1. Origin and Phylogeny of the Mistletoes
Daniel L. Nickrent, Department of Plant Biology and Center for Systematic Biology, Southern Illinois University, Carbondale, IL 62901-6509
Molecular phylogenies have utility beyond simply demonstrating evolutionary relationships. Such phylogenies provide a rigorous framework upon which other data can be interpreted, such as the evolution of morphological features, pollination systems, and biogeography. Mistletoes, a life form unique to the sandalwood order (Santalales), represents an excellent group to examine from these perspectives. Our continuing molecular phylogenetic studies of Santalales have provided increasing resolution of relationships among the component families and genera. DNA sequences from nuclear small-subunit rDNA and chloroplast rbcL and matK, analyzed separately and in combination, give congruent relationships. Mistletoes are found in Misodendraceae, Loranthaceae, Santalaceae and Viscaceae, all present (with Opiliaceae which are all root parasites) in a strongly supported clade that evolved from a paraphyletic group of Olacaceae. Strong support exists for the surprising relationship between Misodendraceae and Schoepfia and this clade is sister to a monophyletic Loranthaceae. Aerial parasites evolved independently at least two times in the grade taxon 'Santalaceae', the first involving 'Eremolepidaceae' and the second in tribe Amphorogyneae. Although only weakly supported, the latter tribe may represent the group from which the strongly monophyletic Viscaceae evolved. Molecular data are in agreement with cytology, morphology, and biogeography in showing that Loranthaceae and Viscaceae are not closely related to each other. Excluding the three root parasites of Loranthaceae, at least four or five independent evolutionary events gave rise to the 86 genera and over 1400 species of mistletoes. Although holoparasites are known from other large assemblages of parasitic plants (e.g. Orobanchaceae), reduced photosynthesis occurs rarely in Santalales (e.g. Arceuthobium, Viscaceae). It appears that photosynthesis cannot be lost entirely in mistletoes because seedlings must be autotrophic for at least some time prior to host attachment. In contrast to many animal parasites that coevolve with their hosts, parasitic plants do not appear to demonstrate the Fahrenholtz Rule, as will be demonstrated using Arceuthobium and its hosts.
2. Physiological Ecology of Mistletoes.
Gerhard Glatzel, Institute of Forest Ecology, Universität für Bodenkultur, Peter Jordan Strasse 82, A-1190 Vienna.
Thought experiments on designing mistletoes are rewarding, because major constraints are easily identified and specific for aerial parasitism on woody hosts. Floral biology and seed dispersal have been discussed along such lines, as well as morphological features in response to snow and windbreak or visually guided herbivores - the famous host leaf mimicking mistletoes of Australia. If physiological ecology is considered, there are constraints on water relations, mineral nutrition and photosynthetic carbon gain as related to growth. As far as water relations are concerned, mistletoes and host foliage may be seen as two independent control systems on a common supply line. In order to be able to compete with the host and its initially much larger leaf area, the parasite must be able to tolerate lower xylem water potential, otherwise it would be easily out competed by the host. An inevitable side effect of two independent control system on a common supply are disturbed feedback and consequently wild oscillations of xylem water potentials. Both phenomena have been repeatedly demonstrated. Mineral nutrition for mistletoes is "take what you get". Hemiparasitic mistletoes are not able to control nutrient uptake in an element specific way, as haustoria lack the control mechanisms of functional roots. "Small is beautiful" is the mistletoe's answer to the danger of outgrowing the supply and developing mineral deficiency. It has been demonstrated that specific photosynthetic carbon gain (photosynthetic water use efficiency) is lower in mistletoes when compared to their hosts. An interesting feature of mistletoes is hyper-accumulation of potassium in their tissues. It results from the fact that potassium is cycled in plants with downward flux of relatively potassium rich phloem sap and returned by acropetal xylem flux. Even though there are phloem contacts between host and mistletoes, in particular in carbon parasitic species, mistletoes do not export substantial amounts of photosynthates to