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CHAPTER 6
Host Relationships
Natural Hosts The hosts of dwarf mistletoes are ranked as "prin
cipal," "secondary," "occasional," and "rare." Potential hosts that are not parasitized are designed as "immune". These susceptibility classifications are defined in table 6.1, and were devised by Hawksworth and Wiens (1972). They were based on an "infection index" defined by percentage classes of infected trees (for each host species) within 6 m of a heavily parasitized host. Infection indices are meaningful only in stands with trees older than 30 years.
The susceptibility classification (table 6.1) is not a measure of the frequency with which a host species may be infested over its geographical distribution. For example, Pinus cembroides is designated as a principal host of Arceuthobium divaricatum, even though the two species occur together only in the Davis Mountains of west Texas. In this region, however, P. cembroides is as susceptible as the other pinyons that act as principal hosts in other portions of this dwarf mistletoe's distribution.
Some variation in susceptibility is to be expected over the geographical distribution of a host species, as well as in certain habitats (see chapter 7). Such differences could reflect variation in the host, parasite, or environment (Wiens 1961). Nonetheless, the host relationships of each dwarf mistletoe species are sufficiently consistent to make the rankings meaningful.
The principal hosts of both New World and Old World dwarf mistletoes tend to be restricted to a single genus or for Pinus to a single subgenus (figs. 6.1 and 6.2). Only Arceuthobium microcarpum, A. laricis, and A. tsugense have principal hosts that belong to different genera (respectively, Picea and Pinus; Larix and Tsuga; and Abies, Pinus, and Tsuga).
The susceptibility of natural hosts is listed by Arceuthobium taxa in table 6.2 and by host taxa in table 6.3. Host susceptibility classification is usually based on direct field observations; for those cases where data are lacking, we classified taxa on the basis of our field experience. The absence of field studies precludes the preparation of a susceptibility classification for the Old World species.
The susceptibility classes were based on the most common situation encountered for a particular host-parasite combination. For example, in the San Bernardino Mountains near Snow Valley, California, Arceuthobium campylopodum severely parasitizes Pinus coulteri; at lower elevations, however, the mistletoe severely parasitizes P. attenuata and only occasionally infects P. coulteri. Therefore, even though P. coulteri is sometimes heavily infested by A. campylopodum, it is a secondary host in most situations and is classified as such. Fortunately, this kind of variation is rare, and most host taxa readily fall into a single susceptibility class for an associated dwarf mistletoe taxa.
TABLE 6.1 - Classes of host susceptibility to Arceuthobium
Class Susceptibility Infection level
I Principal* ;;::90%
II Secondary 90-50%
III Occasional 50-5%
IV Rare ~5%
V Immunet 0%
*Except for young trees, infection levels usually approach 100% within 6 m of a seed source. tTrees are not infected even where the dwarf mistletoe is common. .
HostRelationships ----------------------------------- 43
This file was created by scanning the printed publication.Errors identified by the software have been corrected;
however, some errors may remain.
Chapter 6
~ e:- :::l
e:- II Q Q .g CI)
~ ~f ~f & .~ .~ :::l
tt .s! ~~ Q) :::l
ARCEUTHOBIUM .Q cu ~ ~ ..:c ...,J Il..~
A abietinum f. sp. concoloris • A abietinum f. sp. magnificae • A abietis-religiosae • A americanum • A apachecum • A aureum subsp. aureum • A aureum subsp. petersonii • A bicarinatum • A blumeri • A californicum • A campylopodum • A cyanocarpum • A divaricatum • A douglasii • A durangense • A gillii • A globosum subsp. globsum • A globosum subsp. grandicaule • A guatemalense • A hawksworthii • A hondurense • A laricis • Alittorum • A microcarpum • • A monticola • A nigrum • A oaxacanum • A occidentale • A pendens • A pusillum • A rubrum • A siskiyouense • A strictum • A tsugense subsp. tsugense • • • A. tsugense subsp. mertensiana • • A tsugense subsp. vagina tum • A. tsugense subsp. cryptopodum • A. verticilliflorum • A. yecorense •
Figure 6.1-Taxonomic affiliations of principal hosts of New World Arceuthobium.
~ ~ ~ CI)
0 ffi :::> ~
0 ffi A RCEUTHOBiUM ~ IJ.j
Cl)ij CI)>< f2 US iti Q.. :::>cr :::>0 j.....: ~ ~~ <=~ Cil t.> IJ.J 0..: ....... a:e. ~ a: ~ ""':I
A. azoricum • A. chinense • A. juniperi-procerae • A. minutissimum • A. oxycedri • A. pini • A. sichuanense • A. tibetense • Figure 6.2 -Taxonomic affiliations of principal hosts of Old World Arceuthobium.
44 Host Relationships
Chapter 6
As shown in table 6.3, some host taxa are parasitized by a number of dwarf mistletoes: 9 taxa infect Pinus durangensis; 7 parasitize P. cooperi, P contorta var. latifolia, P. engelmannii, and P. monticola,' and 6 infect P. arizonica var. arizonica, P. teocote, and P. pseudostrobus.
Some dwarf mistletoes are highly host specificArceuthobium apachecum is restricted to Pinus strobijormis, A. bicarinatum to P. occidentalis, and A. guatemalense to P. ayacahuite. Other dwarf mistletoes, however, have broader host ranges-A. laricis, which principally parasitizes Larix occidentalis, also occurs on Abies, Picea, Pinus, and Tsuga. Arceuthobium douglasii primarily parasitizes Pseudotsuga menziesii although it infects Abies and Picea rarely.
A number of species of Arceuthobium infect nearly all western true firs (Abies) to some extent. However, Abies is the principal host of only 3 dwarf mistletoe species-A. abietinum in the western United States and northern Mexico, A. abietis-religiosae in central Mexico, and A. tsugense in the coastal north Pacific region. There is a single collection by Weir (ILL) of an Arceuthobium on the rare bristlecone fir, Abies bracteata, of the Santa Lucia Mountains, California. The mistletoe species is most likely A. occidentale, which typically parasitizes Pinus sabiniana, but the specimen is poorly documented and so fragmented that positive identification is impossible.
