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19 November 2019

Arceuthobium pusillum (eastern dwarf mistletoe)

Datasheet Types: Pest, Tree, Invasive species

Abstract

This datasheet on Arceuthobium pusillum covers Identity, Overview, Distribution, Dispersal, Hosts/Species Affected, Diagnosis, Biology & Ecology, Environmental Requirements, Natural Enemies, Impacts, Uses, Prevention/Control, Further Information.

Identity

Preferred Scientific Name
Arceuthobium pusillum Peck (1872)
Preferred Common Name
eastern dwarf mistletoe
Other Scientific Names
Arceuthobium abigenium Wood (1881)
Arceuthobium minutum Engelmann (1871)
Razoumofskya minuta (Engelm.) Kuntze (1891)
Razoumofskya pusilla (Peck) Kuntze (1891)
EPPO code
AREPU (Arceuthobium pusillum)

Pictures

Female shoots of A. pusillum on Picea glauca, in Maine, USA.
Female shoot
Female shoots of A. pusillum on Picea glauca, in Maine, USA.
©Daniel L. Nickrent
Male flowers of A. pusillum on Picea glauca, in Maine, USA.
Male flowers
Male flowers of A. pusillum on Picea glauca, in Maine, USA.
©Ken Robertson
Witches brooms (arrowed) in Picea glauca, caused by A. pusillum, in Maine, USA.
Damage symptom
Witches brooms (arrowed) in Picea glauca, caused by A. pusillum, in Maine, USA.
©Daniel L. Nickrent

Summary of Invasiveness

A. pusillum does not spread rapidly and cannot be considered highly invasive. It does, however, constitute a serious threat as a result of its ability to build up gradually over the life of a forest and cause severe damaging effects on a number of important forest species. Its 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 the known hosts, planted as exotics in other countries, but there is also a possibility of spread to related species that are not known to be hosts.

Taxonomic Tree

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Notes on Taxonomy and Nomenclature

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).

Plant Type

Parasitic
Perennial
Seed propagated

Description

Arceuthobium spp. are obligate parasites 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, forming a systemic infection of whole branch systems. A. pusillum has some of the smallest shoots of any Arceuthobium species, only about 1 cm high with a maximum of 3 cm height, virtually unbranched. They appear 2-4 years after the original infection and are pale yellow-green, or male shoots may be reddish. Basal diameter of the shoots is about 1 mm. Third internode 1-4 mm long, about 1 mm thick, length to width ratio 1.9:1. Plants are dioecious. Staminate flowers about 2 mm across, perianth mostly 3-merous (occasionally 2- or 4-merous), segments ca. 0.8 mm long, 0.7 mm wide. Anther diameter 0.4 mm centred 0.5 mm from the tip of the perianth segment. Pollen polar diameter about 22 µm, equatorial diameter 26 µm, spine height 2.2 µm. Mature fruit, green, ca. 3.0 mm long by 1.5 mm wide, proximal portion ca. 2 mm long. Seeds 2.0 by 0.9 mm.

Distribution

A. pusillum is restricted to the eastern side of the USA and Canada and has not apparently spread to any other region.

Distribution Map

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Distribution Table

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History of Introduction and Spread

A. pusillum is not known to have spread outside eastern North America.

Risk of Introduction

The risk of accidental introduction is already well recognized and trade in un-debarked timber is correspondingly controlled in many countries. Arceuthobium species are also specifically listed as prohibited imports in all countries of the European Union, Australia, New Zealand, Turkey, Tanzania, and no doubt many others.

Means of Movement and Dispersal

Natural Dispersal (Non-Biotic)Natural dispersal of Arceuthobium spp. is by the explosive fruits which, in the case of A. americanum, can expel the seeds at speeds of 2.6 m/second up to a 15 m distance (Hinds and Hawksworth, 1965). In spite of this, the natural spread of A. pusillum may not exceed about 1.5 m/annum (Baker and French, 1991).Vector Transmission (Biotic)Long-distance dispersal can occur as a result of seeds sticking to birds or mammals. The grey jay (Perisorius canadensis) is reported to be the most important long-distance vector in Newfoundland, Canada, while squirrels (Glaucomys sabrinus and Tamiasciurus hudsonicus) are known carriers in Minnesota, USA (Hawksworth and Wiens, 1996).Silvicultural PracticesLogging and movement of timber which has not been completely de-barked, can result in movement of complete plants of Arceuthobium and possible transfer of seeds and establishment of new infestations.Accidental IntroductionAccidental 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 be prevented relatively easily. 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 IntroductionIntentional introduction would seem extremely unlikely, other than for research.

