Occurrence of mycorrhizae on ericaceous and pyrolaceous plants in northern California'

DAVIDL. LARGENT,NEIL SUGIHARA, AND CARLWISHNER Departtnetlt oJ'Biology, Hrrt?lbolrlt Stnte Utliuersity, Arcnta, CA, U.S.A. 95521 Received October 23, 1979 LARGENT,D. L., N. SUGIHARA,and C. WISHNER.1980. Occurrence of mycol~hizaeon encace- ous and pyrolaceous plants in northern California. Can. J. Bot. 58: 2274-2279. Four hundred and eighty plants in northern California frorn 27 taxa in the Ericaceae and 5 in the Pyrolaceae were surveyed for presence of ectomycorrhizae, arbutoid, or ericoid mycorrhizae between September 1977 and April 1978. Of these, 337 in the Ericaceae and 8 in the Pyrolaceae had one or more types of mycorrhizae. At least 88% of the plants of larger shrubs or trees (Arbrrtrrs tnetlziesii or A,rtostal>lrylos spp.) were mycorrhizal in various locations in northern California. Of the plants in the remaining twenty-two taxa that were mycorrhizal, 67-100% had ectomycorrhizae or arbutoid mycorrhizae. Twenty-three taxa of ericaceous or pyrolaceous plants in the genera Cnssiope, Goirltherin, Kriltnin, Ledrrtn, Lertcotlror, Pllyllodoce, Rhorlodet~rlrot~,Vrrccitlirrtn, Pyrolrr, and Cllitnrrphilrr were also mycorrhizal. The type and abundance of mycorrhizae appear to depend on as yet undefined ecological factors. Ectomycorrhizae (including the Cet~ococcritntype) or ericoid mycorrhizae are reported for the first time in Arb~rtlr~,most Arctostaplrylos spp., Garrltherirr slrrrllotl, Knltnia poliJolirr, Lrrlron glrrt~rlrrlosrrtnvar. coliitnbirrtrrrtn, Lerrcothoe drruisirrr, Rhorlorlet~drot~tnrrcroplryllrrt?~, Vrrccitlirrtn rrrbrrscrrlrr, V. ou~trit?~,V. scoprrri11t71, Chitnrrplriln tnetrziesii, and Pyrolrr pictrr f. pictrr.

LARGENT,D. L., N. SUGIHARAet C. WISHNER.1980. Occurrence of mycorrhizae on ericaceous and pyrolaceous plants in northern California. Can. J. Bot. 58: 2274-2279. Entre septembre 1977 et avril 1978,480 plantes du nord de la Californie appartenant i 27 taxons parmi les Ericaceae et i 5 taxons parmi les Pyrolaceae ont it6 examinees dans le but d'y verifier la presence d'ectornycorhizes.de mycorhizes arbuto'ides et de mycorhizes erico'ides. Parmi ces plantes, 337 Cricacees et 8 pyrolacees avaient au moins un type de mycorhize. Au moins 88% des gros arbustes et des arbres (Arbrrtrrs tnetlziesii et Arctostrrphylos spp.) etaient mycorhizes dans diverses localites du nord de la Californie. Parmi les plantes des 22 autres taxons mycorhizes, 67-100% avaient des ectomycorhizes ou des mycorhizes arbuto'ides. Les plantes de 23 taxons appartenant aux genres Cnssiope, Gaiiltlrerirr, Krrlt?lirr,Ledrrtn, Lr~rcothoe, Pl~yllodoce,Rhorlodet~drotl, Vnccitliritn, Pyrola et Cl~itnrrphilnetaient aussi mycorhizees. Le For personal use only. type et I'abondance de mycorhizes semblent dependre de facteurs ecologiques non encore identifies. La presence d'ectomycorhizes (y compris le type Cetrococcrrtn) ou de mycorhizes Crico'ides est signalee pour la premiere fois chez Arbrrtrrs, la plupart des especes d'Arctostaphylos, Grrrrltherin shrrllotl, Knltnia polifolirr, Ledrrtn glnt~dirlosrrtn var. col~rmbiat~rrtn,Lerrcothoe drroisine, Rhododetlrlron t?lrrcrophyllritn, Vrrccitlirrtn rrrbrrscrrln, V. oontrrtn, V. scoprrrilrtn, Chitnnphiln tnetlziesii et Pyrolrr pictn f. picta. [Traduit par le journal] Introduction most of these taxa and presents the results of a Forty taxa in the Pyrolaceae and Ericaceae form preliminary survey of the types of mycorrhizae of an integral part of the coastal, mixed evergreen, ericaceous and pyrolaceous plants made in north- montane, and subalpine forests in north central and ern California between September 1977 and April 1978.