All North American spruces-except the Mexican species Picea chihuahuana and P. mexicana (Martinez 1963) and the recently described P. martinezii-are hosts for Arceuthobium. Two dwarf mistletoe species are principal parasites of spruce: (1) A. pusillum on Picea mariana, P. glauca, and P. rubens in the Great Lakes region, New England, and eastern Canada; and (2) A. microcarpum on Picea
j engelmannii and P. pungens in Arizona and New Mexico. Picea sitchensis is rarely parasitized by A. tsugense subsp. tsugense (Laurent 1966, :Mathiasen 1994).
Eight dwarf mistletoe species occur primarily on the North American white pines (subgenus Haploxylon) -Arceuthobium apachecum on Pinus strobiformis,' A. blumeri on P. ayacahuite var. brachyptera and P. strobiformis; A. californicum on P. lambertiana; A. cyanocarpum on P. albicaulis, P. aristata, P. jlexilis, and P. longaeva,' A. divaricatum on numerous pinyons; A. guatemalense on P. ayacahuite var. ayacahuite,' A. monticola on P. monticola; and A. pendens on several pinyons. Pinus chiapensis, a species indigenous to Guatemala and southern Mexico, is the only North American white pine not known to be parasitized by Arceuthobium.
Host Relationships
The hard pines (subgenus Diploxylon) are by far the most common hosts of North American dwarf mistletoes. Twenty-three of the 39 North American taxa are primary parasites of these pines, and 6 other species occur at least rarely on them.
Usually a dwarf mistletoe species parasitizes 1, sometimes 2, or rarely 3 host species in the same stand. We have observed only 3 instances where a particular dwarf mistletoe species parasitized 4 different host species within a stand:
Arceuthobium microcarpum on the San Francisco Peaks, Arizona-Picea engelmannii and Pinus aristata (principal hosts) and Abies lasiocarpa var. arizonica and Pinus strobiformis (rare hosts).
Arceuthobium nigrum near Zacatl<in, Puebla, Mexico-Pinus leiophylla var.leiophylla, P. patula, Pinus teocote (principal hosts), and P. pseudostrobus (occasional host).
Arceuthobium oaxacanum south of Suchixtepec, Oaxaca, Mexico-Pinus lawsonii, P. michoacana, P. pseudostrobus (principal hosts), and P. oaxacana (occasional host).
Artificial Inoculations to Unnatural Hosts
Trees of various species have been inoculated with, and have occasionally become colonized by, dwarf mistletoe species that do not occur naturally within the range of the host species (extra-limital hosts). In some instances, trees co-occurring with a particular dwarf mistletoe are immune to natural infection but can be artificially inoculated. For example, Weir (1918a) inoculated and established Arceuthobium campylopodum on Abies concolor. Even though this species is frequently associated with A. campylopodum in nature, no natural infections have been found. Numerous examples of successful artificial inoculation are reported in table 6.4. Most such experiments have been conducted in unnatural environments, and life cycle data based on such artificial inoculations may be misleading. For example, when Arceuthobium cyanocarpum was grown on Pinus strobiformis in a greenhouse, dwarf mistletoe plants exhibited accelerated growth and produced shoots within 5 months and flowers within 7 months (Hawksworth, unpublished data). In nature, A. cyanocarpum does not produce shoots until 2 or 3 years following infection and flower production requires 4 or 5 years.
The susceptibility of a host species to natural infection by a dwarf mistletoe species with which it
45
Chapter 6
TABLE 6.2 - Susceptibility of hosts for 39 North American taxa of Arceuthobium based on natural infection of native trees
Arceuthobium
A. abietinum f. sp. concoloris
A. abietinum f. sp. magnificae
A. abietis-religiosae
A. americanum
A. apachecum
A. aureum subsp. aureum
A. aureum subsp. petersonii
A. bicarinatum
46
Principal hosts
Abies concolor var. concolor var. lowiana
Abies durangensis ( Abies grandis
Abies magnifica
Abies religiosa var. religiosa var. emarginata
Abies vejari
Pinus banksiana Pinus contorta
var. contorta? var. latifolia var. murrayana
Pinus strobiformis
Pinus montezumae Pinus oaxacana Pinus oocarpa? Pinus pseudostrobus
Pinus michoacana Pinus montezumae Pinus oaxacana Pinus oocarpa Pinus patula Pinus pseudostrobus
Pinus occidentalis
Secondary hosts Occasional hosts
Picea breweriana Abies lasiocarpa var. lasiocarpa
Pinus ponderosa Pinus albicaulis var. scopulorum Pinus flexilis
Pinus jeffreyi Pinus ponderosa
var. ponderosa
Rare hosts Immune taxa
Abies amabilis Abies magnifica Pinus ayacahuite Picea chihuahuana
var. brachyptera Picea engelmannii Pinus contorta Picea pungens
var. murrayana Pinus arizonica Pinus lambertiana Pinus discolor Pinus monticola Pinus flexilis?
