3.  DWARF MISTLETOES WHICH INFECT THE CUPRESSACEAE

According to Hawksworth & Wiens (1976), three Old World species of Arceuthobium which infect host plants of the family Cupressasae (principally Juniperus spp.) are currently recognized. These include A. azoricum Wiens & Hawksworth, A. juniperi-procerae Chiovenda and A. oxycedri (DC.) M. Bieb. These species are distinguished by several morphological characteristics and are geographically separated (Table 5). They can be separated by the following key:

1.   Basal diameter of shoots 5-9 mm; staminate flowers predominantly 4-merous: parasite on Juniperus brevifolia; Azores

1. A. azoricum

1.   Basal diameter of shoots 1-3 mm; staminate flowers predominantly 3-merous; parasites on junipers other than J. brevifolia; Africa, Europe or Asia

2

2.   Less than 5% of nodes with whorled branching; flowering and seed dispersal in March, and possibly also October; shoots greenish-yellow, little or no glaucousness; parasitic on Juniperus procera; Sub-Saharan Africa

2. A. juniperi-procera

2.   Over 30% of nodes with whorled branching; flowering and seed dispersal only in September-November; North Africa and Europe to the Himalayas

3. A. oxycedri

3.1.  ARCEUTHOBIUM AZORICUM

Arceuthobium azoricum is endemic to the Azores where it parasitizes Juniperus brevifolia, a species also endemic to these islands. This dwarf mistletoe was discovered in 1913 but until recently was considered synomymous with A. oxycedri (Hawksworth and Wiens 1976). Presently it is known from the islands of Terceira, San Jorge, Pico and Faial and is the only dwarf mistletoe occurring on oceanic islands. The only other species found away from mainland areas is A. bicarnatum, on the Caribbean Island of Hispaniola.

This mistletoe typically occupies the distal ends of the host branch, where a distinctive gall about four times the size of the uninfected host branch is formed at the point of infection. Portions of the host branch distal to the point of infection are killed and ultimately fall away. This host reaction is frequently caused by mistletoes of other genera but is unknown elsewhere in Arceuthobium (Hawksworth & Wiens 1976).

3.2.  ARCEUTHOBIUM JUNIPERI-PROCERA

Arceuthobium juniperi-procera has been known since 1911 from the northern highlands of Ethiopia and has been alternately recognized as either a distinct species or as A. oxycedri to which it is closely related (Hawksworth & Wiens 1976). It parasitizes the African pencil cedar, Juniperus procera, an economically important species in Ethiopia and Kenya (FAO 1986).

TABLE 5

COMPARISON OF THE THREE SPECIES OF ARCEUTHOBIUM ON OLD WORLD JUNIPERS

CHARACTERISTIC

A. azoricum A. juniperi-procerae A. oxycedri

Number of specimens
examined

Flowering period

Fruit maturation

Shoot height
mean, (range)

Basal shoot diameter
mean, (range)

Third internode above
base, mean length and width

Staminate flowers:
mean width

Staminate flowers:
ratio of 3- to 4- merous1
flowers

Apical portion of mature fruit

Branching type,
percentage of nodes in whorls,
mean (range)

Glaucosness of shoots
 

Shoot color

10
 

September - October

November

10 (7-14) cm
 

7 (5-9) mm
 

12 x 14 mm
 

2.5 mm
 

3.97
 
 

rounded

4 (3-5)
 
 

none
 

greenish-yellow

14
 

March and later

March and later

7 (4-14) cm
 

2 (1-3.5) mm
 

7 x 1 mm
 

1.8 mm
 

100:02
 
 

shouldered

3 (1-7)
 
 

little or none
 

greenish-yellow

20
 

September - October

October - November

6 (3-14) cm
 

2 (1-3) mm
 

7 x 1 mm
 

2.0 mm
 

95:5
 
 

rounded

45 (32-55)
 
 

conspicuous, especially
on distal portions

green

Source: Hawksworth and Wiens (1976)
1 The term "merous" refers to 3-parted and 4-parted. There are 3 or 4 sepals, petals, stamens, etc.
* Only one flowering specimen of this species was available.

This species is presently known only from several sites in Kenya and Ethiopia (Fig 15) (Hawksworth & Wiens 1996) although the host tree is widely distributed from the Arabian Peninsula southward to eastern Zaire and Zimbabwe (FAO 1986). In Kenya, this dwarf mistletoe has been implicated as one of a number of factors involved in an extensive dieback and mortality of J. procera in some, but not in all affected areas (Ciesla et al 1994).

