the position of the continents are: C) 40 mya. D) 60 mya.

510 BS 55

Fig. 4 (E-F). Ilex fossil distributions at different geological periods. Position of landmasses according to Scotese 2003. Posi-tion of pollen according to Martin (1977), Muller (1981) and Wijninga and Kuhry (1993). E) Late Cretaceous. F) Mid-Cre-taceous. The periods of time corresponding at the position of the continents are: E) 70 mya. F) 90 mya.

These facts suggest that the number ofextant species of Ilex could be greatly reducedafter taxonomic study.

Extant distributionA disjunct distribution pattern is observedbetween eastern Asia and eastern North Amer-ica, as there are no Ilex species along the west-ern North American coast. This disjunct distri-bution pattern has been known for many yearsand for numerous taxa (Graham 1972; Raven1972; Raven & Axelrod 1974; Boufford &Spongberg 1983).

This general phytogeographical pattern canbe directly explained by the broad distributionof elements of northern hemisphere forestsduring the mid-Tertiary and subsequentcolonisations in north-western America andwestern Europe in response to climatic coolingat the end of the Tertiary and during the Qua-ternary (Wen 1999). The Bering and northernAtlantic land bridges probably contributed tothe floristic exchanges between southeasternAsia and North America. Tiffney (1985) pro-posed five possible principal periods for theseexchanges: Pre-Tertiary, beginning of Eocene,end of Eocene-Oligocene, Miocene, and theend of the Tertiary-Quaternary.

In eastern Asia, the majority of genera with adisjunct distribution between southeasternAsia and eastern North America are present inthe Sino-Japanese floristic area (Boufford1998). This area extends from western Yunnanand Sichuan, through eastern and southernChina, to eastern Korea and Japan (Wen1999). The Sino-Japanese area is additionallyrich in endemics (Wen 1999).

Ilex seems to follow this pattern of distribu-tion for the eastern and south-eastern Asianand North American species. In the formerarea great species diversity is found whereas inthe latter only few species occur. It is interest-ing to note that deciduous species are only pre-sent in North America and eastern Asia. The

Bering land bridge probably allowed the pas-sage of deciduous taxa of Ilex for a longerperiod of time than for the evergreen ones,because of the capacity of deciduous species tosurvive in a colder climate by losing theirleaves. The deciduous species seem to be themost recently evolved as an adaptation to thecool periods that appeared during the late Ter-tiary. But no information is available thatwould allow us to know when deciduous taxaappeared, or on which continent, or if theyappeared separately on each continent. Plastiddata suggest it happened twice, both in NorthAmerican/Asia disjunctions.

Wen (1999) showed that most intercontinen-tal species pairs are not sister species, whichcould mean that species pairs found in bothcontinents do not necessarily have a direct phy-logenetic link. Three reasons could be invokedto explain this morphological similarity: (1)the pairs of species have been separated for avery long time and did not evolve much beforeor after their separation (Wen 1999), and amorphological “dormancy” theory (stasis) issuggested to explain this, (2) the morphologi-cally similar species are the product of similarevolution in distant, but equivalent environ-ments. Qiu et al. (1995) believe that the similartype of habitat can exert a comparable pres-sure, which influences in a convergent way themorphological adaptation, and 3) pairs ofspecies are not so morphologically similar aspreviously suggested.

These observations could explain why theplastidic, nuclear and morphological phyloge-nies of the Ilex are not congruent.

The specific relations between North Amer-ica and south-eastern and eastern Asia shouldbe studied more deeply to see if sister speciesare present on these two continents. Some ofthe deciduous Ilex species living on one conti-nent are considered to be close to species liv-ing on the other continent by Galle (1997).This suggests that these species could be sister.

BS 55 511

In the plastid phylogeny, deciduous species arelimited to Asian/N. American clades I and II(Manen et al. 2002). However, this characterdoes not seem to prevent interspecifichybridizations between deciduous and ever-green species. Thus Galle (1997) observed pos-sible natural hybridisations in seedling bedsbetween two North American species: I. deciduaWalter (deciduous) and I. opaca Aiton (ever-green).

Potential distributionThe current distribution of Ilex seems to bedirectly related to precipitation, minimumtemperatures and number of frost days. Theprojection of the world potential distributioncalculated on the basis of tropical Americanoccurrences (Fig. 3) gives a map which largelyresembles the current distribution of Ilex, ifone considers a potential distribution between20% and 100% of habitat suitability. However,differences are observed in Europe and SouthAfrica, which have a potential area of distribu-tion smaller than actual, and along the westcoast of Canada, southern coast of Chile, NewZealand and eastern coast of Australia, wherethe potential distributions are larger than theextant ones.