Pinus monophylla Pinus muricata Pinus ponderosa
var. ponderosa var. scopulorum
Pinus strobiformis Pinus washoensis Pseudotsuga menziesii Tsuga heterophylla
Pinus arizonica Pinus hartwegii Pinus leiophylla
var. leiophylla Pinus montezumae Pinusrudis Pseudotsuga menziesii
Picea engelmannii Abies grandis Picea glauca Abies lasiocarpa Picea mariana var. lasiocarpa Picea pungens Abies magnifica Pinus aristata Larix occidentalis Pinus attenuata? Tsuga mertensiana Pseudotsuga menziesii
Abies concolor Abies lasiocarpa
var. arizonica Picea pungens Pinus arizonica Pinus edulis Pinus ponderosa
var. scopulorum
Host Relationships
Chapter 6
TABLE 6.2 - Susceptibility of hosts for 39 North American taxa of Arceuthobium based on natural infection of native trees (continued)
Arceuthobium Principal hosts Secondary hosts Occasional hosts Rare hosts Immune taxa
A. blumeri Pinus ayacahuite Abies concolor var. brachyptera Abies durangensis
Pinus strobiformis Abies vejari var. strobiformis Picea chihuahuana var. potosiensis Pinus arizonica
Pinus ponderosa var. scopulorum
Pinus cooperi Pinus durangensis Pinus leiophylla
var. leiophylla Pseudotsuga menziesii
A. californicum Pinus lambertiana Pinus monticola Abies concolor Pinus attenuata Pinus coulteri Pinus jeffreyi Pinus ponderosa
var. ponderosa
A. campylopodum Pinus jeffreyi Pinus attenuata Pinus contorta Pinus lambertiana Abies concolor Pinus ponderosa Pinus coulteri var. latifolia Abies grandis
var. ponderosa var. murrayana Pinus monophylla var. scopulorum Pinus sabiniana Pinus monticola
Pseudotsuga menziesii
A. cyanocarpum Pinus albicaulis Pinus monticola Pinus balfouriana Picea engelmannii? Abies concolor Pinus aristata Tsuga mertensiana subsp. Pinus contorta Abies lasiocarpa Pinus flexilis balfouriana? var. latifolia var. arizonica Pinus longaeva Pinus ponderosa Abies magnifica
var. scopulorum Pinus edulis Pinus lambertiana Pinus ponderosa
var. ponderosa Pseudotsuga menziesii
A. divaricatum Pinus californiarum Pinus jeffreyi subsp. californiarum Pinus leiophylla subsp.fallax var. chihuahuana
Pinus cembroides Pinus ponderosa Pinus discolor var. scopulorum Pinus edulis Pseudotsuga menziesii Pinus monophylla Pinus quadrifolia
A. douglasii Pseudotsuga menziesii Abies amabilis Abies concolor Abies magnifica var. menziesii Abies lasiocarpa Abies grandis Abies vejari var.glauca var. arizonica Abies lasiocarpa Larix occidentalis
var. lasiocarpa Pinus arizonica Picea engelmannii Pinus ayacahuite Picea pungens Pinus discolor
Pinus edulis Pinus engelmannii Pinus flexilis? Pinus ponderosa
var. ponderosa var. scopulorum
Pinus strobiformis Tsuga heterophylla
Host Relationships 47
Chapter 6
TABLE 6.2 - Susceptibility of hosts for 39 North American taxa of Arceuthobium based on natural infection of native trees (continued)
Arceuthobium Principal hosts Secondary hosts Occasional hosts Rare hosts Immune taxa
A. durangense Pinus douglasiana Pinus herrerai Pinus oocarpa? Pinus leiophylla Pinus durangensis var.leiophylla Pinus michoacana Pinus lumholtzii Pinus montezuma Pinus teocote Pinus pseudostrobus
A. gillii Pinus herrerai Pinus arizonica Pinus cembroides Pinus leiophylla var. arizonica Pinus discolor
var. leiophylla Pinus cooperi Pinus engelmannii var. chihuahuana Pinus ponderosa
Pinus lumholtzii var. scopulorum Pinus strobiformis Pseudotsuga menziesii
A.globosum Pinus coo peri Pinus arizonica Pinus teocote Pinus ayacahuite subsp. globosum Pinus durangensis Pinus leiophylla
Pinus engelmannii var. leiophylla Pinus rudis?
A.globosum Pinus douglasiana Cupressus sp.? Abies guatemalense subsp. Pinus durangensis Abies religiosa grandicaule Pinus hartwegii Pinus ayacahuite
Pinus lawsonii Pinus chiapensis Pinus maximinoi Pinus leiophylla Pinus michoacana var. leiophylla Pinus montezumae Pinus patula Pinus pringlei Pinus pseudostrobus Pinusrudis Pinus teocote
A. guatemalense Pinus ayacahuite Abies guatemalense var. ayacahuite Pinus pseudostrobus
Pinusrudis
A. hawksworthii Pinus caribaea var. hondurensis
Pinus oocarpa?
A. hondurense Pinus maximinoi Pinus oocarpa
A.lariq;is Larix occidentalis Pinus contorta Abies lasiocarpa Abies grandis Pseudotsuga menziesii Tsuga mertensiana var. latifolia var.lasiocarpa Picea engelmannii Tsuga heterophylla
Pinus ponderosa Pinus albicaulis var. ponderosa Pinus monticola
A.littorum Pinus muricata Pinus contorta Abies grandis Pinus radiata var. bolanderi Pseudotsuga menziesii
Tsuga heterophylla
A. microcarpum Picea engelmannii Abies lasiocarpa Abies concolor Picea pungens var. arizonica Abies lasiocarpa Pinus aristata Pinus strobiformis var. lasiocarpa
Pinus ponderosa var. scopulorum
Pseudotsuga menziesii
48 Host Relationships
Chapter 6
TABLE 6.2 - Susceptibility of hosts for 39 North American taxa of Arceuthobium based on natural infection of native trees (continued)
Arceuthobium Principal hosts Secondary hosts Occasional hosts Rare hosts Immune taxa
A. monticola Pinus monticola Pinus lambertiana Picea breweriana Pinus jeffreyi Pinus attenuata Pinus ponderosa
var. ponderosa
A. nigrum Pinus lawsonii Pinus montezumae Pinus arizonica Pinus ayacahuite Pinus leiophylla Pinus pseudostrobus var. arizonica Pinus durangense
var. leiophylla Pinus coo peri Pinus engelmannii var. chihuahuana Pinus oocarpa
Pinus lumholtzii Pinus oaxacana Pinus patula Pinus teocote
A. oaxacanum Pinus lawsonii Pinus oaxacana Pinus michoacana Pinus pseudostrobus
A. occidentale Pinus sabiniana Pinus attenuata Pinus jeffreyi Pinus coulteri Pinus ponderosa
var. ponderosa
A.pendens Pinus discolor Pinus cembroides? Pinus orizabensis