Can. J. Bot. Downloaded from www.nrcresearchpress.com by USDANALBF on 07/22/16 northwestern California (Munz and Keck 1968; Sawyer and Thornburg 1977; Sawyer et a1 1977; Materials and methods Barker 1976; Table 1). Except for Arbutus men- Roots of 32 taxa of ericaceous and pyrolaceous plants were ziesii and Arctostaphylos uua-ursi (Trappe 1964; collected from locations in northern California ranging from California State Highway 128 in the south, the eastern slopes of Zak 1973, 1974, 1976a, 19766) the mycorrhizae of the Klamath National Forest in the east, the California-Oregon these taxa have not been studied. Accordingly, this border in the north, and the Pacific Ocean in the west. The exact paper represents the first reports of mycorrhizae in localities have been placed in the Depository of Unpublished Data.2 lSupport for this study was supplied by the U.S. Department Two to three root samples from an individual plant were of Agriculture Forest Service, Pacific Northwest Forest and Range Experiment Station, Corvallis, OR, cooperative agree- 2This information is available, at a nominal charge, from the ment NO. 60-PNW-79 and frorn McIntyre-Stennis grant No. 48, Depository of Unpublished Data, CISTI, National Research Humboldt State University. Council of Canada, Ottawa, Ont., Canada KIA OS2. 0008-4026/80/212274-06$0 1 .OO/O @ 1980 National Research Council of Canada/Conseil national de recherches du Canada LARGENT ET AL

TABLE1. Ericaceous and pyrolaceous plants located in northern California

Taxa Months studied

Included in this study Ericaceae Arbrrtlrs tt~et~ziesiiPursh. 1977: October-November ; 1978: January-March Arctostapl~yloscntiescetls Eastw. 1977 : November-December ; 1978 : March Arctostnpl~yloscollrtt~binna Piper 1977 : October-November; 1978 : January-March Arctostapltylos glat~dlrlosnEastw. 1977: December Arctostapl~ylosit~tricnto Howell var. oblot~gifolia(Howell) Munz. 1978: February Arctostnpl~ylostt~nt~zntiitn Parry 1977 : November-December Arctostapl~ylost~evnrletrsis Gray 1977 : October-December Arctostapl~ylosn~nt~tt~~rlnrin 1977 : November Arctostnpl~ylospatrrln Greene 1977: October-December: 1978: March Arctostnpl~yloslrva-rrrsi (L.) Spring var, conctilis Fern. & Macbr. 1977: October Arctostnpl~ylosviscido Parry 1977: December; 1978: January Cnssiope tt~ertetuintin(Bong.) D. Don. 1977 : October Garrltherin ovntifolin Gray 1977: October Gnrrltl~erin shallot^ Pursh. 1977: October-November; 1978: January-March Kalttlia polifolia Want. var. ~tlicropl~ylln(Hook.) Rehd. 1977 : September-October Ledlrtt~glandrrlosrrtt~ Nutt. var. cnlifortiicn (Kell.) C. L. Hitchc. 1977: September Lerlrrtt~glnt~rlrrlos~rtti Nutt . ssp. colrrttrbiatilr~~l(Piper) C. L. Hitchc. 1977: November Lelrcothoe davisiae Torr. 1977 : September-October Pl~yllorloceertlpetrifonjlis (Sm.) D. Don. 1977 : September-October Rllododet~drotitt~acropllyll~rt~l D. Don. 1978: January-February Rl~orlorlet~drot~occirletltale (T. & G.) Gray 1977: October Vnccitlilrtjl nrbrrsclrln (Gray) Merriam 1977: September-October Vnccitlirrtjl nletjlbrntlcerrtt~Dougl. 1977: September Vnccitlilrtjr occirlentale Gray 1977; October Vaccinirrtj~ovntlrtjl Pursh. 1977: October-November ; 1978: January-March

