Arceuthobium spp. do not spread rapidly and cannot be considered highly invasive. They do, however, constitute a serious threat as a result of their ability to build up gradually over the life of a forest and cause severe damaging effects on a number...
Arceuthobium spp. do not spread rapidly and cannot be considered highly invasive. They do, however, constitute a serious threat as a result of their ability to build up gradually over the life of a forest and cause severe damaging effects on a number of important forest species.
Their potential to establish in other areas is limited by the need for the living parasite to survive on the pathway and reproduce after entry. Nevertheless, the risk of economic impact is considerable if host species are available. The conifers at greatest risk would be species, known to be hosts, planted as exotics in other continents, but there is also a certain possibility of spread to related species, not known to be hosts.
A detailed discussion of the taxonomy and taxonomic history of the genus Arceuthobium is provided by Hawksworth and Wiens (1996). The genus Arceuthobium is a member of the plant family Viscaceae and is a clearly defined group of small (generally less than 20 cm high), variously coloured flowering plants that are aerial parasites on conifers of the families Pinaceae and Cupressaceae. They are considered to be the most evolutionary specialized genus of the family Viscaceae. Arceuthobium has been previously included in the subfamily Viscoideae of the family Loranthaceae, however, the subfamilies Loranthoideae and Viscoideae are now generally considered to have family status (Loranthaceae and Viscaceae).
A. oxycedri is a member of subgenus Arceuthobium, section Arceuthobium. The species was originally considered to include dwarf mistletoes occurring on Juniperus brevifolia in the Azores (Portugal) and on J. procera in Ethiopia and Kenya, but these are now considered to be the separate species A. azoricum Hawksworth and Wiens and A. juniperi-procerae Chiovenda, respectively Hawksworth and Wiens, 1976). A. oxycedri is the only Arceuthobium species to occur on members of the Cupressaceae.
Like other Arceuthobium spp., A. oxycedri is an obligate parasite with an endophytic 'root' system ramifying within the host branch. This endophyte expands within the cortex and becomes embedded in the xylem for some years before aerial shoots are produced, encircling the infected branch and growing along it. A. oxycedri shoots are 5 to 10 cm high, but can grow up to 20 cm high, with verticillate branching. Staminate (male) flowers 1.5 - 2.0 mm across, perianth mostly 3-merous (ca. 95%), occasionally 4-merous (ca. 5%), rarely 2-merous (Hawksworth and Wiens, 1996). The mature fruit is about 3.0 mm long and 1.5 - 2.0 mm wide.
A. oxycedri is a characteristic plant of the Black Sea coast, where it was first described. The locality of an old record in Italy is now in Slovenia. In Pakistan, A. oxycedri is restricted to one forest in northern Balochistan, on J. excelsa (Ciesla et al., 1998).
The distribution in this summary table is based on all the information available. When several references are cited, they may give conflicting information on the status. Further details may be available for individual references in the Distribution Table Details section which can be selected by going to Generate Report.
The risk presented by Arceuthobium spp. introductions into other areas of the world is related to the availability of their hosts. The most obvious risk arises from the fact that several North American hosts ( for example,Pinus contorta, P. ponderosa, Tsuga spp. and Pseudotsuga menziesii) have been more or less widely planted in other continents, in the absence of these mistletoes (curiously, Pinus radiata, one of the North American pines most widely planted around the world, is hardly reported as an Arceuthobium host, nor is Picea sitchensis, much planted in parts of Europe). Conversely, the European or Asian hosts of Arceuthobium have not been substantially planted outside their natural range. A secondary risk is that, although in their natural range Arceuthobium spp. occur rather rarely on species other than their main hosts, there is limited data suggesting that they may readily infect some exotic species. There is accordingly a certain risk that Arceuthobium spp. may spread to and affect such exotic hosts if they are introduced into other continents, e.g. P. sylvestris in Europe, Juniperus virginiana in North America.
The risk of accidental introduction is already well recognized and trade in conifer plants is correspondingly controlled in many countries. Exotic Arceuthobium species are also specifically listed as prohibited imports in the European Union, other European countries, Australia, New Zealand, Turkey, Tanzania and no doubt many others. North American countries similarly restrict import of conifers.