A.pusillum Picea glauca Larix laricina Abies balsamea Pinus rigida? Picea mariana Pinus banksiana Picea rubens Pinus resinosa
Pinus strobus
A. rubrum Pinus coo peri Pinus ayacahuite Pinus durangensis Pinus engelmannii Pinus herrerai Pinus teocote
A. siskiyouense Pinus attenuata Pinus contorta Pinus lambertiana var. contorta Pinus monticola
Pinus jeffreyi Pinus ponderosa
var. ponderosa
A. strictum Pinus leiophylla Pinus teocote Pinus engelmannii Pinus cembroides var. chihuahuana
A. tsugense Abies amabilis? Abies grandis? Picea engelmannii Pinus contorta subsp. tsugense Abies lasiocarpa Pinus contorta Picea sitchensis var. murrayana
var. lasiocarpa? var. lati/olia Pinus monticola Abies procera? Tsuga mertensiana Pinus contorta Pseudotsuga menziesii
var. contorta Tsuga heterophylla
A. tsugense Abies amabilis Pinus albicaulis Pinus monticola Picea breweriana Abies magnifica subsp. mertensianae Abies lasiocarpa Pinus contorta Pinus contorta
var. lasiocarpa var. lati/olia var. murrayana Abies procera Tsuga heterophylla Pseudotsuga menziesii Tsuga mertensiana Abies grandis
Host Relationships 49
Chapter 6
TABLE 6.2 - Susceptibility of hosts for 39 North American taxa of Arceuthobium based on natural infection of native trees (continued)
Arceuthobium Principal hosts Secondary hosts Occasional hosts Rare hosts Immune taxa
A. vaginatum Pinus arizonica Pinus teocote Pinus culminicola Abies religiosa subsp. vaginatum var. arizonica Abies vejari
var. stormiae Pinus ayacahuite Pinus cooperi Pinus leiophylla Pinus durangensis var. leiophylla Pinus engelmannii var. chihuahuana Pinus hartwegii Pinus lumholtzii Pinus herrerai Pinus pseudostrobus? Pinus lawsonii Pseudotsuga menziesii Pinus montezumae Pinus patula Pinusrudis
A. vaginatum Pinus arizonica Pinus coo peri Pinus aristata Pinus flexilis Abies concolor subsp. cryptopodum var. arizonica Pinus contorta Pinus strobiformis Abies lasiocarpa
var. stormiae var. latifolia var. arizonica Pinus durangensis Picea pungens Pinus engelmannii Pinus californiarum Pinus ponderosa subsp.fallax
var. scopulorum Pinus cembroides Pinus edulis Pinus herrerai Pinus leiophylla
var. leiophylla var. chihuahuana
Pseudotsuga menziesii
A. verticillijlorum Pinus arizonica Pinus ayacahuite var. arizonica Pinus cembroides
Pinus cooperi Pinus leiophylla Pinus durangensis var. leiophylla Pinus engelmannii var. chihuahuana
Pinus teocote
A. yecorense Pinus durangensis Pinus engelmannii Pinus arizonica Pinus herrerai Pinus leiophylla
var. chihuahuana Pinus lumholtzii
Note: a question mark indicates that we have not determined the appropriate susceptibility class or that the reported host-parasite combination has not been confrrmed.
50 Host Relationships
Chapter 6
TABLE 6.3 - Host susceptibility of 85 taxa of North American Pinaceae to natural infection by Arceuthobium
Host
True firs
Abies amabilis
Abies balsamea
Abies concolor var. concolor
Abies concolor var. lowiana
Abies durangensis
Abies grandis
Abies lasiocarpa var. lasiocarpa
Abies lasiocarpa var. arizonica
Abies magnifica
Abies procera
Abies religiosa var. religiosa
Abies religiosa var. emarginata
Abies vejari
Larches
Larix laricina
Larix occidentalis
Spruces
Picea breweriana
Host Relationships
Arceuthobium
A. abietinum f. sp. concoloris A. douglasii A.~ugensesubsp.~ugense A. tsugense subsp. mertensianae
A.pusillum
A. abietinum f. sp. concoloris A. douglasii
A. abietinum f. sp. concoloris
A. abietinum f. sp. concoloris
A. abietinum f. sp. concoloris A. douglasii A.laricis A.~ugensesubsp.~ugense
A. tsugense subsp. mertensianae
A. abietinum f. sp. concoloris A. douglasii A.laricis A.~ugensesubsp.~ugense A. tsugense subsp. mertensianae
A. douglasii A. microcarpum
A. abietinum f. sp. magnificae
A.~ugensesubsp.~ugense A. tsugense subsp. mertensianae
A. abietis-religiosae
A. abietis-religiosae
A. abietis-religiosae
A.pusillum
A.laricis A. tsugense subsp. tsugense
A. abietinum f. sp. concoloris A. monticola A. tsugense subsp. mertensianae
Susceptibility
Rare Occasional Principal? Principal
Rare
Principal Rare
Principal
Principal
Principal Rare Rare Occasional? Rare
Occasional Rare Occasional Principal? Principal
Occasional Rare
Principal
Principal? Principal
Principal
Principal
Principal
Occasional
Principal Rare
Secondary Occasional Rare
51
TABLE 6.3 - Host susceptibility of 85 taxa of North American Pinaceae to natural infection by Arceuthobium (continued)
Host
Spruces (continued)
Picea engelmannii
Picea glauca
Picea mariana
Picea pungens
Picea rubens
Picea sitchensis
Pines - Subgenus Haploxylon
Pinus albicaulis
Pinus aristata
Pinus ayacahuite var. ayacahuite
Pinus ayacahuite var. brachyptera
Arceuthobium
A. americanum A. cyanocarpum A. douglasii A.laricis A. microcarpum A.~ugensesubsp.~ugense
A. americanum A.pusillum
A. americanum A.pusillum
A. americanum A. douglasii A. microcarpum
A.pusillum
A.~ugensesubsp.~ugense
A. americanum A. cyanocarpum A.laricis A. tsugense subsp. mertensianae
A. americanum A. cyanocarpum A. microcarpum A. vaginatum subsp. cryptopodum
A. guatemalense
A. abietinum f. sp. concoloris A. blumeri
Pinus balfouriana subsp. balfouriana A. cyanocarpum
52
Pinus californiarum subsp. californiarum
Pinus californiarum subsp.fallax
Pinus cembroides
Pinus orizabensis
Pinus culminicola
Pinus discolor
A. divaricatum
A. divaricatum
A. divaricatum
A.pendens
A. vaginatum subsp. vaginatum
A. divaricatum A.pendens
Susceptibility
Rare Rare? Rare Rare Principal Rare
Rare Principal
Rare Principal
Rare Rare Principal
Principal
Rare
Occasional Principal Rare Secondary
Rare Principal Principal Occasional
Principal
Rare Principal
Occasional?