For personal use only. Vnccitlilrnlpnrvifolirrnl Sm. in Rees. 1977: October; 1978: January Vnccitlilrttl sropnrilrtjl Leib. 1977: September; 1978: January-February Pyrolaceae Cllitjlaplriln t~letlziesii(R. Br. ex D. Don.) 1977: October; 1978: March Cllitjlnphila lrtjlbellntn (L.) Barton vat. occirletltale (Rydb.) Blake 1977: October; 1978 : February-March Pyrola pictn Sm. f. pictn 1977: October-November; 1978 : March Pyroln pictn Sm. f. npl~ylln(Sni.) Camp. 1977: October-December Pyroln secrrtldo L. 1977: October-December Excluded from this study Ericaceae Arctostapl~yloscit~erea Howell A. elegntls Jeps. A. pnrvifolin Howell Can. J. Bot. Downloaded from www.nrcresearchpress.com by USDANALBF on 07/22/16 A. statldfordiata Parry Menziesin ferrrrgitlen Sm. Pyrolaceae Motleses rrtli'orn (L.) Gray vat. reticrrlntn (Nutt.) Blake Pyrola nsarifolin Michx. vat. bracteata (Hook.) Jeps. P. asarifolin var. plrrprrrea (Bunge) Ferm.

excavated intact, carefully wrapped in damp paper, and en- roots were preserved in a solution of Craf 111 and retained for closed in watertight containers. Specimens were taken to the reference. laboratory within 2 days after collection, and the soil was gently Each mycorrhiza was classified into one of three general washed from the roots. Several rootlets from each sample were categories. Ectomycorrhizae were defined as having a fungal hand sectioned with a razor blade, the sections mounted in mantle and Hartig net but no intracellular penetration by the Amman's solution, and examined microscopically. Mycorrhizal fungal symbiont; arbutoid, if fungal mantle, Hartig net, and 2276 CAN. J. BOT. VOL. 58. 1980

intl.acellular penetration by the fungal symboint were all pres- TABLE2. Previously reported mycorrhizae of ericaceous and ent; ericoid. if septate hyphae were scattered to rare on the pyrolaceous plants (excluding Cc~rrococcrrti~-type) surface of the rootlet, a Hartig net was absent, and intl-acellular penetration by the fungus was present. If a fungal mantle was No. of obvious on the rootlet but a Hartig net was difficult to discern, or species Type of if the rootlet examined was heavily tanninized so that intracel- Genus cxanlined mycorrhiza Reference lular hyphae were difficult to observe, the mycorrhiza was categorized as ectotrophic-arbutoid. Ectotrophic mycorrhizae Arbutoid Dufrenroy (1964) were further divided into two subtypes, those formed by Rivett (1924) Zak Cer~oc.occ.rirrrgc~opliilrrrrr Fr. (= C. grtrrr[fbrtiic (Sow.) Ferd. & (1 974) Winge) whose black hyphae form a distinct, easily recognized Arbutoid Mentz (1909) mycorrhiza (Trappe 1964) and those Formed by other fungi. Ericoid in Christoph (1921) Because vesicular-arbuscular mycorrhizae have not been re- peat Friesleban (1933, ported for ericaceous plants (Table 2) and require time- 1934) consuming staining techniques, their determination was Peyronel (1930) excluded in the present study. Madej (1968) Root samples of 451 plants from 27 taxa in the Ericaceae and Mejstrik and Hadac 29 from 5 taxa in the Pyrolaceae were studied for the presence of (1975) the three types of ~nycorrhizae.Eight taxa in these families Ericoid Rayner (1915) present in northern California were not included because of their Friesleban (1936) rare occurrence. limited distribution, or difficulty in identifica- Nieuwdrop (1969) tion (Table I ). Reatl and Str~bley Results (1973) Of the 451 plants examined in the Ericaceae, 337 Pearson and Read possessed mycorrhizae, whereas only 8 of the 29 (1973n, 19736) Ericoid Khan (1972) plants in the Pyrolaceae were mycon-hizal. All Ericoid Councilnlan (1923) taxa, except Pyrolcr sc~c~rtzcicr,possessed one or Ericoid Friesleban (1936) more of the three types of mycorrhizae (Table 3). Stalder and Schulz (1957) Ericaceae Nieuwdrop (1969) The majority of the plants of Arh~rtustnc~nzic~sii Robins011 (1973) and of the 10 species of Arc.tostcrplry1o.r possessed Pearson and Read (19730, 19736) ectomycorrhizae (including CPtrococc~rrm)or at-- Ericoid McNabb (1961) butoid mycorrhizae. Khan (1972)