Because of the differences in seasonalitybetween the northern and the southern hemi-spheres, only the monthly averages of themonth which expresses an annual limit of agiven climatic variable were considered. Thusfor example it is the monthly average of thecoldest month for each point independentlythrough all the twelve months which is used toestablish the layer of the minimum tempera-ture. Our model could have been more preciseconsidering each month as a variable. But asour presence data cover primarily the tropicsof Central and South America, a model usingall monthly averages would have increased thearea of potential distribution for the habitatsuitability values between 80% and 100% in the

southern hemisphere, whereas it would havedecreased it in the northern hemisphere. Tocorrect this artifact due to sampling bias in thesouthern hemisphere it would be necessary toreverse monthly data in the northern hemi-sphere, i.e. to make it coincide between theseasons of both hemispheres.

Ilex is a genus represented by plants growingin relatively wet places and is mostly found inforests (Martin 1977). Even if Ilex sometimesgrows in drier areas, e.g. on tops of hills in thecentre of primary forests, or in secondary forestformations, or in savannas, the genus is alwaysnear water (forest gallery, swamp). Thus Ilexseems to be able to survive in drier types of veg-etation if it receives a water complement. As aconsequence even if the potential distributionis more restricted than the extant one, particu-lar local climatic conditions approaching opti-mal ones would allow the genus to survive in ar-eas indicated as unfavourable at the resolutionof the map. These particular climatic condi-tions cannot appear on a potential map of dis-tribution using 0.5° square pixel. These micro-climatic conditions could explain the occur-rences of Ilex where the ecological niche proba-bility is low. However, it seems that the thresh-old of 20% of habitat suitability is the lower lim-it in our modelled pattern to find an Ilex plant.

Our modelled pattern corresponds ratherwell to the reality of the potential distributionof the genus. It requires improvements byintroducing more events, particularly in thenorthern hemisphere and temperate areas,and by adding other climatic variables. How-ever, general differences between the modeland the observed distributions could also bethe result of earth’s climatic history which, willbe discussed further.

MigrationBecause the fruit of Ilex is adapted to bird dis-persal and the embryo can take between 2 to 8years to germinate (Galle 1997), conditions for

512 BS 55

successful long-distance dispersal are met. Tak-ing into account the study of Myking (2002) onthe dissemination of Ilex aquifolium L., thegenus Ilex would take 100,000 years to migratearound the earth under good conditions byterrestrial pathways. Bird-effected dispersalhighly accelerates this speed, and moreovermakes it possible to place the seeds directlyinto favourable biotopes, since the birds tendto seek similar climatological conditions andbiotopes throughout their migration. Crossingoceans can be achieved by birds in a few days(Schlüssel pers. comm.). Alerstam (1990) indi-cated a 20-hour, non-stop flight to cross theGulf of Mexico (1000 km) for the Turdidea(typical Ilex fruit dispersors) in their migrationway from United States to Yucatán. In addition,the probability that a seed carried by themarine currents can cross is weak but exists.

PaleogeographyBroad distribution of pollen of Ilex at the endof the Cretaceous and throughout the Tertiarysuggests that this genus was widespread at thattime. Projection of pollen fossil occurrenceson paleo-environmental maps drawn fromBeerling and Woodward (2001) (data notshown) showed that in the late Cretaceous, asin the Eocene, Ilex was found in zones sup-posed to have at least 20° C minimum averagesannual temperature and monthly precipitationaverage of 100-125 mm. These are coarse dataand thus represent only tendencies in tempera-ture and rainfall variables. But they correspondrelatively well to the ecological preferencesobserved for extant species.

The oldest Ilex pollen, from Australia, wasdated to be from 90 mya. There are fiverecords of Ilex in the Cretaceous, which are dis-tributed in Africa, southeastern Australia,northwestern Borneo, California and formerU.S.S.R. These data do not give any indicationon the place of origin of the genus. Althoughdata on Cretaceous Ilex fossils should be con-

firmed, nevertheless, one must wonder howthis genus could have been so widespread atthat time, since the continents were alreadyquite separate.

A first assumption would be that the genusIlex is even older, and that its origin goes backto the time when the continents were stillunited (early Cretaceous). Willis and McElwain(2002) in particular place the origins of theangiosperms approximately 140 mya. It isstrongly unlikely that the genus Ilex, as recog-nised today, was already present at that time.APG (1998) places the Aquifoliaceae in a basalposition of the Asterideae, which suggests amuch more recent appearance of this familywithin the angiosperm phylogeny.

The current distribution pattern of thegenus Ilex and the available palynologic datasuggest an Arcto-Tertiary origin of the family.The current distribution of diversity centreswould thus be directly related to the evolutionof paleo-environmental conditions. The genuswould have disappeared from the continentswhich would have undergone cooling eventsduring Miocene until the glaciations of theQuaternary. The study of paleo-environmentalmodels (Beerling & Woodward 2001) lead usto believe that no climatic variation, besidesthat of the Quaternary between 25,000 and15,000 years ago could have been the cause ofthe extinction of some species of Ilex from cer-tain areas of the world, e.g. Europe, Africa orNew Zealand, where specific diversity is verylow for the first two areas and null for the last(no extant Ilex in New Zealand). Paleo-environ-mental considerations are discussed further,and references are drawn from Adams (1997)and Adams and Faure (1997).