Principal
Principal
Principal
Principal
Rare
Principal Principal
Chapter 6
Host RelationshiPs
Chapter 6
TABLE 6.3 - Host susceptibility of 85 taxa of North American Pinaceae to natural infection by Arceuthobium (continued)
Host
Pines - Subgenus Haploxylon (continued)
Pinus edulis
Pinus flexilis
Pinus lambertiana
Pinus longaeva
Pinus monophylla
Pinus monticola
Pinus quadrifolia
Pinus strobiformis var. strobiformis
Pinus strobiformis var. potosiensis
Pinus strobus
Pines - Subgenus Diploxylon
Pinus arizonica var. arizonica
Pinus arizonica var. stormiae
Host Relationships
Arceuthobium
A. diva rica tum
A. americanum A. cyanocarpum A. vaginatum subsp. cryptopodum
A. abietinum f. sp. concoloris A. californicum A. campylopodum A. monticola
A. cyanocarpum
A. divaricatum
A. abietinum f. sp. concoloris A. californicum A. cyanocarpum A.laricis A. monticola A. tsugense subsp. tsugense A. tsugense subsp. mertensianae
A. divaricatum
A. apachecum A. blumeri A. microcarpum A. vaginatum subsp. cryptopodum
A. blumeri
A.pusillum
A. gillii A. globosum subsp. globosum A. nigrum A. vaginatum subsp. vaginatum A. vaginatum subsp. cryptopodum A. verticilliflorum
A. vaginatum subsp. vaginatum A. vaginatum subsp. cryptopodum
Susceptibility
Principal
Occasional Principal Rare
Rare Principal Rare Secondary
Principal
Principal
Rare Secondary Secondary Rare Principal Rare Occasional
Principal
Principal Principal Rare Rare
Principal
Rare
Rare Occasional Rare Principal Principal Principal
Principal Principal
53
TABLE 6.3 - Host susceptibility of 85 taxa of North American Pinaceae to natural infection by Arceuthobium (continued)
Host
Pines - Subgenus Diploxylon (continued)
54
Pinus attenuata
Pinus banksiana
Pinus caribaea var. hondurensis
Pinus contorta var. contorta
Pinus contorta var. bolanderi
Pinus contorta var. lati/olia
Pinus contorta var. murrayana
Pinus cooperi
Pinus coulteri
Pinus douglasiana
Pinus durangensis
Arceuthobium
A. americanum A. campylopodum A. occidentale A. siskiyouense
A. americanum
A. hawksworthii
A. siskiyouense A. tsugense subsp. tsugense
A.littorum
A. americanum A. campylopodum A. cyanocarpum A.laricis A.~ugensesubsp.~ugense A. tsugense subsp. mertensianae A. vaginatum subsp. cryptopodum
A. abietinum f. sp. concoloris A. americanum A. campylopodum
A. gillii A. globosum subsp. globosum A. nigrum A. rubrum A. vaginatum subsp. vaginatum A. vaginatum subsp. cryptopodum A. verticilliflorum
A. campylopodum A. occidentale
A. durangense A. globosum subsp. grandicaule
A. abietinum f. sp. concoloris A. durangense A. globosum subsp. globosum A. globosum subsp. grandicaule A. rubrum A. vaginatum subsp. vaginatum A. vaginatum subsp. cryptopodum A. verticilliflorum A. yecorense
Susceptibility
Rare? Secondary Secondary Principal
Principal
Principal
Rare Principal
Occasional
Principal Occasional Rare Secondary Occasional Rare Occasional
Rare Principal Occasional
Rare Principal Rare Principal Principal Secondary Principal
Secondary Secondary
Principal Principal
Principal Principal Principal Principal Principal Principal Principal Principal Principal
Chapter 6
Host Relationships
Chapter 6
TABLE 6.3 - Host susceptibility of 85 taxa of North American Pinaceae to natural infection by Arceuthobium (continued)
Host
Pines -Subgenus Diploxylon (continued)
Pinus engelmannii
Pinus hartwegii
Pinus herrerai
Pinus jeffreyi
Pinus lawsonii
Pinus leiophylla var. leiophylla
Pinus leiophylla var. chihuahuana
Pinus lumholtzii
Pinus maximinoi
Pinus michoacana
Host Relationships
Arceuthobium
A. globosum subsp. globosum A. rubrum A. strictum A. vaginatum subsp. vaginatum A. vaginatum subsp. cryptopodum A. verticilliflorum A. yecorense
A. globosum subsp. grandicaule A. vaginatum subsp. vaginatum
A. durangense A. gillii A. rubrum A. vaginatum subsp. vaginatum A. yecorense
A. americanum A. campylopodum A. monticola A. occidentale A. siskiyouense
A. globosum subsp. grandicaule A. nigrum A. oaxacanum A. vaginatum subsp. vaginatum
A. gillii A. nigrum
A. gillii A. nigrum A. strictum A.yecorense
A. gillii A. nigrum A. yecorense
A. globosum subsp. grandicaule A. hondurense
A. aureum subsp. petersonii A. durangense A. globosum subsp. grandicaule A. oaxacanum
Susceptibility
Principal Principal Rare Principal Principal Principal Secondary
Principal Principal
Secondary Principal Principal Principal Principal
Occasional Principal Rare Occasional Rare
Principal Principal Principal Principal
Principal Principal
Principal Principal Principal Principal
Principal Principal Principal
Principal Principal
Principal Principal Principal Principal
55
TABLE 6.3 -Host susceptibility of85 taxa of North American Pinaceae to natural infection by Arceuthobium (continued)
Host
Pines-Subgenus Diploxylon (continued)
Pinus montezumae
56
Pinus muricata
Pinus oaxacana
Pinus occidentalis
Pinus oocarpa
Pinus patula
Pinus ponderosa var. ponderosa
Pinus ponderosa var. scopulorum
Pinus pringlei
Pinus pseudostrobus
Arceuthobium
A. aureum subsp. aureum A. aureum subsp. petersonii A. durangense A. globosum subsp. grandicaule A. nigrum
A.littorum
A. aureum subsp. aureum A. aureum subsp. petersonii A. nigrum A. oaxacanum
A. bicarinatum
A. aureum subsp. aureum A. aureum subsp. petersonii A. durangense A. hawksworthii A. hondurense
