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«Doris Kahle-Zuber Diss. ETH No. 18080 Biology and evolution of the European mistletoe (Viscum album) A dissertation submitted to the ETH ZURICH for ...»

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Biology and evolution of the European

mistletoe (Viscum album)

Doris Kahle-Zuber

Diss. ETH No. 18080

Biology and evolution of the European mistletoe

(Viscum album)

A dissertation submitted to the


for the degree of


presented by

Doris Kahle-Zuber

Dipl. Natw. ETH

born March 26, 1970

citizen of Germany

accepted on the recommendation of Prof. Dr. Alex Widmer, examiner Prof. Dr. Matthias Baltisberger, co-examiner Dr. Rolf Holderegger, co-examiner Table of contents Summary


General introduction

Chapter I Biological Flora of Central Europe:

Viscum album L

Chapter II Genetic evidence for host specificity in the hemiparasitic Viscum album L.


Chapter III Phylogeography and host race differentiation in the European mistletoe (Viscum album L)


Appendix Notes on the Cretan mistletoe, Viscum album subsp. creticum subsp. nova (Loranthaceae/Viscaceae)


Curriculum vitae

Summary Parasitic interactions among organisms are highly diverse and play important roles in all ecosystems. These interactions span all group of organisms, from phages and viruses to bacteria, animals (mainly insects) and fungi to flowering plants. A well-known group of flowering plant parasites are mistletoes.

The European mistletoe Viscum album (Viscaceae) is a known pathogen, a pharmaceutical plant, and a symbol in mythology. The aim of this thesis was to provide new insights into the biology and evolution of this mistletoe with the help of molecular markers.

Viscum album is an evergreen hemiparasitic shrub, growing on different woody hosts.

Viscum is dioecious, insect pollinated and has fleshy fruits that are bird dispersed. Based on host specificity, three host races are distinguished in Europe: V. album album grows on a wide variety of deciduous trees, V. a. abietis is restricted to fir (Abies spp.), and V. a. austriacum occurs mainly on pine (Pinus spp.). A fourth host race, V. a. creticum, is associated with a sole pine host, Pinus halepensis ssp. brutia, and occurs exclusively on the island of Crete (CHAPTER I & APPENDIX).

Nuclear ribosomal DNA (nrDNA) ITS sequences and partial sequences of three noncoding chloroplast DNA (cpDNA) introns and spacers were used to assess genetic variation within and among these presumed host races. The molecular analysis of DNA variation supported the distinction of these four taxa, although sequence variation was low. We interpret the small genetic distances among host races as evidence for their recent formation.

The results further suggest that V. a. album and V. a. abietis are more closely related to each other than to V. a. austriacum and that hybridization is more likely between V. a. album and V. a. abietis. Indeed, putative hybrids found so far are the result of crosses between V. a.

album and V. a. abietis (CHAPTER II).

Chloroplast DNA fragment length polymorphisms were used to study genetic differentiation among the host races, population genetic structure, and to elucidate the postglacial migration history of Viscum album across the entire natural distribution range in Europe. The populations sampled belonged to the four closely related European Viscum races.

The molecular analysis of cpDNA variation further supported the distinction of four taxa on a much larger geographic and sampling scale. We further found evidence for phylogeographic structure in each of the three widely distributed host races. The parasitic life form and the scattered distribution of hosts may have favoured the high degree of population differentiation found in Viscum. Possible glacial refugia and postglacial immigration routes of mistletoe host


races were found to be only roughly comparable with those of their host trees, because each mistletoe host race is able to parasitize several tree species and may have switched among closely related hosts during glacial survival and subsequent recolonization.

Independent of host race, mistletoe haplotypes from Turkey were distinct and distant from those found elsewhere in Europe, suggesting that highly differentiated populations, and possibly new taxa, exist at the range limit of the species (CHAPTER III).


Parasitische Interaktionen zwischen Organismen sind vielfältig und spielen eine wichtige Rolle in allen Ökosystemen. Solche Interaktionen sind in allen Organismusgruppen vertreten von Phagen und Viren über Bakterien, Tiere (v.a. Insekten) und Pilzen bis hin zu Blütenpflanzen. Die Gruppe von Misteln ist ein bekanntes Beispiel für parasitische Blütenpflanzen.

Die Europäische Mistel Viscum album (Viscaceae) ist als Schädling, als Arzneipflanze und als ein Symbol in der Mythologie bekannt. Das Ziel der vorliegenden Arbeit ist es, mit Hilfe von molekularen Markern einen neuen Einblick in die Biologie und Evolution dieser speziellen Mistel zu geben.