Eurasia – In the Tertiary, pollen of Ilex wasfound throughout Asian continent and thegenus was widespread from Europe to China.During the Quaternary, conditions all overnorthern Eurasia appear to have been dry andthe continent was treeless. It was dominated by

BS 55 513

polar desert or semi-desert steppe-tundra.These conditions also extended towards thesouth in Europe, western and central Asia. Inboth tropical and temperate southern Asiaconditions were much drier and colder thannow, with diminished areas of forests andexpanded areas of desert. It thus seems thatthese climatic conditions made it possible forIlex to survive in certain areas. The climaticchanges did not completely extinguish theextant species, but instead probably isolatedthem in refugia. This isolation may be thecause of the large number of species in south-eastern and eastern Asia today. Isolation couldcreate conditions for allopatric speciationevents without a complete genetic separationof the species, which would maintain thepotential of inter-specific hybridisation in thecase of Ilex. With later climatic warming thetaxa would again come into contact andhybrids appeared. South-eastern Asia becamethe region which offered the most refugia dur-ing the successive cooling periods of the Qua-ternary. It has been considered as the center oforigin for Ilex by Hu (1967), but this has notbeen confirmed by the palynological studieswhich show Ilex was already widespread (Mar-tin 1977).

The high specific diversity in this area couldhave two causes which do not exclude eachother: 1) the rate of extinction in the genuswas weaker in south-eastern Asia than in otherareas of the world due to greater availability ofrefugia during the Quaternary and 2) a greaternumber of sister species were derived byallopatric speciation during periods of expan-sion and regression of refugia and later byhybridization of taxa when they came back intocontact.

During the Tertiary, Europe was covered byan Arcto-Tertiary flora which included Ilex. Alot of Ilex fossil pollen grains have been foundfrom this period. During the Quaternary, cli-matic conditions were extreme, very cold and

very dry, and it is supposed that Ilex was mostlyabsent from the continent. Only four speciesare found in Europe (including the CanaryIslands, Madeira and Azores) today, Ilexcanariensis Poir., Ilex colchica Pojark., Ilex peradoAiton, and Ilex aquifolium L., which are allclosely related. A common ancestor could havebeen the only survivor of the glaciations. It mayhave found refuge in the south of Spainand/or in the Canary Islands. If conditionsexcluded its survival during the Quaternary itspresence could be the result of a recolonisa-tion. The four species present in Europe,although they are quite isolated from eachother are nevertheless relatively close to eachother in their morphology. This could meanthat they result from a unique taxon that waswidespread during the Tertiary and whichwould have survived in disjunct areas duringthe Quaternary.

North America – During the Tertiary, fossilIlex pollen was present on the North Americancontinent. The presence of the Quaternary icesheet implies that Ilex was absent from all overnorthern North America, nevertheless somespecies may have existed in refugia in theforests of the south-east (Webb & Overpeck,http://web.ngdc.noaa.gov/paleo/image/-gsafinal.gif). Availability of refuge areas couldbe an important factor in the diversification ofthe species and therefore, could explain theabsence of Ilex in western North Americadespite a potential distribution along the west-ern coast of Canada.

Central and South America – Central Americawas formed relatively recently (Burnham &Graham 1999) and no Ilex pollen older than 10mya has been found. On the other hand, inSouth America, three Ilex pollen stations of 40mya in the north and 60 mya in the south havebeen found. We can conclude that the genuswas present in South America before the junc-tion with North America was formed. A signifi-cant event on the South American landmass is

514 BS 55

the uplift of the Andes. The presence of Ilexpollen at the beginning of the uplift of theAndes allows us to suppose that the genusshifted up with the uplift of the Andes. Gradu-ally climatic conditions changed and somepopulations were isolated in valleys by highmountains, allowing for allopatric speciation.

It seems that Quaternary cooling did nothave such an important influence on Centraland South America as it did on Europe andNorth America. Central and South Americaprobably had refugia in the tropical forests,such as in Panama and the Amazonian basin.The connection between the Andes and Cen-tral America probably allowed the Andeanspecies, driven out by unfavourable climaticconditions in the Quaternary, to take refuge inless arid areas of Central America. The Andeanuplift and the extensions and regressions offavourable habitats during the Quaternary andthe absence of desertification probably sup-ported specific diversity of Ilex in this region.