A. aureum subsp. petersonii A. globosum subsp. grandicaule A. nigrum A. vaginatum subsp. vaginatum
A. americanum A. campylopodum A.laricis A. occidentale A. siskiyouense
A. americanum A. campylopodum A. cyanocarpum A. vaginatum subsp. cryptopodum
A. globosum subsp. grandicaule
A. aureum subsp. aureum A. aureum subsp. petersonii A. durangense A. globosum subsp. grandicaule A. nigrum A. oaxacanum
Susceptibility
Principal Principal Principal Principal Occasional
Principal
Principal Principal Principal Occasional
Principal
Principal? Principal Occasional? Principal? Principal
Principal Principal Principal Principal
Occasional Principal Occasional Occasional Rare
Secondary Principal Rare Principal
Principal
Principal Principal Principal Principal Occasional Principal
Chapter 6
Host Relationships
Chapter 6
TABLE 6.3 -Host susceptibility of 85 taxa of North American Pinaceae to natural infection by Arceuthobium (continued)
Host
Pines-Subgenus Diploxylon (continued)
Pinus radiata
Pinus resinosa
Pinusrudis
Pinus sabiniana
Pinus teocote
Douglas-fir
Pseudotsuga menziesii
Hemlocks
Tsuga heterophylla
Tsuga mertensiana
Arceuthobium
A.littorum
A.pusillum
A. globosum subsp. globosum A. globosum subsp. grandicaule A. vaginatum subsp. vaginatum
A. campylopodum A. occidentale
A. globosum subsp. globosum A. globosum subsp. grandicaule A. nigrum A. rubrum A. strictum A. vaginatum subsp. vaginatum
A. americanum A. douglasii A. tsugense subsp. tsugense
A.~ugensesubsp.~ugense
A. tsugense subsp. mertensianae
A. cyanocarpum A.laricis A.~ugensesubsp.~ugense
A. tsugense subsp. mertensianae
Susceptibility
Principal
Rare
Principal? Principal Principal
Occasional Principal
Rare Principal Principal Principal Occasional Secondary
Rare Principal Rare
Principal Rare
Secondary Principal Rare Principal
Note: A question mark indicates that we have not determined the appropriate susceptibility class or that the reported host-parasite combination has not been confirmed.
Host Relationships 57
does not naturally occur is sometimes economically important (table 6.5). For example, Graham and Leaphart (1961) reported that Pinus sylvestris cultivated in Washington was so severely parasitized by Arceuthobium laricis that they recommended this species should not be planted where A. laricis is present.
Nonhosts Because dwarf mistletoes parasitize so many west
ern conifer species, it is of interest to know which are not hosts. We list here the few members of the Pinaceae from the western United States and Mexico that have not been found to be naturally infected by Arceuthobium. Some of these species, however, could be hosts because many Arceuthobium collections from Mexico do not identify the host species. Of the 14 species of pine listed below, 6 are pinyons (indicated by asterisks).
True firs
Abies guatemalensis Abies hickelii Abies mexicana Abies oaxacana
Spruces
Picea chihuahuana Picea martinezii Picea mexicana
Pines
Pinus balfouriana subsp. austrina Pinus chiapensis Pinus greggii Pinus jaliscana Pinus johannis* Pinus lagunae Pinus maximartinezii * Pinus nelsonii * Pinus pinceana * Pinus praetermissa Pinus remota * Pinus rzedowskii* Pinus torreyana Pinus washoensis
Douglas-fir
Pseudotsuga macrocarpa
58
Chapter 6
Host-Parasite Relationships An interesting feature of parasitism by
Arceuthobium is the existence of a kind of "competitive host exclusion" between different mistletoe species (Hawksworth 1969). If a species of Arceuthobium that typically infests a certain host species is present in an area, then other dwarf mistletoe species only rarely infest that host species; if the principal parasite of that host species is not present, however, then another dwarf mistletoe species present in the area is likely to infest the host species. Several examples of host exclusion are found in the Colorado Front Range, where Pinus contorta is typically the principal host of A. americanum and P ponderosa is typically the principal host of A. vaginatum subsp. cryptopodum. Infection of P ponderosa trees by A. americanum was only 13% in stands where both mistletoe species were present, but 64% in stands where A. vaginatum subsp. cryptopodum was absent (Hawksworth 1969), The converse situation also occurs with respect to infection of P contorta trees by A. vaginatum subsp. cryptopodum and A. americanum (Hawksworth 1969). Other examples involve the combination of A. americanum (principal host P contorta) withA. cyanocarpum (principal host Pflexilis) in Colorado (Hawksworth and Wiens 1972) andA. occidentale (principal host P sabiniana) with A. campylopodum (principal hosts P ponderosa and P jeffreyz) in California. Wiens (1961) also noted such competitive host exclusion in mistletoes of the genus Phoradendron parasitizing junipers near Sedona, Arizona (Pjuniperinum andP densum). The mechanism that controls this phenomenon constitutes a fascinating subject for additional research.
If a host is rarely parasitized by a species of Arceuthobium, parasitism is often an "all or nothing" phenomenon: that is, most trees of a rare host species are immune, but trees that are infected tend to be heavily infected. For example, Picea engelmannii is a rare host «1 % of trees infected) of A. americanum, but those trees that are parasitized typically bear hundreds of infections (Hawksworth and Graham 1963).