Viscum album wächst als immergrüner halb-parasitischer Strauch auf zahlreichen verschiedenen Wirts-Holzpflanzen. Viscum ist zweihäusig, wird von Insekten bestäubt und bildet fleischige Beeren, die von Vögeln verbreitet werden. Aufgrund der Wirtsspezifität werden innerhalb Europas drei Wirtsrassen unterschieden: V. album album kommt auf verschiedenen Laubbäumen vor, V. a. abietis wächst auf Tannen (Abies spp.), und V. a.

austriacum ist vor allem von Kiefern (Pinus spp.) bekannt. Eine vierte Wirtsrasse, V. a.

creticum, kommt nur auf einer bestimmten Kiefernart (Pinus halepensis ssp. brutia) auf Kreta vor (KAPITEL I & APPENDIX).

Um die genetische Variation sowohl innerhalb als auch zwischen den möglichen Wirtsrassen zu untersuchen, wurden ITS Sequenzen der ribosomale Kern DNA (nrDNA) und Teilsequenzen von drei nicht kodierenden Chloroplast DNA (cpDNA) Abschnitten benutzt.

Die molekuare Analyse der Sequenzunterschiede unterstützt die Unterscheidung der vier Taxa, obwohl die Unterschiede gering waren. Wir nehmen an, daß die geringen genetischen Unterschiede ein Zeichen dafür sind, daß die Wirtsrassen erst kürzlich entstanden sind. Die Ergebnisse lassen weiter den Schluß zu, daß V. a. album und V. a. abietis näher miteinander verwandt sind als mit V. a. austriacum und daher eine Hybridisierung zwischen V. a. album und V. a. abietis am wahrscheinlichsten ist. Tatsächlich sind mögliche Hybride, die bisher gefunden wurden, ein Ergebnis einer Kreuzung zwischen V. a. album und V. a. abietis (KAPITEL II).

Chloroplast-DNA-Abschnitt-Längen-Polymorphismen wurden benutzt, um die genetische Differenzierung zwischen den Wirtsrassen, die genetische Populationsstruktur und die Migrationsgeschichte von V. album in ihrem natürlichen Verbreitungsgebiet in Europa nach You are reading a preview. Would you like to access the full-text?

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For what it is worth, this tree lends support to the autonomous status of the new subspecies and underlines its ambiguous relationship with the two other conifer parasite taxa. Viscum album subsp. creticum branches off the common tree at the same basal level as subsp. abietis but by its nrDNA ITS profile matches subsp. austriacum instead.

Discussion So far, Viscum album subsp. creticum must be regarded as a Cretan endemic. If indeed it is, it may either have evolved anew in its present location, in insular isolation; or it may be the last remnant of a formerly more widespread taxon. Supposing it is not endemic, the question then arises: Where else should we look for it?

Viscum album subsp. creticum is exceptional, if not unique, in parasitising Pinus halepensis subsp. brutia. Few other records of Viscum album growing on Aleppo pine exist, and they need to be verified as they might perhaps refer to subsp. creticum. We already mentioned one from S. Anatolia [Balls 1301 from Adana: Bürücek], and both Miller (1982) and Erun et al. (1994) cite many additional mistletoe gatherings from the same general area for which the host tree is not known. A second area which to look is eastern Spain, the only region where Viscum is known to grow on P. halepensis subsp. halepensis.


Irrespective of the question of endemism, it is tempting to speculate on the mode of survival of the Cretan mistletoe in relation to the past and present condition of its host. It is a proven fact that Pinus halepensis subsp. brutia, Crete’s single wild pine species, is a member of the old autochthonous flora: Pine pollen, plentiful in the single polliniferous core, was found to reach back to pre-settlement (pre-Neolithic) time, from a location near Ayia Galini in South Central Crete (Bottema, 1980). However, while native status is undisputed, past presence of pine woods in areas where they stock today may not been taken for granted. The extension of pine woods on the island has varied greatly through historical times. Rackham and Moody (1996) demonstrated that it has never before been as large as it is now. Their map (p. 62) shows old pine woods or stands on the southern slopes of all major mountain massifs, most of which, especially in the east, have spread considerably in recent years, conquering large new areas. Rackham (1972) gives details for the southern foothills of the Lasithi Mts., where pine, he believes, arrived around 1850 and gradually spread ever since, having been rare if at all present in the Early Bronze Age, and absent in the 16th century. Higher up in the Selakano Valley, presently the centre of extensive pine woods, Tournefort in 1700 found a woodland of Quercus ilex L., Quercus coccifera L. and Acer sempervirens L.