Australia and New Zealand – Ilex pollen fromsouthern and eastern Australia has been foundfrom the Tertiary and in New Zealand from themiddle Tertiary. During the Quaternary,species took refuge in the northern Australia(Martin 1977). At that time the centre of Aus-tralia became a desert and the south-easternforest went extinct. A bridge connected Aus-tralia to New Guinea. Some rain forests proba-bly survived in New Guinea and in the farnorth of Australia implying potential refugiafor Ilex. In New Zealand forests probably disap-peared completely leading to the extinction ofthe genus in these islands.

Africa – It is surprising to note that very fewIlex pollen grains have been identified from theTertiary of Africa. Only two occurrences areknown, dated 85 mya and 5 mya, respectively.Nothing indicates that the climate during theTertiary or Quaternary in Africa could have ledto the extinction of the genus. Indeed, duringthe coldest period of the Quaternary refugia

for tropical forests, and in drier areas forgallery-forests, existed. In spite of that, thegenus is represented only by one species, I.mitis (L.) Radl. This single species is found inthe southern part of the continent south ofequator, excluding the desert regions of south-western Africa. It is also present in Madagascar.

A first hypothesis could be that Ilex was notwidespread in Africa during the Tertiary andthat it was only present in areas that underwentthe strongest climatic variations during theQuaternary. Another hypothesis would be thatIlex species were widespread during the Ter-tiary, but species were not isolated in refugiaduring the cooling periods and they werealmost eliminated at that time, and/or later,during the cooling periods of the Quaternary.The genus would finally almost disappear fromthis continent, Ilex mitis being the only speciesto survive.

But if all species of Ilex were eliminated fromAfrica, its presence could still be the result of asubsequent colonisation. The fact that I. mitis iswell established in Madagascar could also sug-gest a colonization of continental Africa fromthis island. The Malagasy flora seems to passmore easily from the island to the African con-tinent than the opposite. In addition, the ori-gin of a great number of Malagasy speciescould be Asia, due to favourable marine cur-rents which cross the Indian Ocean and whichwould support long distance dispersal (Gautierpers. comm.). This could explain why I. mitis isclose to a certain number of Asian species inthe nuclear and plastid clades (Manen et al.2002). Additional studies are needed.

ConclusionsThe genus Ilex was probably widespread fromthe beginning of the Tertiary, and perhapsbefore. The first Ilex pollen fossils are datedolder than 85 mya, and were found in Africa,Australia and Asia. Consequently it is impossi-

BS 55 515

ble to have an idea of the origin of the genuson the basis of palynological studies. In addi-tion, a calculation based on the molecularclock for the extant Ilex species gives an originof approximately 50 mya. This is interpreted asbeing the age of the oldest ancestor of the cur-rent species. Any trace of even older ancestorsis lost with the extinction of the brancheswhich corresponded to them.

The study of the extant species shows a greathomogeneity of floral morphology within thegenus in spite of, according to the molecularclock, approximately 50 million years of evolu-tion. This fact suggests a “morphological sta-sis,” that is to say a great stability of charactersover a very long time period. In addition, itseems that different species hybridize leadingup to morphological and molecular homo-geneisation. This apparent great stability ofcharacters and the possibility of hybridisationmakes the elucidation of relations betweenspecies even more difficult.

Attempts to reconstruct phylogenies ofextant species based on sequencing of plastidand nuclear DNA, confirm the potential tohybridize. A phylogeny based on morphologi-cal characters was not resolved and brought nonew information to the problem. Comparisonbetween morphological characters and plastidphylogeny, which seemed to give the most sig-nificant results compared to the nuclear one,showed that there was no correlation betweenthem. All the above mentioned factors high-light the enormous difficulty encounteredwhen attempting to connect the evolutionaryhistory of the genus with the extant distribu-tion, and in determining centres of origin forthe genus. Information currently available can-not give any indication of the number ofspecies present in the past, and it gives only afew indications of possible migratory pathwaysof these species according to extant distribu-tions.

A statistical analysis based on specimen

records in our database (more than 3500 indi-viduals from Central and South America)made it possible to propose a potential distrib-ution of the genus Ilex. The potential distribu-tion corresponds, in the broad outline, to theextant distribution except for some areas inwestern North America and in Africa. Theassumption made is that the genus was wide-spread at the end of the Tertiary and that it hasbeen restricted to the current distribution dueto colder and drier climatic conditions duringthe Quaternary. The very high number ofspecies in south-eastern Asia and South Amer-ica could be directly related to these two areasacting as refugia during the Quaternary, and tothe slow uplift of the Andes during the Tertiaryin South America.

The situation seen in Africa is not clear.Either Ilex was never widespread on this conti-nent during the Tertiary, or it was widespreadbut climatic conditions of the Quaternary weremore drastic than currently knowledge sup-poses implying widespread extinction in Africa(Raven & Axelrod 1974).