Arceuthobium juniperi-procerae has either two flowering periods or a long flowering period with two peaks. This is in contrast to the other two juniper infesting species, which flower annually in September and October (Hawksworth and Wiens 1976).

3.3.  ARCEUTHOBIUM OXYCEDRI

3.3.1.  SYNONYMY - Arceuthobium oxycedri is the type species of the genus Arceuthobium and, as such, has a long taxonomic history (Hawksworth & Wiens 1976, 1996):

Viscum oxycedri DC., Fl. Fr. 4:274, 1805.
Razoumofskya caucasica Hoffman, Hortus Mosquensis (unpaged), 1808.
Arceuthobium oxycedri (DC.) M. Bieb., Flora Taurico-Caucasica III 629, 1819
Razoumofskya oxycedri (DC.) Schultz, ex Nym. Consp.: 320, 1853.
Viscum caucasum Steud. No. ed 1:888, 1891.
Arceuthobium juniperi Bubani, Flora Pyrenaceae: 131, 1897.
A. juniperorum Reynier, Bull. Soc Bot. Fr. 66:97, 1919
A. oxycedri (DC.) M. Bieb. var. cupressi Zefirov, Akademi Nauk SSR. Bot. Inst. 17:110, 1955.

Type locality is France, without a specific location given.

3.3.2.  HOSTS - Arceuthobium oxycedri infects a large number of Juniperus spp. across its natural range and has also been known to infect species of Chamaecyparis, Cupressus and Thuja although it is interesting to note that Cupressus sempervirens, which occurs naturally in portions of Mediterranean Europe and the Near East, has not been reported as a host. Infections on trees representing species of the genera Chamaecyparis, Cupressus and Thuja are all the result of either artificial inoculations or exotic trees having been introduced into areas within the natural range of this dwarf mistletoe. There is also a report of infection on the North American juniper, J. virginiana, in the Ukraine (Isikov & Zakharenko 1988). J. oxycedrus and J. communis are the most commonly reported host plants in Europe and J. oxycedrus is the most commonly reported host plant in North Africa (Tables 6-7). J. oxycedrus is also reported as the principle host of A. oxycedri on the Crimean Peninsula of the Ukraine (Isikov 1986, Isikov & Zak 1988).

The complex taxonomy of Juniperus spp within the natural range of A. oxycedri makes compilation of a comprehensive host list for this dwarf mistletoe difficult, especially for the Near East and Asian portions of its range. Unfortunately, the host list presented by Hawksworth & Wiens (1996) contains errors in botanical nomenclature. The following host list is based on nomenclature of Juniperus spp. given by two authorites, (Rushforth 1987 and Vidakovik 1991):

Chamaecyparis thyoides*
Cupressus arizonica*
Cupressus macrocarpa*
Juniperus communis
Juniperus drupacea
Juniperus excelsa
(Synonyms - J. macropoda?, J. polycarpus)
Juniperus foetidissima
Juniperus macrocarpa
Juniperus macropoda
(Synonym - J. seravishanica, possible synomym of J. excelsa)
Juniperus oxycedrus
(Synonym - J. rufescens)
Juniperus phoenicia
Juniperus sabina
Juniperus semiglobosa
(Synonym - J. servascanica)
Juniperus tibetica
Juniperus turkestanica
Juniperus virginiana*
Juniperus wallichiana
Thuja orientalis*

Species with an asterisk have been introduced into the natural range of A. oxycedri and summaries of the geographic distributions of various Juniperus hosts of A. oxycedri are given in the annex. Hosts infected by various countries is summarized in Tables 6-8.

3.3.3.  DISTRIBUTION -.Arceuthobium oxycedri has the widest distribution of all of the known species of dwarf mistletoes and extends over 100o of latitude or about 10,000 km from Spain and Morocco east through the Mediterranean Region, the Caucuses and the Himalayas to southwestern China (Figs 14-16, Tables 6-8). Distribution within this range is reported to be spotty, however. Elevation range is generally 1,000-2,500 m but it can be found as low as 550 m in Italy and as high as 2,700-3,100 m in Pakistan and up to 3,000-3,500 m in southwestern China (Hawksworth & Wiens 1996).