Size fluctuation of host stands and consequent population bottlenecks may be one factor accounting for the present rarity and patchy occurrence of Cretan mistletoe. Another factor of obvious importance is forest fires. To quote Rackham and Moody (1996), “Pine is the most

ferociously combustible Cretan plant“, and they go on with their own, plausible hypothesis:

“Cretan pine is not flammable by misfortune: these features are adaptations to promoting fire.

It is the business of this [pine]... to ignite from time to time and burn up its less fire-adapted competitors” - and why not, may we add, its parasites.

Forest fires are not a human invention, but their number and frequency have dramatically increased through the presence and action of Man. The published record is patchy, but includes the burning of 5000 acres of pinewoods in the Selakano valley on 23 June 1969 (Zaharês, 1977) and of several square kilometres of pine forest above Monastiraki in 1987, in a conflagration that Rackham & Moody (1996) compare with a small atomic bomb in terms of energy release. These two places happen to coincide with the known occurrences of the Cretan mistletoe. But anyway, all Mediterranean pine stands are bound to burn down sooner or later.

Fire is likely a major problem for mistletoes, and may be the cause for their general rarity and patchy occurrence on Mediterranean pine trees. Sometimes a fire is not strong enough to kill the trees, and in that case the parasite might survive within the host and re-sprout along


with it, but we know nothing positive of potential fire resistance of mistletoe in general or of the Cretan taxon in particular. Survival as seed in the guts of dispersing birds, and migration from one unburned patch of wood to the next, are another likely answer. Whereas no direct observations of dispersal by birds have been made in Crete, one of the notorious dispersers, the mistle thrush (Turdus viscivorus), is known to occur on the island (Peterson et al., 1983).

Birds play an essential role in mistletoe dispersal, but “the normal dispersal range of mistletoes is probably small... and distance dispersal may depend on unusual events” (Barlow, 1983).

Whether endemic or not, old relict or newly evolved, Viscum album subsp. creticum is an interesting plant full of riddles for us to solve. This paper is but a first step destined to ignite its further study.

Acknowledgements We are grateful to R. Jahn, Dresden, for providing liberal access to the Viscum material in his personal herbarium, and to G. Kuhlmann and J. Bansemer, Berlin, for their assistance in the preparation and photography of seeds and embryos.

References Ball, P.W. 1993. Viscum L. In: Tutin, T.G., Burges, N.A., Chater, A.O., Edmondson, J.R., Heywood, V.H., Moore, D.M., Valentine, D.H., Walters, S.M., Webb, D.A., Eds. Flora Europaea. Vol. 1, ed. 2. Cambridge University Press, Cambridge, p. 86.

Barclay, C. 1986. Crete. Checklist of the vascular plants. Englera 6.

Barlow, B.A. 1983. Biogeography of Loranthaceae and Viscaceae. In: Calder, M., Bernhardt, P., Eds. The biology of mistletoes. Academic Press, Sydney, pp. 19-46.

Barney, C.W., Hawksworth, F.G., Geils, B.W. 1998. Hosts of Viscum album. Eur. J. Forest Pathol. 28: 187-208.

Bergmeier, E. 1994. Bestimmungshilfen zur Flora von Deutschland. Florist. Rundbr., Beih. 4.

Bolós, O. de, Vigo, J. 1990. Flora dels països catalans. Flora of the Catalan countries. Vol. 1. Barcino, Barcelona.

Bottema, S. 1980. Palynological investigations on Crete. Rev. Palaeobot. Palynol. 31: 193-217.

Catalán, P., Aparicio, A. 1997. Viscum L. In: Castroviejo, S. (ed.), Flora iberica. Vol. 8. CSIC, Madrid, pp. 160Ehrendorfer, F. Ed. 1967. Liste der Gefäßpflanzen Mitteleuropas. Notring der wissenschaftlichen Verbände Österreichs, Wien.

Ergun, F., Deliorman, D., Sener, B. 1994. Viscum album L. (ökse otu) (Loranthaceae) bitkisinin morfolojik özellikleri ve Türkiye’deki yayılısı hakkında bazı ara tırmalar. (Studies of morphological characters of Viscum album L. (mistletoe) (Loranthaceae) and its distribution in Turkey.) Ot 1(2): 47-62.

Gäumann, E. 1946. Pflanzliche Infektionslehre. Lehrbuch der allgemeinen Pflanzenpathologie für Biologen, Landwirte, Förster und Pflanzenzüchter. Birkhäuser, Basel.


Grazi, G., Urech, K. 1982. Einige morphologische Merkmale der Mistelbeere (Viscum album L.) und deren taxonomische Bedeutung. Beitr. Biol. Pflanzen 56: 293-306.

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