For personal use only. Cetzococcrrt~z-type ectomycorrhizae were ob- Ericoid Friesleban (1936) served in At.hrrt~rstnetz~iesii and in all species of Ericoid Friesleban (1936) Bain (1937) Arctostcipl~y1o.sstudied except A. glcrtzcirrloscr (with Ericoid Friesleban (1936) one individual studied) and A. r~uci-r~,:vi(six indi- Ericoid Friesleban (1936) viduals). These species commonly possessed more Ericoid Friesleban (1936) than one mycorrhizal type. Arctostapl~ylosu~:cr- Brook (1952) rrrsi has been recorded as a host to Cetzococcrrtn by Morrison (1957) McNabb (1961) Trappe (1964) and Zak (1973). Ericoid mycorrhizae Arbutoitl Christoph (1921) were observed in two species of Arc~tostcrplzylos,A. Luck (1940, 1941) tzel;acic~tzsis,and A. pcrt~rla. Khan (1972) Half or more of the plants were mycorrhizal in 10 Lihnell (1942) of the other taxa studied. Only one type of mycor- Ericoid Gordon (1937) Khan (1972) rhiza was observed on the two individuals studied

Can. J. Bot. Downloaded from www.nrcresearchpress.com by USDANALBF on 07/22/16 Ericoid Rayner (1915, of Cassiope tnertensianci (ericoid), Gcirrltheria Arbutoid 1929) ol;citifolia (ericoid), and Rlzociode~tzdrotz occidc.tz- in one Doak (1928) tale (arbutoid-ectomycorrhiza). In Vcrccinirrtn oc- Hasselbaum (1 931) Friesleban (1934) cicientczle two of the three plants were found to Bain (1937) possess mycon-hiza, both ericoid. Three of the Nieuwdrop (1969) plants had ericoid mycorrhizae in Ledr~tnglcitz- I'earson and Read cirrlosutn var. californiccz. Five of the plants formed (1 9730) mycorrhizae in RIzodocienciron rnczo-ophyllutn Stribley and Read (19740, 19746, (three ectomycorrhizal and two arbutoid-ectomy- 1975,1976) corrhizal), six in Kciltnirr polifolia (two ectomycor- rhizal and four ericoid), and seven in Ledirrn glrrn- cirrlosum var. colutnbirrnutn (six Cenococcurn-type LARGENT ET AL.

TABLE3. Types of mycorrhizae in ericaceous shrubs and pyrolaceous plants of northern California

No. of plants with No. of one or more ECT plants than one Total no. ------examined ~nycorrhiza observed Other Cen AR AR/ECT ER None