their hosts. Thus a more holoparasitic life results in potassium gain both via phloem and xylem. This is probably one of the reasons why such mistletoes must have low specific transpiration rates. In all mistletoes, excess potassium can be exported via leaf turnover and fruiting. Mistletoes can afford to produce large amounts of fruits, which have been observed to be rich in potassium. Mistletoes are sometimes found on hosts which are hyper-accumulators of some nutrients. Examples are sulphur in some Capparis species or manganese in Rhododendron species on highly acidic soils. As mistletoes can't block uptake, these elements accumulate in the mistletoe tissue. Trace elements are tolerated to an amazing extent, without apparent harm to the mistletoe. This enables some mistletoe species to parasitize a range of host trees which grow on very different soils and do not co-occur at the same site. mistletoes responde to loading with osmotically relevant substances by becoming succulent, i.e. using water in expanding tissues to dilute these substances. A fine example is Amyema mackayense on Avicennia marina, a salt excreting mangrove. The mistletoe appears highly succulent as salt is sequestered in bloated, yellowing leaves. Leaf turnover is rapid and yellowing of old leaves can be taken as an indication of internal re-translocation of nutrients. To conclude, mistletoes are fine examples of the adaptability of physiological processes if constraints (the adaptive landscape) remains fairly constant. Adaptation of hosts to mistletoes is obviously a totally different story.
3. Birds and Mistletoes.
Nick Reid. University of New England, Armidale, NSW, Australia. Mark Stafford Smith and Jake Overton.
Most species of mistletoe (Loranthaceae, Viscaceae) are dispersed
by birds. Even mistletoes with explosively-dispersed seed are
reliant on bird dispersal for long-distance dissemination. Birds
may therefore be important determinants of the spatial and temporal
dynamics of mistletoe populations. Several studies of bird-dispersed
mistletoes over the past decade have enhanced our understanding
of bird-mistletoe interactions from the plant perspective. These
are reviewed with the aim of disentangling the importance of avian
dispersal and other ecological and genetic factors in regulating
mistletoe population structures at four different spatial scales
at the level of the host branch, host, host stand (within-patch),
and landscape (between-host patch). We conclude that avian dispersal
is important at all these scales in producing observed patterns
of mistletoe population structure and dynamics. However, the relative
contribution of disperser behaviour to host-mistletoe genetic
and eco-physiological compatibility, host demography and population
structure, predation, the dispersion of host and non-host populations,
and landscape patterns of resource (water and nutrient) concentration,
is unknown.
4. Ecology of Dwarf Mistletoes in Western North America.
Robert Mathiasen, School of Forestry, Northern Arizona University, Flagstaff, AZ 86011 USA
In western North America, dwarf mistletoes (Arceuthobium spp., Viscaceae) are important pathogens on members of the Pinaceae because severe infections affect biomass distribution. Furthermore, severely infested forests, dead trees contribute to fuel loads which increase the fire hazards. Because of the increased fire risk associated with dwarf mistletoe-infested forests, wildfires have probably occurred at more frequent intervals and at greater intensities within infested forests. Therefore, attempts to reintroduce fire to historic levels in western forests must take into account infestations of dwarf mistletoes and this is proving to be a challenging aspect of reintroducing prescribed fire in western North American forest ecosystems. Another important ecological consideration related to dwarf mistletoe infestations in western forests is their use by various wildlife species. Our research in northern Arizona has documented the use of witches' brooms induced by dwarf mistletoe infection by wildlife for hiding, resting, and nesting sites, including some endangered species. Therefore, forest managers are keenly interested in how to mitigate the influence of dwarf mistletoes on tree mortality, growth loss, and fire hazards, while at the same time enhancing their value as wildlife habitat in western North America.
5. Epiparasitism in mistletoes, a neglected phenomenon in forest canopy biology.
Del Wiens and Bryan Barlow. Australian National Herbarium, CSIRO Plant Industry, Canberra, ACT, Australia.