Plant Trade

Plant parts liable to carry the pest in trade/transportPest stagesBorne internallyBorne externallyVisibility of pest or symptoms
Bark
weeds/whole plants
   
Stems (above ground)/Shoots/Trunks/Branches
weeds/whole plants
   
Plant parts not known to carry the pest in trade/transport
Flowers/Inflorescences/Cones/Calyx
Fruits (inc. pods)
Growing medium accompanying plants
Leaves
Roots
Seedlings/Micropropagated plants
True seeds (inc. grain)

Host Plants and Other Plants Affected

Similarities to Other Species/Conditions

Arceuthobium species are all superficially similar in their morphology and may be difficult to separate. A. pusillum is distinguished from all other N. American species by its occurrence on Picea species, and by its small size, the only other N. American species on Picea being A. microcarpum with shoots usually more than 5 cm high. Confusion is theoretically possible with the Old World species A. sichuanense, which also occurs on Picea spp., but this has larger shoots, at least 2 cm, and verticillate branching.

Habitat

A. pusillum is associated with moist habitats, e.g. in areas of bog, and neighbouring rivers and lakes, and is thought to require uninterrupted high atmospheric humidity in the spring for normal growth (Hawksworth and Wiens, 1996).

Habitat List

CategorySub categoryHabitatPresenceStatus
TerrestrialTerrestrial – ManagedManaged forests, plantations and orchardsPresent, no further detailsHarmful (pest or invasive)
TerrestrialTerrestrial ‑ Natural / Semi-naturalNatural forestsPresent, no further detailsHarmful (pest or invasive)

Biology and Ecology

GeneticsChromosome number 2n = 28. Physiology and PhenologyArceuthobium spp. are obligate parasites, depending on an endophytic system within the host branch to draw water and nutrients from their hosts. Germination of A. pusillum occurs in early summer following autumn dispersal and is favoured by light, but the seedling shows negative phototropism, causing it to bore directly into the host shoot, even from below. The seedlings of most Arceuthobium spp. can only penetrate young branches less than 5 years old, developing a 'penetration wedge' after germination, which enters the cortex and then ramifies throughout the bark, developing sinkers into the xylem. These sinkers, however, do not necessarily contain xylem elements. Furthermore, there is no evidence for any direct symplastic connection with the host tissues, and 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 2-5 years (usually 3-4) of its life A. pusillum 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'.After emergence from the endophyte, the shoots of A. pusillum produce flowers and fruits within a further 2 years and then die. A. pusillum is unusual in that the shoots are not perennial and do not normally flower a second time. Reproductive BiologyArceuthobium spp. are dioecious. In A. pusillum, female plants may predominate in a ratio of 3:2 but this is not consistent. Pollination in A. pusillum appears to be predominantly due to insects but may also occur by wind (Hawksworth and Wiens, 1996). Anthesis occurs between April and June. Following fertilization of the ovule, the fruit matures in September or October of the same year, more rapidly than almost any other Arceuthobium species. 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. The embryo is green, a few mm 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, sometimes beyond 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 (see section on 'Movement and Dispersal'). However, any seeds that are ingested by animals are destroyed. Seeds of Arceuthobium spp. do not 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. Germination of A. pusillum seeds may be quite low - a figure of 7% is quoted by Hawksworth and Wiens (1996).AssociationsThe grey jay (Perisorius canadensis) uses the witches' brooms of A. pusillum as a preferred nesting site (Hawksworth and Wiens, 1996).