3.3.4.  DAMAGE - While there are many reports of the occurrence of A. oxycedri, there are relatively few reports of damage or impacts caused by this parasite. Those few reports which do occur indicate that this dwarf mistletoe can cause potentially serious damage to host plants throughout its range.

According to a paper by Lararev and Grigorov (1980), A. oxycedri was relatively rare on the Crimean Peninsula of the Ukraine in 1908 but now causes significant damage, especially along the Peninsula’s southern shore. In a single 0.25 ha study plot, 238 of 262 trees (90.8%) were infected and 135 (51.5%) of the trees had been killed. At elevations of 500-600 m, an infection rate of 10-20% was reported.

Rios Insua (1984) provides some insights into damage caused by A. oxycedri in natural forests of Juniperus near Madrid in central Spain and reports that the level of infection was increasing to the point that research studies were justified. He tested applications of the herbicides 2-4D and 2-4-5T applied to infected portions of trees. While there was reportedly no adverse effects of the herbicides on the host trees, no data on the efficacy of the treatments is given. Rios Insua (1987) also reports that A. oxycedri caused problems to ornamental plants in residential areas, especially Cupressus arizonica and Juniperus communis.

No mention is made of the type of witches brooms caused by A. oxycedri in either Hawksworth & Wiens 1977 or 1996. Examination of infections in Balochistan by the author indicate that they are of the non-systemic or anisophasic type.

distribution of A. oxycedri in Europe
Figure 14 - Generalized distribution of A. oxycedri in Europe

distribution of A. oxycedri and A juniperiprocera in Africa
Figure 15 - Generalized distribution of A. oxycedri and A. Juniperiprocera in Africa

distribution of A. oxycedri in Asia and the Near East
Figure 16 - Generalized distribution of A. oxycedri in Asia and the Near East

TABLE 6

DISTRIBUTION AND HOSTS OF ARCEUTHOBIUM OXYCEDRI
MEDITERRANEAN EUROPE

COUNTRY LOCATIONS HOSTS2 REFERENCES

Albania

Lake Scutari, (Lake Scutair) Bogdan, Kapinova

Juniperus spp

Hawksworth & Wiens 1996
Turrill 1926

Bosnia-Herzogovina

 

J. oxycedrus
J. phoenicea
J. sabina

Ascherson & Grabner 1913
Turrill 1926

Bulgaria

Causova Planina, Bachkovo (Backova), Karlik Dagh, Zlatograd

J. communis
J. oxycedrus

Bondev & Lyubenova 1984
Hawksworth & Wiens 1996

Croatia

Istrian Peninsula, Dalmatia (Coastal and southern Croatia)

Ch. thyoides
J. oxycedrus
J. phoenicea
J. sabina

Ascherson & Grabner 1913
Spaulding 1956
Turill 1926

France

Alpes de Haute Provence, Avignon, Bauden, Bouches du Rhone, Corsica?, Sisteron, Var, Vaucluse

J. communis
J. oxycedrus
J. phoenicia
J. sabina

Ascherson & Grabner 1913
Pignati 1982
Fiori 1923-29
Girerd 1978
Heckel 1902
Loret, 1859
Offner 1904

Greece

Macedonia, Mt. Elias (Ilias?), Thasos

J. drupacea
J. oxycedrus

Boissier 1879
Rechinger 1943

Hungary

Lika-Krabava, Valle Senjska

J. oxycedrus (Reported as J. rufescens)

Hawksworth & Wiens 1996

Italy

Marches, Tuscany

J. communis
J. oxycedrus

Brilli-Cattarina & Gubellini 1981

Macedonia

Ochoida

Juniperus spp

Hawksworth & Wiens 1996
Turrill 1926

Montenegro

 

 

Mijuskovik 1972
Turrill 1926

Russia

North Ossetia

 

Kapush & Tavasiev 1979

Serbia

 

Juniperus spp.