To improve our knowledge of Ilex distribu-tion patterns, it will be necessary to work onseveral levels:

Complete the pollen data, particularly forSouth America and Africa. In addition, itwould be interesting to have informationabout the presence of Ilex in the Antarctic dur-ing the Tertiary (Partridge pers. comm.).

Improve our knowledge of the pattern ofpotential distribution by integrating data fromtemperate zones of the northern hemisphere,and increasing the number of climatic vari-ables. This will better define the ecologicalniche and allow us to compare it to paleoenvi-ronmental patterns.

Improve our knowledge of species variability.This will allow us to have a better understand-ing of the different taxa and clarify better theircurrent distribution patterns.

516 BS 55

Acknowledgements

We thank all the herbaria mentioned in thetext for kindly lending us Ilex material; CyrilleChatelain for his invaluable council concern-ing GIS; Michelle Price for checking the Eng-lish text, André Schlüssel for suggestions dur-ing the drafting of the manuscript.

Literature cited

Adams, J.M. 1997. Global land environments since the last inter-glacial. Oak Ridge National Laboratory, TN, USA.http://www.esd.ornl.gov/ern/qen/nerc.html

Adams, J.M. & Faure, H. (eds.), 1997. QEN members. Reviewand Atlas of Palaeovegetation: Preliminary land ecosystemmaps of the world since the Last Glacial Maximum. OakRidge National Laboratory, TN, USA.http://www.esd.ornl.gov/ern/qen/adams1.html

Alerstam, T. 1990. Bird Migration. Cambridge UniversityPress, Cambridge.

APG. 1998. An ordinal classification for the families offlowering plants. Ann. Missouri Bot. Gard. 85: 531-553.

Austin, M.P., Nicholls, A.O., Doherty, M.D. & Meyers, J.A.1994. Determining species response functions to anenvironmental gradient by means of a beta-function. J.Veg. Sci. 5: 215-228.

Baas, P. 1973. The wood anatomical range in Ilex (Aquifo-liaceae) and its ecological and phylogenetic significance.Blumea 21: 193-258.

Baas, P. 1975. Vegetative anatomy and affinities of Aquifoli-aceae, Sphenostemon, Phelline and Oncotheca. Blumea22: 311-407.

Beerling, D.J. & Woodward, F.I. 2001. Vegetation and Terres-trial Carbon Cycle: Modelling the first 400 million years. Cam-bridge University Press, Cambridge.

Behling, H., Negrelle, R.R.B. & Colinvaux, P.A. 1997. Mod-ern pollen rain data from the tropical Atlantic rain for-est, Reserva Volta Velha, south Brazil. Rev. Palaeobot. Paly-nol. 97: 287-299.

Boufford, D.E. 1998. Eastern Asian – North Americanplant disjunctions; opportunities for further investiga-tion. Korean J. Pl. Taxon. 28: 49-61.

Boufford, D.E. & Spongberg, S.A. 1983. Eastern Asian –eastern North American phytogeographical relation-ships – a history from the time of Linnaeus to the twenti-eth century. Ann. Missouri Bot. Gard. 70: 423-439.

Burnham, R.J. & Graham, A. 1999. The history of neotrop-ical vegetation: new developments and status. Ann. Mis-souri Bot. Gard. 86: 546-589.

Cronquist, A. 1981. An integrated System of Classification ofFlowering Plants. Columbia University Press, New York.

Cuénoud, P. 1998. Phylogénie moléculaire, taxonomie et biogéo-graphie du genre Ilex L. (Aquifoliaceae). Thèse n° 3046. Uni-versité de Genève. Département de botanique et biolo-gie végétale.

Cuénoud, P., del Pero Martínez, M.A., Loizeau, P.-A.,Spichiger, R., Andrews, S. & Manen, J.-F. 2000. Molecularphylogeny and biogeography of the genus Ilex L.(Aquifoliaceae). Ann. Bot. (Oxford) 85: 111-122.

Dudley, T.R. & Sun, S.C. 1983. Aquifoliaceae. The 1980Sino-American botanical expedition to Western Hubeiprovince, Poeple’s Republic of China. J. Arnold Arbor. 64:63.

Fielding, A.H. & Bell, J.F. 1997. A review of methods for theassessment of prediction errors in conservation pres-ence / absence models. Environm. Conservation 24: 38-49.

Galle, F.C. 1997. Hollies. The Genus Ilex. Timber Press, Port-land.

Giberti, G.C. 1994. Aquifoliaceae. In: Spichiger, R. & Ramel-la, L. (eds.), Fl. Paraguay. Vol. 24. Editons des Conserva-toire et Jardin botanique, Genève, Switzerland. Pp. 1-34.

Graham, A. (ed.), 1972. Floristics and Paleofloristics of Asiaand Eastern North America. Elsevier, Amsterdam.

Hastie, T. & Tibshirani, R. 1987. Generalized additive mod-els: some applications. Journal of the American StatisticalAssociation 82(398): 371-386.