Latitude/Altitude Ranges

Latitude North (°N)Latitude South (°S)Altitude lower (m)Altitude upper (m)
0000

Air Temperature

ParameterLower limit (°C)Upper limit (°C)
Mean annual temperature111
Mean maximum temperature of hottest month1828
Mean minimum temperature of coldest month-26-5

Rainfall

ParameterLower limitUpper limitDescription
Dry season duration08number of consecutive months with <40 mm rainfall
Mean annual rainfall3801150mm; lower/upper limits

Rainfall Regime

Summer
Uniform

Notes on Natural Enemies

The fungi recorded in the table of natural enemies are not known to cause serious damage to A. pusillum.

Natural enemies

Natural enemyTypeLife stagesSpecificityReferencesBiological control inBiological control on
Caliciopsis arceuthobiiPathogen
Fruits/pods
    
Septogloeum gilliiPathogen
Stems
Leaves
    

Impact Summary

CategoryImpact
Animal/plant collectionsNone
Animal/plant productsNone
Biodiversity (generally)Positive
Crop productionNone
Environment (generally)None
Fisheries / aquacultureNone
Forestry productionNegative
Human healthNone
Livestock productionNone
Native faunaPositive
Native floraNone
Rare/protected speciesNone
TourismNone
Trade/international relationsNegative
Transport/travelNone

Impact

Arceuthobium species as a whole are regarded as some of the most serious of all pests/diseases of N. American forests. Dwarf mistletoes are very much more damaging to their hosts than the 'green' mistletoes in both Loranthaceae and Viscaceae. Having little photosynthetic capacity, they draw more heavily on host carbohydrate, and furthermore interfere with photosynthate translocation to the roots. The mistletoe has a girdling effect, resulting in an accumulation of photosynthate above the site of infection. Apparently, carbohydrates are withheld from the roots in quantities sufficient to cause the characteristic decline of the tree (Rediske and Shea, 1961; Hawksworth and Wiens, 1996). There are also severe growth-regulatory effects resulting from cytokinin production at the point of infection and the redirection of host photosynthate into the resulting witches' broom growths. These distort and suppress growth of branches and even the main trunk. Wood quality is further affected as a result of swellings, witches' brooms and knots, and structural weakening associated with shortened, distorted tracheids.In spite of its small size, A. pusillum is a very damaging parasite. Mortality is severe in Picea mariana along the coast of Maine, USA, and it is considered the most serious disease agent of P. mariana in the Great Lakes region of the USA (Geils et al., 2002). In Manitoba, Canada, infection of Picea glauca by A. pusillum ranged from 25 to 100%. The presence of mistletoe reduced the annual radial increment from 0.67 cm to 0.04-0.14 cm over a period of 5 years. Seedlings suffered 20% mortality over a 2-year period and 25% of the survivors were infected. The annual height growth of infected seedlings was reduced by 40% (French et al., 1981). In New Hampshire, USA, P. pusillum causes growth reduction and mortality of Picea rubens. It also reduces timber quality by causing marked trunk swellings (Hawksworth and Shigo, 1980).

Impact: Environmental

No serious impact reported.

Impact: Biodiversity

The opening of the canopy, and the creation of witches' brooms, may result in some increase in biodiversity, as a number of bird species have been noted to favour the witches' brooms as nesting sites.

Impact: Social

No serious impact reported.

Risk and Impact Factors

Invasiveness

Invasive in its native range
Highly mobile locally
Has high reproductive potential

Impact outcomes

Negatively impacts agriculture

Impact mechanisms

Competition - monopolizing resources

Likelihood of entry/control

Difficult/costly to control

Uses

No uses of this species are known.

Prevention and Control

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.