A. oxycedri is limited to habitats where its main host Juniperus oxycedrus occurs, i.e. rocky slopes in Mediterranean and Central Asian countries. Its range does not extend to that of the other Juniperus spp. It is a rather uncommon and local species, though with a very extensive overall range.
Several other Juniperus spp., of more restricted distribution in the Mediterranean area or Central Asia, have been recorded as hosts. Isikov and Zakharenko (1988) found A. oxycedri on 18 species of Cupressaceae in Krym, Ukraine, including cultivated exotics (Juniperus virginiana, Cupressus macrocarpa, C. lusitanica, C. arizonica, C. macnabiana, C. funebris, Platycladus orientalis). C. arizonica is also noted as a host in Spain (Rios-Inusa, 1987). A. oxycedri does not occur on the native Cupressus sempervirens, nor apparently has it been reported on these other Cupressaceae elsewhere, despite the fact that several are widely planted as ornamentals.
Like other Arceuthobium spp., A. oxycedri is an obligate parasite, depending on an endophytic system within the host branch to draw water and nutrients from their hosts. The seedling shows negative phototropism, causing it to bore directly into the host shoot, even from below. Seedlings of most Arceuthobium spp. can only penetrate young branches less than 5 years old. Most Arceuthobium spp. have no phloem tissue. Transfer of nutrients, including sugars, may depend on close association of host and parasite parenchyma cells, and apoplastic movement via the walls of these cells. Graniferous tracheary elements could also be involved (see Hawksworth and Wiens (1996), for detailed discussion on this topic).
Photosynthesis is apparently important in supporting the seedling as it germinates and attaches, but for the next 2-7 years (usually 3-4) of its life, the parasite persists only as the endophyte inside the host tissue without any aerial shoot. Even after emergence of the aerial shoots, the established parasite has a relatively low photosynthetic capacity, usually much less than 50% of 'normal'.
Once emerged, the parasite shoots produce fruits annually, for at least 2 years, and often for 5 years or more (Hawksworth and Wiens, 1996).
Reproductive Biology
Arceuthobium spp. are dioecious. Pollination appears to be predominantly due to insects (especially ants and flies) but may also occur by wind (Hawksworth and Wiens, 1996). In A. oxycedri, anthesis occurs mostly in September- October (August - September in China). Following fertilization of the 'ovule', the fruit matures 13 months later in October - November of the following year. No true seed is formed, as there is no testa, but the embryo is embedded in chlorophyllous endosperm, surrounded by viscin. This will be referred to as a seed for convenience. In Arceuthobium spp., the embryo is green, a few millimetres long, and has a meristematic radicular apex without a root cap. Dispersal of the seed is exceptional, involving a hydrostatic, explosive process which expels the seed at least 10 m. Most dispersal occurs as temperatures rise and humidity declines in the morning. The viscin ensures that it is retained by any host shoot that is hit, but if this is a needle, it may slide down with gravity to the base of the needle and germinate there. Although this is the main means of dispersal over a short range, long-distance dispersal also occurs as a result of seeds sticking to birds or mammals. However, any seeds that are ingested by animals are destroyed. Seeds of Arceuthobium spp. do not generally show dormancy and germination normally occurs in the first season after dispersal, though seeds may retain dormancy for 1-4 years when stored in ideal conditions.
Environmental requirements
The main environmental constraint on an Arceuthobium sp. is the presence of its host, which is in turn determined by multiple environmental requirements. A. oxycedri differs from the North American species in having Juniperus as host plants, and in its wide geographical distribution, mainly at relatively low altitude, and in a relatively mild Mediterranean climate.
Various insects and fungi have been recorded attacking Arceuthobium spp., but none is noted in Europe to have a particular importance on A. oxycedri. In Pakistan (Arif and Muhammad-Irshad, 1986), two lepidoptera, two coleoptera, two diptera and a mite were found feeding of A. oxycedri. Dioryctria taiella was considered to have the greatest potential for biological control.
