dwarf mistletoes: biology, pathology, and systematics · chapter 6 as shown in table 6.3, some host...

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



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




Chapter 6



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


Chapter 6



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


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.


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. 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.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


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


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


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


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 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


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


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. cyanocarpum A.laricis A.~ugensesubsp.~ugense


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.


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


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


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


A. campylopodum A.laricis

A. cyanocarpum

A. cyanocarpum

A. campylopodum A.laricis A. tsugense subsp. tsugense


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



Smith 1974

Smith and Craig 1968

Scharpf 1969a


Weir 1918a Hawksworth and Wiens 1972



Weir 1918a Graham and Leaphart 1961


Kuijt 1960a


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


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

dwarf mistletoes: biology, pathology, and systematics · chapter 6 as shown in table 6.3, some host...

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