Some species that are exceedingly rare appear to have little resistance to dwarf mistletoe infection. For example, Pinus culminicoldhas one ofthe most restricted distributions of all pinyons, yet it is readily parasitized by Arceuthobium vaginatum subsp. vaginatum on Cerro Potosi, Mexico. Also, Picea breweriana is often heavily infested by A. abietinum f. sp. concoloris, A. monticola, and A. tsugense subsp. mertensianae where the host occurs with these dwarf mistletoes. No dwarf mistletoe occurs within the limited distribution ot Pinus torreyana, but Kuijt (1960a)
Host Relationships
Chapter 6
TABLE 6.4 -Extension of Arceuthobium host range for 27 Pinaceae taxa based on reports of successful artificial inoculation
Host
True firs
Abies amabilis
Abies concolor
Abies grandis
Larches
Larix decidua
Larix kaempferi
Larix occidentalis
Spruces
Piceaabies
Arceuthobium Reference
A.laricis Smith and Wass 1972b A. tsugense subsp. tsugense
(shore pine race) Smith 1974
A. campylopodum Weir 1918a
A. campylopodum Weir 1918a A.~ugensesubsp.~ugense
(shore pine race) Smith 1974
A.laricis Weir 1918a
A.laricis Weir 1918a
A. campylopodum Weir 1918a A.~ugensesubsp.~ugense
(shore pine and western hemlock races) Smith 1970a
Weir 1918a A. campylopodum A.laricis A.~ugensesubsp.~ugense
Hawksworth and Wiens 1972
Picea glauca
Picea engelmannii
Pines
Pinus banksiana
Pinus bungeana
Pinus caribaea
Pinus contorta var. latifolia
Host Relationships
(western hemlock race)
A.laricis A.~ugensesubsp.~ugense
(western hemlock race) A. tsugense subsp. tsugense
(shore pine race)
A. tsugense subsp. tsugense (shore pine and western hemlock races)
A.laricis A. occidentale
A. occidentale
A. occidentale
A. tsugense subsp. tsugense (shore pine and western hemlock races)
Smith 1965
Smith 1974
Smith 1965
Smith 1974
Smith 1970b
Graham 1959a Hedgcock and Hunt 1917
Hedgcock and Hunt 1917
Hedgcock and Hunt 1917
Smith 1974
59
Chapter 6
TABLE 6.4 -Extension of Arceuthobium host range for 27 Pinaceae taxa based on reports of successful artificial inoculation (continued)
Host
Pines (continued)
Pinus flexilis
Pinusmugo
Pinus palustris
Pinuspinea
Pinus ponderosa
Pinus radiata
Pinus resinosa
Pinus strobiformis
Pinus strobus
Pinus sylvestris
Pinus torreyana
Pinus virginiana
Douglas-fir
Pseudotsuga menziesii
Hemlocks
Tsuga canadensis
60
Arceuthobium
A. apachecum A. blumeri A. microcarpum
A. americanum A. campylopodum
A. occidentale
A. occidentale
A.laricis A.~ugensesubsp.~ugense
(shore pine and western hemlock races)
A. occidentale A. tsugense subsp. tsugense
(western hemlock race)
A. campylopodum A.laricis
A. cyanocarpum
A. cyanocarpum
A. campylopodum A.laricis A. tsugense subsp. tsugense
(western hemlock race)
A. occidentale
A. occidentale
A.~ugensesubsp.~ugense (shore pine and western hemlock races)
A. tsugense subsp. tsugense (western hemlock race)
Reference
Mathiasen 1978 Mathiasen 1978 Mathiasen 1978
Weir 1918a Weir 1918a
Hedgcock and Hunt 1917
Hedgcock and Hunt 1917
Smith 1974
Smith and Craig 1968
Scharpf 1969a
Smith and Craig 1968
Weir 1918a Hawksworth and Wiens 1972
Hawksworth and Wiens 1972
Hawksworth and Wiens 1972
Weir 1918a Graham and Leaphart 1961
Smith and Craig 1968
Kuijt 1960a
Hedgcock and Hunt 1917
Smith and Wass 1972a
Weir 1918a
Host Relationships
Chapter 6
TABLE 6.5 -Natural infection by Arceuthobium on extra-limital hosts
Host Arceuthobium Location Reference
Cypress
Cupressus arizonica A.oxycedri Spain Rios Insua 1984b A.oxycedri Russia Isikov and Zakharenko 1988
Cupressus lusitanica A.oxycedri Russia Isikov and Zakharenko 1988
Cupressus macrocarpa A.oxycedri Russia Zefirov 1955, Isikov and Zakharenko 1988
Cupressus macnabiana A.oxycedri Russia Isikov and Zakharenko 1988
Juniper
Juniperus virginiana A.oxycedri Russia Isikov and Zakharenko 1988
Larch
Larix decidua A.~ugensesubsp.~ugense BC, Canada Kuijt 1964 (western hemlock race)
Spruce
Piceaabies A. campylopodum WA K. Russell (first report) A.laricis ID Hawksworth and Wiens 1972
Picea pungens A.pusillum MA USDA 1960 A.pusillum Canada Davis and Myren 1990
Pine
Pinus banksiana A.laricis ID Graham 1960
Pinus halepensis A. campylopodum CA Scharpf and Hawksworth 1986 A. occidentale CA Scharpf and Hawksworth 1986
Pinus pinaster A. campylopodum CA Kuijt 1960b A. occidentale CA Scharpf and Hawksworth 1986
Pinuspinea A. occidentale CA Scharpf and Hawksworth 1986
Pinus radiata A. occidentale CA Hawksworth and Wiens 1972
Pinus resinosa A.laricis ID Hawksworth and Wiens 1972
Pinus sylvestris A. americanum AB, Canada Powell 1968 A. americanum WA Graham and Leaphart 1961 A. campylopodum ID Hawksworth and Wiens 1972 A.laricis WA Graham and Leaphart 1961 A. occidentale CA Scharpf and McCain 1988 A. vaginatum subsp. cryptopodum CO Hawksworth and Laut 1981 A. vaginatum subsp. cryptopodum AZ R. Celaya
(personal communication 1992)
Pinus thunbergii A. occidentale CA Scharpf and Hawksworth 1986
Platycladus
Platycladus orientalis A.oxycedri Russia Isikov and Zakharenko 1988
Host Relationships 61
inoculated a tree of this species with A. occidentale and found it to be susceptible.