Epiparasitism is the occurrence of a parasitic species on another parasitic species to which it is related. We discuss such relationships, world-wide, among mistletoes of the families Loranthaceae and Viscaceae. These mistletoes are aerial branch-parasites, with sticky bird-dispersed seeds. Epiparasitism is divided into several categories: (1) autoparasitism, where individuals infect others of the same species; (2) incidental epiparasitism, where a species may occasionally and sporadically infect other mistletoe species, but typically occurs on terrestrial woody hosts; (3) facultative epiparasitism, where a species may commonly infect other mistletoe species, showing some co-adaptation, but still parasitize terrestrial hosts as well; and (4) obligate epiparasitism, where mistletoes are exclusively parasitic on other mistletoe species. Discussion focusses primarily on obligate epiparasitism, in relation to difficulties of detection, physiological anatomy, cell recognition phenonema, pollination and seed dispersal.
1. Is differential accumulation of elements in leaves of mistletoes and their hosts related to greater water loss in mistletoes?
Peter BannisterA, Graham L. Strong and Inge Andrew Department of Botany, University of Otago, P.O. Box 56, Dunedin, New Zealand.
It has been generally assumed that differential accumulation of elements, leading to greater accumulation of elements in mistletoe tissues, is associated with greater transpiration in the mistletoe than in the host. Only a few investigations have measured both tissue element concentrations and transpiration, or transpiration-related parameters such as carbon isotope ratios (13C ) . We investigated ten mistletoe-host pairs, nine involving the mistletoe Ileostylus micranthus and one with Tupeia antarctica over the course of a year. Annual and seasonal means of transpiration and 13C were similar in mistletoes and hosts, but hosts showed greater variation in both transpiration and 13C than mistletoes. We also obtained annual and seasonal means for foliar concentrations of Ca, Mg, K, Na,. P and N. Foliar concentrations of Ca and Mg in mistletoes were similar to those of their hosts, N concentrations were less, and foliar concentrations of K, Na and P were considerably greater in mistletoes than in their hosts. Ratios of foliar concentrations of Ca, Mg, Na and P in mistletoes to those in their hosts (M/H) were greatest when host transpiration was low, when host 13C was least negative, and when the difference between mistletoe and host 13C was most negative. M/H ratios of foliar N concentration in host and mistletoe were positively correlated with mistletoe transpiration. Passive water relations (transpiration and water potential gradients) probably influence the accumulation of all measured elements in mistletoes and their hosts (particularly Ca, Mg, P and N), but the possibility that active transport is involved in producing the high concentrations of K, Na and P in mistletoes cannot be discounted.
2. Ecophysiology of teak (Tectona grandis) and its canopy parasite Dendrophthoe falcata
Jose Kallarackal, C.K. Somen and N. Rajesh, Plant Physiology Division, Kerala Forest Research Institute, Peechi 680653, Kerala, India.
Teak (Tectona grandis), the most important timber species in India, is widely infested with the angiosperm hemiparasite Dendrophthoe falcata. This mistletoe causes enormous damage, sometimes leading to the death of the entire tree. Thus, studies were conducted to help understand the ecophysiology of the host and parasite. Diurnal water potential measurements taken from both the host and the parasite during different seasons revealed that the parasite always maintained lower water potential as compared to the host tree. The lowest water potentials recorded were -1.07 MPa in teak and -1.8 MPa in the parasite. The stomatal conductance values recorded during the pre-monsoon (dry) period were similar in both the host and the parasite. Maximum values were in the range of 500 to 600 mmol m-2s-1. A maximum net photosynthesis value of 13 mmol m-2s-1 was observed in teak whereas the parasite showed values greater than 9 mmol m-2s-1 . Diurnal measurements of light availability showed that the parasite receives only 40% of the light received by the host. In addition to well-exposed situation, the parasite was able to survive even when host leaves blocked 70% of the solar radiation. This behaviour has great implications on the ability of this parasite to adapt to contrasting light environments and must be taken into account when attempting to control the parasite on teak trees. Transpiration (measured using a sap flow sensor) was monitored simultaneously on the host and the parasite. Parasite transpiration was less than the host during mornings and evenings but greater than the host during peak hours. Chemical analyses indicate that more K and Na are present in the leaves of the parasite as compared to the host. Mortality on teak is higher than several other tropical tree-mistletoe combinations. It is suggested that attempts to control the mistletoe using herbicides should be conducted during the deciduous stage of the host tree.