Cultural Control

In the absence of any simple direct means of control of dwarf mistletoes, and the vast areas of forest involved, cultural management is virtually the only approach for dealing with this species. The techniques vary according to the type of stand in which the problem occurs. Silvicultural treatments considered by Muir and Geils (2002) for cultural control of Arceuthobium species in general include:- Harvest, retention, and regeneration by clear-felling (even-aged silviculture), or selective harvesting to establish and maintain uneven or all-aged stand stuctures- Design and layout of harvest and treatment blocks- Site preparation and vegetation management by brushing, prescribed burning, and other methods- Planting or retaining residual and advanced regeneration- Thinning and sanitation- Pruning brooms and infected branchesSilvicultural guides with specific recommendations for control of A. pusillum in Picea mariana include Johnson (1977) and Ostry and Nicholls (1979).Detailed surveys are an essential ingredient of successful control programmes and the 6-class rating system (Hawksworth, 1977) is widely accepted as a standard. This involves a 0-6 score based on 0, 1 or 2 for each third (lower, middle, upper) of the tree; 0 for no infection, 1 for light infection (less than half branches affected) or 2 for heavy infection (more than half infected). The general aim of management is to reduce the risk of further spread of the mistletoe by removing sources of infection and/or creating barriers to its movement. In recently harvested, regenerating stands, the emphasis may be on the complete removal of any infected trees over 2 m, regardless of commercial value, both within the stand, and along borders to a distance of 18 m, before the regeneration is 1 m high.In pre-commercial stands in which surveys show less than 40% infected trees, it should be economic to do selective thinning to remove all those infected. Above 40% this is unlikely to be economic. Severely infested stands may best be harvested early and regenerated, but decisions may require use of available models to help devise the most economic option. Some of the available models are described by Muir and Geils (2002).In many cases the presence of dwarf mistletoe may pose no serious threat to productivity. Where wildlife objectives take precedence, retention of some dwarf mistletoe may even be desired. It may contribute in various ways to biodiversity - by creating openings in the forest following tree death, by providing nesting sites in the 'brooms' and by providing food for a range of vertebrates and invertebrates.

Mechanical Control

Pruning may be appropriate as a means of reducing damage to individual trees, but more generally to reduce the source of infection for surrounding trees. The practicality, however, is that it will only be feasible in particular amenity and recreation areas.Clear-felling (with or without fire) is appropriate where a stand is so severely infested that it needs to be abandoned and regenerated or re-planted.

Chemical Control

The only chemical approved for use against dwarf mistletoes is the ethylene-releasing growth regulator, ethephon, which can cause abscission of the shoots of A. pusillum 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, while applications from the air fail to penetrate the canopy adequately. The treatment is therefore of interest mainly for high value amenity trees.

Biological Control

The use of the fungus Caliciopsis arceuthobii for biological control of A. pusillum has been considered, but potential is apparently limited by extreme variation in infection rates from one season to another.

References

Baker FA, French DW, 1991. Radial enlargement of mortality centers caused by Arceuthobium pusillum Peck in black spruce stands. Forest Science, 37(1):364-367
EPPO, 2014. PQR database. Paris, France: European and Mediterranean Plant Protection Organization. http://www.eppo.int/DATABASES/pqr/pqr.htm
French DW, Baker FA, Laut J, 1981. Dwarf mistletoe on white spruce in Sprucewoods Provincial Park, Manitoba. Canadian Journal of Forest Research, 11(1):187-189
Geils BW, Tovar JC, Moody B, (technical coordinators), 2002. Mistletoes of North American Conifers. General Technical Report RMRS-GTR-98. Ogden, USA: United States Department of Agriculture Forest Service.
Hawksworth FG, 1977. The 6-class dwarf mistletoe rating system. USDA Forest Service General Technical Report, Rocky Mountain Forest and Range Experiment Station, No. RM-48:7 pp.
Hawksworth FG, Shigo AL, 1980. Dwarf mistletoe on red spruce in the White Mountains of New Hampshire. Plant Disease, 64(9):880-882
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.
Johnson WF, 1977. Manager's handbook for black spruce in the North-Central States. General Technical Report NC-34. St Paul MN: US Department of Agriculture, Forest Service, North Central Forest Experiment Station.
Muir JA, Geils BW, 2002. Management strategies for dwarf mistletoe: silviculture. General Technical Report - Rocky Mountain Research Station, USDA Forest Service, No. RMRS-GTR-98:83-94.
Ostry ME, Nicholls TH, 1979. Eastern dwarf mistletoe on black spruce. Forest Insect and Disease Leaflet 158. Washington DC: US Department of Agriculture, Forest Service.
Rediske JH, Shea KR, 1961. The production and translocation of photosynthate in dwarf mistletoe and Lodgepole Pine. American Journal of Botany, 48:447-452.

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Published online: 19 November 2019

Language

English

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CABI
CABI Head Office, Wallingford, UK

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