A number of inoculation experiment'i have shown that various species are not compatible hosts for particular dwarf mistletoes (table 6.6). Features of the dwarf mistletoe that often indicate host- parasite incompatibility are reduced (sometimes complete lack of) shoot development and unusually large swellings at the point of infection.
Host Reactions to Dwarf Mistletoe Infection
The first external symptom of dwarf mistletoe infection is usually a swelling of the host tissues. As an infection develops, swelling enlarges and eventually becomes fusiform. Typically, dwarf mistletoe infection leads to the production of the profusely branched, dense masses of distolled host branches called "witches' brooms." Two basic types of witches' brooms are formed (Kuijt 1960b, Hawkswollh 1961a):
Systemic or isophasic (fig. 6.3)-Growth of the endophytic system keeps pace with apical and cambial growth of the infected branch, and the dwarf mistletoe shoots are scattered along the host branch or concentrated at branch girdles.
Non-systemic or anisophasic (fig. 6.4)-Shoots of the dwarf mistletoe remain localized near the original site of infection, and the endophytic system only keeps pace only with cambial growth.
Chapler6
Figure 6.3 -Arceulhoblum pusiiJllm on Picea g/auca; note typical systemic (isophasic) infection; lack of host swelling and presence of sequentially more marure mistetoe shoots on older portion of host branch.
In general, the type of witches' broom formation is characteristic of the parasite species rather than the host species; therefore broom type is an important taxonomic character in Arceuthobium. Although a dwarf mistletoe species that typicaUy forms non-systemic brooms will rarely induce formation of a systemic broom, there is never any question regarding the basic type of witches' broom produced.
Systemic witches' brooms are consistently formed by Arceuthobium americanum, A. douglasii, A. guatema/ense, A. minutissimum, and A. pusi//um, and apparently by the Asian species A. chinense, A. sichuanense, and A. pini (Hawksworth and Wiens
TABLE 6.6 - Incompatible relationships of Arceuthobium with potential hosts
Arceuthobium
A. abietinum f. sp. conc%ris
A. americanum
A.pusillum
A. tsugense subsp. tsugense
A. vaginatuffl subsp. cryptopodum
62
Potential host
Pinus ayaeahuite Pinus contorta Pinus lambertiana
Pinus a/bieau/is Picea pungens Pseudotsuga menziesii
Larix /ancina
Larix decidua Larix occidenta/is Picea enge/mannii Picea sitchensis
Pinusjlexflis
Reference
First repoll Hawksworth and Wiens 1972 Hawksworth and Wiens 1972
Weir 1918b Hawksworth and Wiens 1972 Hawksworth and Wiens 1972
Tainter and French 1967
Kuijt 1964 Hawksworrh and Wiens 1972 Hawksworth and Wiens 1972 Laurent 1966
First report
Host Relationships
Chapter 6
Figure 6.4 -Arceulhobium vaginalum subsp. crytopodum on Pinus ponderosa; note typical local (anisophasic) infection: tight clustering of mistletoe shoots on a swollen branch.
Figure 65 -Arcellthobillm allrel/m subsp. aureum on Pil/US pseudostrobus; note the presence of local infections but lack of broom formation. (c. G. Shaw III)
1972, Kiu 1984b). Non-systemic witches' brooms are much more common among trees parasitized by North American dwarf mistle[Qes. At the type locality of A. pendens, only staminate plants appeared to produce systemic infections; this particular form of sexual dimorphism deserves fu rther study.
A few dwarf mistletoe taxa do not induce witches' broom formation in their hosts-Arceuthobium aureum subsp. aureum (fig. 6.5) and A. globosum subsp.globosum. Although A. occidentale does not induce typical broom formation, it does promote some "broom-like development in Pinus sabiniana (R. F. Scharpf, personal communication).
Host Relationships
Arceuthobium americanum produces shoots only at the girdles and not on segments of Pinus contorta branches more than 5 years old (Kuijt 1960b). Similarly, our limited observations of systemic infections of A. abietis-religiosae on Abies religiosa suggest that here, also, the dwarf mistletoe shoots are produced only at girdles.
Within a particular host genus, the types of witches' broom formed by a dwarf mistletoe species are generally similar [Weir 1916c, Hawksworth 1956a, Kuijt 1960b). For example, the witches' brooms formed by Arceuthobium americanum on all pines are similar, but brooms on spruces are distinctly different from those on pines (Hawksworth and Graham 1963, Kuijt 1960b),
Although systemically infected branches are USll
ally immune to additional infection, Muir (1968) reported several secondary infections of Arceuthobium americanum on a witches' broom of Pinus banksiana. In Oregon, R. Tinnin (personal communication) has also observed secondary infections on witches' brooms of P. contorla induced by A. americanum. Secondary infections are detectable by location of shoots, differences in shoot color, differences in sex, and the formation of swellings. We have also rarely observed secondary infections in the following paraSite-host combinations:
Arceuthobium americanum on Pinus contorta in Colorado.
Arceuthobium douglasii on Pseudotsuga menziesii in Oregon.
Arceuthobium guatemalense on Pinus ayacahuite in Guatemala.
Arceuthobium vaginaturn subsp. cryptopodum on Pinus ponderosa in Arizona. Arceuthobium tsugense on Tsuga heterophylla in Alaska (c. Shaw, personal communication)
Kuijt (1960b) reported that cones usually are not produced on witches' brooms, particularly on systemic brooms. We have frequently observed cone formation on witches' brooms of Pseudotsuga menziesii caused by Arceuthobium dougfasii, however. Cones were about half normal size, and apparently contained viable seeds. Bonga (1964) noted fertile cones on an aberrant witches' broom in Picea mariana caused by A. pusillum. Schaffer and others (1983) obs,erved cones on several systemic witches' brooms on Pinus contorta induced by A. arnericanum, but all the cones were sterile.
63