Arblrtrrs t~letrziesii 55 6 55 7 16 24 8 0 6 Arctostapl~yloscnt~escetls 13 I 13 -1 5 -1 4 0 I Arctostapl~yloscohrtrlbiotro 47 4 5 1 5 5 34 7 0 0 Arctostaplrylos glatrrlrrloso I 0 I 0 0 0 I 0 0 Arctostapl~ylositrtricntn 2 1 3 24 6 6 I I 1 0 0 Arctostapl~ylostrrntlznr~itn 18 -1 2 1 4 4 6 7 0 0 Arctostaplrylos nruncirletrsi.~ 44 -1 45 5 7 16 16 I 1 Arctostnplrylos rrirtrrrrrrrlorio 1 0 I I 0 0 0 0 0 Al~ctostoplgvlospntlrlo 52 13 66 12 8 30 13 3 2 Arctostaplrylos rruo-lrrsi 6 0 6 1 0 4 I 0 0 Arctostophylos viscirlo 10 2 I I I 3 4 3 0 I Cossiope rrlertensiatro 2 0 1 0 0 0 0 I 0 Goriltlrerio ouotijolirr 2 0 I 0 0 0 0 I I Gorrltherio shollorr 29 0 I I 2 I 1 -1 5 18 Kalt~riopolijblirr 9 0 6 2 0 0 0 4 3 Lecllrrrl glorrrlr~losirtrr var. calijbrrziccc 5 0 3 0 0 0 0 3 0 Ledrirrr glarrcl~rlosr~rrr ssp. glor~drrlosrirrr 8 I 7 0 6 0 0 I 2 Lelicothoe rlovisioe 2 1 0 15 0 6 3 0 6 6 Plryllocloce errlpetrVorrrris 14 0 4 0 0 0 0 4 10 Rhodoclerlclrorr rrrocroplryll~irrr 6 0 5 2 I 0 2 0 1 Rhorlocletrclron occirlet~tole 2 0 I 0 0 0 1 0 0 Vaccbli~irrlorb~iscrilrr 17 0 8 1 0 0 0 6 9 Voccinirirrr rrrerrrbrorlcerirrr 4 0 -1 0 0 0 0 2 2 .Voccinbitrr occirl~r~tr~l~ 3 0 -7 0 0 0 0 2 I Voccit~irirrro~.otriirr 37 0 I6 0 8 I 3 4 21 Vaccitririrrr poruijoliriirr 8 0 -1 I 0 0 0 1 6 Vaccitririrrr scopot.irirrr 17 0 3 0 1 0 I 0 14 For personal use only. Clritrrophilo rrrerriiesii -7 0 2 0 0 1 I 0 0 Clritrroplrilri ritrrbellotr~ 15 0 3 2 0 0 0 I 12 Pyrolo picta f. pictri 8 0 2 0 0 1 0 1 6 Pyrolo picto f. ri~~lryllrr I 0 L 0 0 0 0 1 0 Pyrola sec~irrrla 3 0 0 0 0 0 0 0 3

NOTE:ECT, ectoniycorrhizae; AR, ;~rbutoid;ARIECT, arbuloid or ectornycorrhizae; ER, ericoid; Cen. Cetrococcrml geophilrr,n.

and one ericoid). In Le~rcothoeclauisiae, 15 of 21 of the Cenococcurn-type and one was ectomy- plants had mycorrhizae of all three types. corrhiza-arbutoid. In four of the other taxa studied, 26-41% of the plants were mycorrhizal. In Vc~ccirziurnarbusculm, Pyrolaceae 8 of 17 plants had mycorrhizae (6 ericoid and 2 Five taxa in the Pyrolaceae were examined; four Can. J. Bot. Downloaded from www.nrcresearchpress.com by USDANALBF on 07/22/16 ectomycorrhizal). In Gaultheric~shnllorz, 11 of 29 possessed at least one of the three types of mycor- plants were found to have mycorrhizae, whereas in rhizae. In Chirnuphiln rnerzziesii and Pyroln pictn f. Vc~ccinilrrn oumtunz, 16 of 37 plants possessed aphylla, all plants studied were mycorrhizal. In mycorrhizae. In each of these species, all three Pyrolc~picta and Clzinzc~philaurnbellc~tn, very few types of mycorrhizae were observed. In Plzyl- of the plants possessed mycorrhizae. locloce ernpetriforr?zis, 4 of the 14 plants possessed ericoid mycorrhizae. Discussion and conclusion Only 2 of 8 plants in Vc~cciniurnparuifoliurn and 3 Excluding Gu~lltherin and Rhoclodentlron of 17 plants in V. scopcpcrrium possessed the types of species, it appears that all of the larger ericaceous mycorrhizae studied. In the former species, one shrubs or trees in northern California, i.e., Arb~lt~ls mycorrhiza was ericoid and one ectotrophic, rnenziesii and Arctostnphylos spp., possess either whereas in the latter species two mycorrhizae were ectomycorrhizae or arbutoid mycorrhizae. Except 2278 CAN. J. BOT. VOL. 58. 1980