Hill, R.S. 2001. Biogeography, evolution and palaeoecol-ogy of Nothofagus (Nothofagaceae): the contribution ofthe fossil record. Austral. J. Bot. 49: 321-332.

Hirzel, A.H., Hausser, J., Chessel, D. & Perrin, N. 2002.Ecological-niche factor analysis: How to compute habi-tat-suitability maps without absence data? Ecology 83:2027-2036.

Hu, S.-Y. 1949. The genus Ilex in China, [I]-II. J. ArnoldArbor. 30: 233-344, 348-387.

Hu, S.-Y. 1967. The evolution and distribution of thespecies of Aquifoliaceae in the Pacific Area (1). J. Jap.Bot. 42: 13-27.

Hutchinson, G.E. 1957. Population studies – Animal ecol-ogy and demography – Concluding remarks. Cold SpringHarbor Symp. Quant. Biol. 22: 415-427.

Hyde, H.A. 1961. Welsh Timber Trees. Ed. 3. NationalMuseum of Wales, Cardiff.

Judd, W.S., Campbell, C.S., Kellogg, E.A. & Stevens, P.F.1999. Plant Systematics: a Phylogenetic Approach. SinauerAssociates, Sunderland.

Lavin, M. & Luckow, M. 1993. Origins and relationships oftropical North America in the context of the boreotrop-ics hypothesis. Amer. J. Bot. 80: 1-14.

Lobreau-Callen, D. 1975. Les variations dimensionnellesdu pollen du genre Ilex (Aquifoliaceae) et leurs rap-ports avec le climat. Bull. Soc. Bot. France 122: 179-199.

BS 55 517

Loesener, T. 1901. Monographia Aquifoliacerum. Pars I.Nova Acta Acad. Caes. Leop.-Carol. German. Nat. Cur. 78: 1-598.

Loesener, T. 1908. Monographia Aquifoliacerum. Pars II.Nova Acta Acad. Caes. Leop.-Carol. German. Nat. Cur. 89: 1-313.

Loesener, T. 1942. Aquifoliaceae. In: Engler, A. & Prantl, K.(eds.), Die Natürlichen Pflanzenfamilien, 20b. Ed. 2. Wil-helm Engelmann, Leipzig. Pp. 36-86.

Loizeau, P.-A. 1994. Les Aquifoliaceae péruviennes (élé-ments pour une révision des Aquifoliaceae néotropi-cales). Boissiera 48: 1-306.

Loizeau, P.-A., Savolainen, V., Andrews, S. & Spichiger, R.(in press). Aquifoliaceae. In: Kubitzki, K. (ed.), The Fam-ilies and Genera of Vascular Plants. Springer-Verlag, Berlin.

Loizeau, P.-A. & Spichiger, R. 1992. Proposition d’une clas-sification des inflorescences d’Ilex L. (Aquifoliaceae).Candollea 47: 97-112.

Maddison, W.P. & Maddison, D.R. 1992. MacClade, version3. Analysis of Phylogeny and Character Evolution. SinauerAssociates, Sunderland, Massachusetts.

Manen, J.-F., Boulter, M.C. & Naciri-Graven, Y. 2002. Thecomplex history of the genus Ilex L. (Aquifoliaceae):evidence from the comparison of plastid and nuclearDNA sequences and from fossil data. Pl. Syst. Evol. 235:79-98.

Martin, H.A. 1977. The history of Ilex (Aquifoliaceae) withspecial reference to Australia: evidence from pollen.Austral. J. Bot. 25: 655-673.

McCullagh, P. & Nelder, J.A. 1989. Generalized Linear Models.Ed. 2. Chapman and Hall, London.

Muller, J. 1981. Fossil pollen records of extantangiosperms. Bot. Rev. (Lancaster) 47(1): 1-142.

Myking, T. 2002. Evaluating genetic resources of foresttrees by means of lifehistory traits – a Norwegian exam-ple. Biodiversity and Conservation 11: 1681-1696.

New, M., Hulme, M. & Jones, P.D. 1999. Representingtwentieth century space-time climate variability. Part I:development of a 1961-90 mean monthly terrestrial cli-matology. Journal of Climate 12: 829-856.

Peters, D. & Thackway, R. 1998. A New Biogeographic Region-

alisation for Tasmania. Parks and Wildlife Service GIS Sec-tion. Report for the National Reserve System ProgramComponent of the National Heritage Trust. ProjectNR002, Undertake biophysical regionalism for Tasma-nia.

Powell, M., Savolainen, V., Cuénoud, P., Manen, J.-F. &Andrews, S. 2000. The mountain holly (Nemopanthusmucronatus: Aquifoliaceae) revisited with moleculardata. Kew Bull. 55: 341-347.