Josifovic 1973
Turrill 1926

Spain

Madrid, eastern Spain

C. arizonica
J. communis
J. macrocarpa
J. oxycedrus
J. phoenicia
T. orientalis

Bolos & Vigo 1990
Cadevell & Diars 1933
Rios Insua 1987

Ukraine

Crimean Peninsula

C. macrocarpa
Juniperus
spp.
Thuja orientalis

Lazarev & Grigorov 1980
Isykov & Zaharenko 1988
Isykov 1986

1 Locations in italics could not be confirmed on maps or atlases either due to size of location, name change or possible misspelling in original report.
2 C. = Cupressus, Ch.= Chamaecyparis, J. = Juniperus, T.= Thuja

TABLE 7

DISTRIBUTION AND HOSTS OF ARCEUTHOBIUM OXYCEDRI
NORTH AFRICA

COUNTRY

LOCATION(S)1

HOSTS

REFERENCES

Algeria

Oran, Viada, Batna,Gharnoubau, Dhaya, Lella-Khadidja, Temet, Auries, Atlas Mountains

J. oxycedrus
J. phoenicia
(rare)

Battandier & Trabut 1888
Maire 1961
Quezel& Santa 1962

Morocco

Middle Atlas, High Atlas

J. oxycedrus
J. phoenicia
(rare)

Emberger & Maire 1941
Maire 1961

1 Locations in italics could not be confirmed on maps or atlases either due to size of location, name change or possible misspelling in original report.

TABLE 8

DISTRIBUTION AND HOSTS OF ARCEUTHOBIUM OXYCEDRI
ASIA/NEAR EAST

COUNTRY

LOCATION(S)1

HOSTS2

REFERENCES

Azerbaijan

Greater Caususes, Steppe Plateau; Kubinsky, Ansheron and Vartashen Regions

Juniperus spp.

Fataliev 1987

China

Xizang (Xinjiang Province, Tibet)

J. tibetica
J. wallichiana
(Genus reported as Sabina.)

Kiu 1984a,b
Kiu and Ren 1982

India

Lahaul (Lahul) Upper Chenab River, Punjab, Himachal Pradesh, Kashmir: Pahalgam, Sonamarg, Srinagar, Uttar Pradesh:Gangotri

J. excelsa
(J. macropoda)

Bhattacharyya & Uniyal 1982
Brandis 1907
Duthie 1885
Hawksworh & Wiens 1996
Rau 1975

Iran

Elburzienne (Elburz Mountains), Radkane (Râdkâne)

J. sabina

Parsa 1949

Iraq

Mam, Nazarki and Sapna Valleys, Zawita Gorge, Suwara, Tuka, Sersang

J. oxycedrus

Townsend 1980

Lebanon

Emej, Laqour,Forêt d’Ehden, Forêt de Qamou’a

J. drupacea

J. oxycedrus

Mouterde 1966

Pakistan

Balochistan; Ziarat

J. excelsa3

Beg 1964
Ciesla 1993
Jamal & Beg 1974
Siddiqi 1974

Syria

Slenfe, Col de Nebi-Youmes, Col de Freiket

J. drupacea
J. oxycedrus

Mouterde 1966

Tajikistan

 

J. semiglobosa
(J. servaschanica)
J. turkestanica

Ovchinnikov 1968

Turkey

Anatolia (Sinkepass) Antalya, Bolu, Istanbul (Constantinople)

J. drupacea
J. excelsa
J. foetidissima
J. oxycedrus

Hawksworth & Wiens 1996
Miller 1982

Uzbekistan

 

J. semiglobosa
(J. servaschanica)

Botshantev 1953

1 Locations in italics could not be confirmed on maps or atlases either due to size of location, name change or possible misspelling in original report.
2 C. = Cupressus, Ch.= Chamaecyparis, J. = Juniperus, T.= Thuja. Species listed in parenthesis have a questionable status (See Annex 1).
3 The population of J. excelsa in Balochistan has also been referred to as J. ploycarpos and J. macropoda (Beg 1973, Brandis 1907, Jamal and Beg 1974)

An early report by Brandis (1907) indicates that A. oxycedri often kills Juniperus excelsa (reported as J. macropoda) at elevations of 9000-11000 ft (ca 2700-3350 m) in the Upper Chenab River Basin of northern Himachal Pradesh, India. Greater detail is provided in a later report by Bhattacharyya and Uniyal (1982) which indicates that A. oxycedri is a common

parasite of J. excelsa (reported as J. polycarpos). Heavily infected trees die after a few years. While there are indications of much damage to standing trees, infections are reportedly localized and scattered.

Fataliev (1987) reports that in Azerbaijan, A. oxycedri, causes decreased growth of affected trees, deformity and often high levels of mortality, especially in plantations. He recommends that presence of dwarf mistletoe infections should be taken into account when selecting evergreen species for forest plantings.