for Arctostaphylos glarzclulosa, all species of BROOK,P. J. 1952. Mycorrhiza of Pc,rtlcd/yn tncrcros/igtno. New Arctostaphylos and Arbutus were found to form Phytol. 51: 388-397. CHRISTOPH,H. 1921. Untersuchungen uber die mykotrophen more than one type of mycorrhiza in certain as yet Verhaltnisse der "Ericales" und die Keimung von Pirola- undefined ecological situations. ceen. Beih. Bot. Centrabl. 38: 115-157. The ericaceous and pyrolaceous plants in the COUNCILMAN,W. T. 1923. The root system of Epigcrc~clrc>pcJt~s genera Cassiope, Kalmia, Ledum, Leucothoe, and its relation to the fungi of the humus. Proc. Natl. Acad. Plzyllodoce, Vclccinilrrn, Chitnaphila, and Pyrola, Sci., U.S.A. 9: 279-285. DOAK,K. D. 1928. The rnycorrhizal fungus of Vnccitliirtn. as well as the genera containing shrubby plants, Phytopathology, 18: 148. Gaultheria and Rhododendron appear to be DUFRENROY,J. 1964. The endophytis mycorrhiza of Ericaceae. mycorrhizal. The type of mycorrhiza and its abun- New Phytol. 16: 222-228. dance appears to depend on unknown ecological FRIESLEBAN,R. 1933. ~berexperirnentelle mycorrhizabildung bei Ericaceen. Ber. Dtsch. Bot. Ges. 51: 351-357. factors. Even though many of these taxa possessed 1934. Zur Frage der Mykotrophie in der Gattung Vcic- neither ectomycorrhizae, arbutoid, nor ericoid citlirrtn L. Jahrb. Wiss. Bot. 80: 421-456. mycorrhizae, they may form vesicular-arbuscular 1936. Weitere untersuchungen uber die rnykotrophie der mycorrhizae. Consequently, these species need Ericaceen. Jahrb. Wiss. Bot. 82: 413-459. further study before any conclusion can be made GORDON,H. D. 1937. Mycorrhiza in Rl~ododetlclrot~.Ann. Bot. (London), 1: 593-6 13. about their type of mycorrhizal association. HASSELBAUM,G. 1931. Cytologische und physiologische Stu- Previous reports indicate that ericaceous shrubs dien in ericoiden endotrophen Mycorrhiza von Etnpe/rrrtn or subshrubs in Arbutus, Arctostaphylos, and tligrrrttl. Bot. Arch. 31: 386-440. Pyrola possess arbutoid mycorrhizae, and those in KHAN,A. G. 1972. Mycorrhizae in the Pakistan Ericales. Pak. J. Bot. 4(2): 183-194. Gaultheria, Kcllrnia, Ledum, Rhodoclendron, and LIHNELL,D. 1942. Keimungsversuche rnit Pyrolasarnen. Symb. Vucciniurn are ericoid (Table 2). Two exceptions to Bot. Ups. 6(3): 1-37. this generality exist, a report of an arbutoid mycor- LUCK.R. 1940. Zur biologie der heirnischen Pirolonr/etl. Schr. rhiza in Vuccirziurn and an ericoid mycorrhiza in Konigl. Phys.-Okon. Ges. Konigsberg, 71: 300-334. Arctostaphylos. Our study reveals that ericoid 1941. Zur. Keimung der heimischen Pirolocrr/rtl. Flora (Jena), 135: 1-5. mycorrhizae do occur in some species of Arcto- MCNABB,R. F. R. 1961. Mycorrhiza in the New Zealand staphylos but that they are rare. Ericales. Aust. J. Bot. 9: 57-61. Previously unreported arbutoid mycorrhizae MADEJ,T. 1968. Studium nad rnikotrofizrnen wrzosowatych occur in Gaulthericl slznllon as well as in Vc~cciniurn (Ericaceae) w. Polsce. Folia For. Pol. Ser. A, 14: 189-238. oljat~rrnand may occur in Rhododendron mac- MEJSTRIK,V., and E. HADAC.1975. Mycorrhizas of Arctostel- phylos rrticr-rrrsi. Pedobiologia, 15: 336-342. For personal use only. roplzyllutn, R. occicientale, and Vaccitzium sco- MENTZ,A. 1909. Studier over danske Hedeplantes Okologie (11. parhm. Arctostnphylos-Typen). Bot. Tidsskr. 29: 260-290. Ectomycorrhizae (excluding the Cetzococcum- MORRISON,T. M. 1957. Host-endophyte relationships in mycor- type) have rarely been reported from ericaceous rhizas of Pernettycr tncrcrostigtnn. New Phytol. 56: 247-257. MUNZ,P. A,, and D. D. KECK.1968. A California Flora. Uni- shrubs or subshrubs, but in northern California versity of California Press, Berkeley and Los Angeles. they were found in Arbutus rnenziesii, all 10 spe- NIEUWDROP,P. J. 1969. Some investigations on the mycorrhiza cies of Arctostaplzylos, and in Gaulthericl shallorz, of Cnllrrtlcr, Ericu and Vcrccitlirrtn. Acta Bot. Neerl. 18(1): Kulrnia polifolia, Rhododendron macrophyllurn, 180- 196. PEARSON,V.. and D. J. READ.19730. The biology of rnycorrhiza Vc~ccirziurn arbusculcl, and V. paruifolium. in the Ericaceae, I. The isolation of the endophyte and syn- Cenococcum-type ectomycorrhizae have been re- thesis of mycorrhizas in aseptic culture. New Phytol. 72: ported from Arbutus rnenziesii (Trappe 1964) and 371-379. Arctostaphylos uua-ursi (Zak 1976). In northern 19736. The biology of mycorrhiza in the Ericaceae, 11. The transport of carbon and phosphorus by the endophyte. . Can. J. Bot. Downloaded from www.nrcresearchpress.com by USDANALBF on 07/22/16 California they form on all species of Arctostaphy- and the rnicorrhiza. New ~h~iol.72: 1325-1331. 10s (except A. glarzdulosa in which only one plant PEYRONEL,B. 1930. Simbiosi rnycorrhica tra piante e was studied), as well as on Gaultheria shallon, Basidiomiceti. Nuovo G. Bot. Ital. 37: 655-663. Ledurn gland~rlosurn ssp. columbianur?~,Leu- RAYNER,M. C. 1915. Obligate symbiosis in Colllrtzcr tirrlguris. cothoe dauisiae, Rhododendron macrophyllurn, Ann. Bot. (London), 29: 970135. 1929. Biology of fungus infection in the genus Vuc- Vacciniurn ouatifolia, and V.scoparium. cit~ilrtn.Ann. Bot. (London), 43: 55-70. RIVETT,M. 1924. The root tubercles in Arbrrtrrs rrtz'do. Ann. BAIN,H. F. 1937. Production of synthetic mycorrhiza in the Bot. (London), 38: 361-367. cultivated cranberry. J. Agric. Res. (Washington, D.C.), 55: READ,D. J., and D. P. STRIBLEY.1973. Effect of rnycorrhizal 81 1-837. infection on nitrogen and phosphorus nutrition of ericaceous BARKER,L. M. 1976. A vascular plant inventory and vegetation plants. Nature (London) New Biol. 244: 81-82. map of the Lanphere-Christensen dunes. M.S. thesis, Hum- ROBINSON,R. K. 1973. Mycorrhiza in certain Ericaceae native boldt State University, Arcata, CA. to southern Africa. J.S. Afr. Bot. 39: 123-129. LARGENT ET AL. 2279