3. Ecology of Arceuthobium tsugense (Viscaceae), Cascade Mts. USA.
David C. Shaw, Wind River Canopy Crane Research Facility, University of Washington, 1262 Hemlock Road, Carson, WA 98610, USA.
The ecology of Arceuthobium tsugense (Viscaceae) in the Cascade Mountains of Washington State, USA is being investigated to better understand this hemiparasite in forests where its host, Tsuga heterophylla (Pinaceae) is a secondary successional species. A. tsugense is dioecious, having a male to female sex ratio of 1:1, based on 1,608 plants examined. Plants flower in late July through August and explosive seed dispersal occurs from mid September to early October. The occurrence of aerial shoots is strongly associated with light, with a 50% probability of shoots at 2200 MJ m2y-1 and virtually no aerial shoot occurrence in the lower canopy of closed forests. Herbivory is attributed to a specialized hairstreak butterfly (Mitoura johnsoni, Lycaenidae) and is currently under investigation. Based on data collected from sap flow sensors placed in three infected and three uninfected trees at the end of the dry season (late summer), uninfected trees used 25% more water than heavily infected trees of similar size. Foliage nitrogen amounts were significantly lower at or distal to mistletoe infections as compared to amounts from foliage proximal to the infection or on uninfected trees. Investigation of spatial patterns indicates discreet infection centers in 500 year old forests. Initial investigations of mistletoe occurrence in a sequence of forest ages indicates mistletoe is persisting on trees that survive disturbance, although a large infection center encompassing several hundred hectares was discovered which may act as a refugium.
4. Effects of infection of Scurrula elata (Edgew.) Danser (Loranthaceae) on the wood properties of its host Rhododendron arboreum Sm.
Mohan P. Devkota and Gerhard Glatzel, Institute of Forest Ecology, Universität für Bodenkultur, Peter Jordan Strasse 82, A-1190 Vienna.
Effects of infection of the mistletoe, Scurrula elata (Edgew.) Danser, on wood properties of its common host, Rhododendron arboreum Sm., were studied in the Annapurna Conservation Area of the Central Nepal Himalayas. Heavy infection by mistletoes invariably causes decline of the host. Infested branches show inhibition of growth, defoliation and eventual death of branch parts distal to infection. Vessel density, vessel area, percentage lumen area and mean vessel diameter were compared in infected and uninfected host wood. The hypothesis that infection influences these anatomical parameters could not be proven. Vessel density, vessel area, percentage lumen area and mean vessel diameter of the wood of infested and uninfested branches did not show any significant differences. No significant influence of host branch diameter on the studied anatomical parameters could be detected. These results show that the infection of Rhododendron arboreum by Scurrula elata does not cause any change in basic host wood anatomy. It appears that the studied anatomical parameters of Rhododendron wood are fairly stable and are not changed by stress due to infection by mistletoes. The damage of infected host trees most likely results from a decline of total conductive area, a parameter we could not evaluate as planned, as R. arboreum does not develop usable annual tree rings in the climate of the study area.
5. Mistletoe as a keystone resource a progress report
David M. Watson, The Johnstone Centre, Charles Stuart University, Australia
In a recent review paper, I consolidated known interactions between mistletoes and animals (primarily vertebrates) throughout the world, and proposed that mistletoe functions as a keystone resource. While consistent with available information, the widely supported positive association between mistletoe and diversity is based primarily on correlational data, and the causal effect of mistletoe on diversity remains equivocal. Here, I report on an experimental approach to this issue, comparing species richness patterns in areas of artificially manipulated mistletoe densities. I sampled the avifauna of two adjacent woodland remnants, one of which has had most mistletoe plants removed (the treatment patch), but otherwise comparable in area, vegetation and grazing history. The richness of the control patch was 20% greater than the treatment patch, with 70% of woodland-dependent species more frequently recorded in the control patch. Results of this small-scale study are then used to design a large-scale replicated study currently being developed.