Qiu, Y.-L., Chase, M.W. & Parks, C.R. 1995. A chloroplastDNA phylogenetic study of the eastern Asia – easternNorth America disjunct section Rytidospermum of Mag-nolia (Magnoliaceae). Amer. J. Bot. 82: 1582-1588.

Raven, P.H. 1972. Plant species disjunctions: a summary.Ann. Missouri Bot. Gard. 59: 234-246.

Raven, P.H. & Axelrod, D.I. 1974. Angiosperm biogeogra-phy and past continental movements. Ann. Missouri Bot.Gard. 61: 539-673.

Scotese, C. 2003. The Earth System History GIS. PaleomapProject: http://www.scotese.com

Setoguchi, H. & Watanabe, I. 2000. Intersectional geneflow between insular endemics of Ilex (Aquifoliaceae)on the Bonin Islands and the Ryukyu Islands. Amer. J. Bot.87: 793-810.

Standley, P.C. 1931. Aquifoliaceae. Studies of Americanplants – V. Publ. Field Columbian Mus., Bot. Ser. 8: 315-316.

Swofford, D.L. 2000. PAUP*. Version 4. Phylogenetic analysisusing parsimony (*and other methods). Sinauer Associates,Sunderland, Massachusetts.

Tiffney, B.H. 1985. The Eocene north Atlantic land bridge:its importance in Tertiary and modern phytogeographyof the northern hemisphere. J. Arnold Arbor. 66: 73-94.

Wen, J. 1999. Evolution of eastern Asian and eastern NorthAmerican disjunct distributions in flowering plants.Annual Rev. Ecol. Syst. 30: 421-455.

Wijninga, V.M. & Kuhry, P. 1993. Late Pliocene paleoecol-ogy of the Guasca Valley (Cordillera Oriental, Colom-bia). Rev. Palaeobot. Palynol. 78: 69-127.

Willis, K.J. & McElwain, J.C. 2002. The Evolution of Plants.Oxford University Press, Oxford.

518 BS 55

BS 55 519

Appendix 1: The 47 Ilex species selected for the morphological phylogeny. Descriptions were based on cited literature andspeciminens seen which are indicated with the collector, the collector’s number, the acronym of the herbarium and theirsexual status (f: female, m: male, st: sterile).

Taxa Literature and Specimens seen

I. amelanchier M. A. Curtis Loesener 1901, Galle 1997, Drummond s.n. 1832 BM f, Leonard 1728 BM f, Curtis s.n. 1852G f

I. anomala Hook. & Arn. Loesener 1901, Galle 1997, Faurie 282 G mf, Degener 20061 G f, Degener 3316 G m, Degener3324 G m,

I. argentina Lillo Galle 1997, Beck 9660 G m, Venturi 4623 S m, Giberti 508 G f, Venturi 9990 S f

I. brasiliensis (Sprengel) Loes. Giberti 1994, Regnell II 56 S m, Mosén 4243 S f, Mosén 1822 S f

I. brevicuspis Reissek Giberti 1994, Balansa 1793 S f, Hatschbach 30782 MU m

I. canariensis Poir. Loesener 1901, Galle 1997, Mandon s.n. 1865-1866 G m, Mason 349 G f, Asplund 1112 G m

I. cassine L. Galle 1997, Standley 190 BM f, Tracy 6829 BM mf, Drummond s.n. BM st, Curtiss 1747 BM m

I. crenata Thunb. Loesener 1901, Galle 1997, Anonymous 155 G m, Kasapligil 3660 G f, Faurie 3114 G m

I. decidua Walter Loesener 1901, Galle 1997, Ventenat s.n. G m, Godfrey 54470a G m, Eisenbeiss & Dudley s.n.1979 G f, Bosc s.n. G f, Godfrey 54549 G f

I. dumosa Reissek Giberti 1994, Schinini 31582 G m, Hatschbach 22945 S m, Schinini 31420 G f

I. glabra (L.) A. Gray Galle 1997, Bartram 445 BM mf, Bray 8423 BM m, Rugel 3365 BM f

I. goshiensis Hayata Galle 1997, Furuse 2498 G m, 2768 K f, 2959 K m, 3550 K f

I. guianensis (Aubl.) Kuntze D’Arcy & al. 15500 G m, 15506 G m, Churchill 4284 G m, Gentry & al. 47534 COL m, 47555COL f, Werff, van der & al. 6153 G f, 6916 G m

I. hippocrateoides Kunth Humboldt & Bonpland s.n. P m, Núñez & al. 9034 G st, 9904 G f, Hamilton & Holligan 661K st, Smith 2723 G f

I. integerrima (Vell.) Reissek Loesener 1901, Freyreis s.n. S f

I. latifolia Thunb. Loesener 1901, Galle 1997, Maximowicz s.n. G mf

I. laurina Kunth Bernardi 1045 NY m, Sneidern 4356 F m, Lehmann B.T.668 G, NY m, B.T.959 NY f, Williams6995 COL, F f, Cuatrecasas 18281 F, G, US f, Humboldt & Bonpland s.n. W m