In Arceuthobium spp., natural dispersal is by the explosive fruits, which can expel the seeds for some distance from the parent plant (Hinds and Hawksworth, 1965). In spite of this, the natural spread may not exceed about 1.5m/annum (Hawksworth, 1958).
Vector Transmission (Biotic)
Seeds of Arceuthobium spp.falling onto the plumage of birds, or the fur of animals, tend to stick and may be dispersed for long distances. In North America, about 7% of birds and mammals trapped, carried seeds, or as high as 22% during the 2-week period of maximum seed release (Hawksworth and Johnson, 1989). The importance of this method of transmission in A. oxycedri is not known.
Agricultural Practices
Logging and movement of wood which has not been completely de-barked, can result in movement of complete plants of Arceuthobium, or transfer of seeds and establishment of new infestations.
Accidental Introduction
Accidental introduction of Arceuthobium spp. into new areas or continents does not appear very likely. Seeds are short-lived, and unlikely to reach a host tree under circumstances in which they could develop. Conifer plants could carry living mistletoe plants, especially in the prolonged endophytic stage before the external plant develops, but young plants, as normally traded, are not very likely to be infected. Mistletoes could be carried on cut branches, including Christmas trees and possibly on logs with bark (though mistletoes normally occur on the branches of trees, not on trunks). But it seems unlikely that mistletoes borne on cut, dead plants present any risk of transmission. Accordingly, introduction can relatively easily be prevented. The prohibition of import of plants for planting of the main host genera (as established, for example, in the phytosanitary regulations of the European Union) blocks the only really dangerous pathway.
Intentional Introduction
Intentional introduction seems extremely unlikely, other than for research.
Though A. oxycedri damages its Juniperus hosts, this is of no real economic significance, since they are not forest trees grown for wood, nor important amenity trees. Juniperus spp. are significant components of Mediterranean vegetation, but their status in this respect is not impaired by Arceuthobium infection. A. oxycedri has the potential for economic impact however, as in North America Cupressaceae, (e.g. Juniperus virginiana), are of major economic importance.
A. oxycedri never occurs on conifers other than Cupressaceae, and is allopatric to its sister species on the same family, so there are no possibilities of confusion.
Due to the variable regulations around (de)registration of pesticides, your national list of registered pesticides or relevant authority should be consulted to determine which products are legally allowed for use in your country when considering chemical control. Pesticides should always be used in a lawful manner, consistent with the product's label.
In its natural range, A. oxycedri is not an invasive pest, nor are its hosts of importance for forestry, and it is therefore not subject to any particular control measures. On the contrary, as the sole European representative of its genus, it has value for biological diversity in Europe. If, however, it was introduced into other continents and attacked Juniperus spp., or other Cupressaceae, valuable for forestry, the measures applied for North American species would no doubt be appropriate.
Herbicides have been investigated in Spain for the control of A. oxycedri, and 2,4-D and MCPA was found to be most effective (Rios-Unsua, 1994). The only chemical approved for use against dwarf mistletoes is the ethylene-releasing growth regulator, ethephon, which can cause abscission of the shoots and delay fresh seeding for 2-4 years, but there is eventual re-growth from the endophyte. It is difficult to achieve good coverage in larger trees from the ground, whereas applications from the air fail to penetrate the canopy adequately. It is not known whether this treatment has been tested on A.oxycedri.
Hawksworth FG; Wiens D, 1996. Dwarf Mistletoes: Biology, Pathology, and Systematics. Agriculture Handbook 709. Washington DC, USA: United States Department of Agriculture Forest Service.
Hinds TE; Hawksworth FG, 1965. Seed dispersal velocity in four dwarf mistletoes. Science, 148:517-519.
Hawksworth FG, Wiens D, 1996. Dwarf Mistletoes: Biology, Pathology, and Systematics. In: Agriculture Handbook 709, Washington DC, USA: United States Department of Agriculture Forest Service.
Martincic A, 1999. Mala Flora Slovenije., Ljubljana, Tehniska Zalozba Slovenije.