1. Historical biogeography of Loranthaceae inferred from chloroplast matK sequences
Jonathan F. Cabrera and Daniel L. Nickrent, Department of Plant Biology and Center for Systematic Biology, Southern Illinois University, Carbondale, IL 62901-6509
According to historical biogeographic analyses, the distributions of a number of southern hemisphere families (e.g. Nothofagaceae) can be explained by vicariance as opposed to long-distance dispersal. The mistletoe family Loranthaceae can be used to investigate such questions and in fact represents a model group for these analyses because dispersal is limited by restrictions imposed by their parasitic habit. Three endemic, relictual, root-parasitic X=12 loranth genera occur on continents that were formerly part of Gondwana: Atkinsonia, Nuytsia, and Gaiadendron. Additional chromosome numbers that existed in taxa prior to the breakup of Gondwana include X=8, 9, 10 and 11. The biogeographic histories of various loranth groups are strongly tied to the tectonic histories of their respective landmasses. For example, X=12 Indogondwanan elements such as Decaisnina arrived in Asia from India and subsequently spread to Malesia. When the Australian plate collided with the Sunda island arc in the mid Miocene, the long isolated loranth flora of Australia was supplemented by "intrusive" elements from Malesia. We have generated nearly complete sequences of the chloroplast gene matK for over 50 of the 74 genera of Loranthaceae. Using Olacaceae as outgroup, molecular phylogenetic analysis of the aligned sequences were conducted using parsimony as implemented by PAUP*. The monophyly of the family receives high bootstrap support (100%). As predicted by base chromosome number, Nuytsia and Atkinsonia (both Australian) are, respectively, sister to the remaining members of the family. Other highly-supported clades correspond well to base chromosome number and geographic distribution and include 1) the X=8 New World genera, 2) a portion of tribe Elytranthinae that are mainly Malesian (e.g. Lepidaria, Macrosolen, Amylotheca, Loxanthera), 3) Alepis and Peraxilla (X=12, New Zealand), 4) Ileostylus (X=11, New Zealand) and Muellerina (X=11, Australia), and 5) a large clade comprising X=9 Australian and African genera plus the remainder of Elytranthinae (e.g. Decaisnina, Elytranthe). Despite sharing the X=11 chromosome number with Ileostylus and Muellerina, Tupeia is not resolved as part of that clade. The strong association of the Indian and African clades is in agreement with the tectonic history of these land masses and vicariance as an explanation for their distribution. Additional tests of vicariance and dispersal will be conducted for the remaining clades.
2. Mistletoes of the Annapurna Conservation Area, Central Nepal
Mohan P. Devkota and Gerhard Glatzel, Institute of Forest Ecology, Universität für Bodenkultur, Peter Jordan Strasse 82, A-1190 Vienna.
Mistletoes in the Himalayas of Central Nepal in the southern part of the Annapurna Conservation Area were studied with regard to abundance, host specificity and distribution pattern. A total of twelve mistletoe species, eight belonging to five genera in the family Loranthaceae and four belonging to one genus in the family Viscaceae were recorded on 93 host species from 73 genera in 46 unrelated families. The following three mistletoe species were recorded for the first time in Nepal: Scurrula gracilifolia, Loranthaceae, Viscum multinerve and V. loranthi, both Viscaceae. In contrast to Loranthaceae, which are mostly generalists, mistletoes in Viscaceae were found to be highly host specific. The distribution of mistletoes in the southern Annapurna region reflects both climatic factors and habitat features for dispersers. Mistletoes are most frequent below 3000 meters altitude on ridges and sunny, exposed, warmer southeast facing slopes and are rare or absent in cooler and moister areas. Two bird species Aethopyga ignicauda (fire tailed sunbird) and Dicaeum ignipectus (fire breasted flower pecker) are the most important species for pollination and dispersal of mistletoes, respectively.