I. leucoclada (Maxim.) Galle 1997, Wilson 7099 BM mf, Wilson 7630 BM fMakino

I. liebmannii Standl. Standley 1931, Galle 1997, Liebmann 14927 G f (fragments).

I. longipes Trel. (= I. collina) Loesener 1901, Galle 1997, Nogle s.n. 1956 BM f, Dudley s.n. 1976 BM m, K f

I. macrocarpa Oliver Loesener 1901, Galle 1997, Linsley Gressitt 1736 G f

I. macropoda Miq. Loesener 1901, Galle 1997, Tschonoski s.n. 1864 G mf, Watari s.n. 1951 G f, Anonymous s.n.1888 G m, Nagamasu 5457 G m

I. maximowicziana Loes. Loesener 1901, Galle 1997, Furuse 3400 G m, Furuse 1060 K f, Furuse 2883 K f,.

I. micrococca f. pilosa S. Y. Hu Galle 1997 (I. micrococca), Henry 11974a K f, Fang 5656 K f, Forrest 8651 K f, 15749 K m

I. microdonta Reissek Hatschbach 24206 S f, 22837 COL m

I. mitis (L.) Radlk. Galle 1997, Pegler 1366 BM m, Zeyher 1129 BM m, Bolus 5202 BM mf, Drege s.n. BM mf

I. mucronata (L.) M. Powell, Loesener 1901, Chapman s.n. 1844 G m, Pringle s.n. 1877 G f, Cinq-Mars 67-54 G mV. Savolainen & S. Andrews

520 BS 55

Taxa Literature and Specimens seen

I. mutchagara Makino Furuse 4812 K m

I. oppositifolia Merrill Galle 1997, Clemens 31108 BM f, 31375 BM st, 32249 BM f, 40539 BM m

I. pedunculosa Miq. Galle 1997, To Hara 2441 K m, Maximowicz s.n. K mf, Murata 15833 K f

I. perado Aiton Galle 1997, Loesener 1901, Reverchon 76 G f, Mason 343 G st

I. pseudobuxus Reissek Loesener 1901, Mosén 2898 S m, 3651 S f, Britez 1397 MBM f, Tessmann s.n. 1953 MBM m

I. pubescens Hook. & Arn. Loesener 1901, Galle 1997, Shiu Ying Hu 8996 G f, Tso 20100 G m, Lingnan 12016 G f

I. purpurea Hassk. Loesener 1901, Galle 1997, Chiao 1683 G f, Nagamasu 5516 G f, 5524 G m

I. repanda Griseb. Wright 1142 BR f, Wright 1142 K mf, Curtiss 88 K mf, Jack 4835 K f

I. revoluta Stapf Galle 1997, Clemens s.n. BM m, 32315 BM m, Gibbs 9127 BM f

I. rotunda Thunb. Galle 1997, Wright 184 K mf, Furuse 2695 K m, Furuse 2939 K f

I. rugosa F. Schmidt Loesener 1901, Galle 1997, Yatabe s.n. 1882 G f, Tschonoski s.n. 1864 G mf

I. serrata Thunb. Loesener 1901, Galle 1997, Maximowicz s.n. 1862 [Fudziyama] G f, Maximowicz s.n. 1862[Yokohama] G f, Franchet 178 G m

I. shennongjiaensis Dudley & Sun 1983, Galle 1997T.R.Dudley & S.C. Sun

I. sugerokii Maxim. Galle 1997, Wilson 7100 K mf, Fukuoka 1052 K m, Maximowicz s.n. K f, Wilson 7183 K f

I. teratopis Loes. Pearce s.n. K mf

I. theezans Reissek Giberti 1994, Dusén 15543 S m, Oliveira 682 MU f, Dusén s.n.1909 S f, Francisco & al.s.n.1999 G m

I. triflora Blume Galle 1997, Kerr 13277 BM f, 15523 BM f, 17771 BM m, Tsang 29153 G m, Taam 675 G m

I. verticillata (L.) A. Gray Galle 1997, Anonyme s.n. [1824] BM m, Euphrosin s.n. [1926] BM m, Judd s.n. [1932] BMf, Bauers 4 K f

I. vomitoria Aiton Galle 1997, Rugel 92 BM mf, Hood 1996 BM f, Miller 9460 BM f

I. yunnanensis Franch. Hu 1949, Galle 1997, Delavay 2673 K m, Forrest 10247 K m, Fliegner 1193 K f

Towards an understanding of the distribution of Ilex L.(Aquifoliaceae) on a World-wide scale

Documents

Transcript of Towards an understanding of the distribution of Ilex L.(Aquifoliaceae) on a World-wide scale