SAWYER,J. O., and D. THORNBURGH.1977. Montane and sub- ous mycorrhizas. 111 Endomycorrhizas. Eciirrci by F. E. Saun- alpine vegetation of the Klamath Mountains. It1 Terrestrial ders, B. Mossee, and P. B. Tinker. Academic Press, London. vegetation of California. Eciireci by M. G. Barbour and J. pp. 198-208. Major. John Wiley & Sons, Inc. pp. 700-732. 1976. The biology of mycorrhiza in the Ericaceae VI. SAWYER,J. O., D. THORNBURG,and J. R. GRIFFIN.1977. The effects of mycorl.hizal infection and concentration of Mixed evergreen forest. Iti Terrestrial vegetation of Califor- ammonium nitrogenon growthof cranberry (Vr~ccirrilorrlt~erc- nia. Eciirrci by M. G. Barbour and J. Major. John Wiley & rocrrrpoti Ait.) in sand culture. New Phytol. 77: 63-72. Sons, Inc. pp. 360-381. TRAPPE,J. M. 1964. Mycol-rhizal hosts and distribution of ~T'ALDER,L., and F. SCHULTZ.1957. Untersuchungen iiber die C'II~C~CCIIIIIgrrlti$orttze. Lloydia, 27: 100- 106. kausalen Zusammenhange des Erikawurzelsterbens. ZAK,B. 1973. Classification of ectomycorrhizae. Itr Ectomycor- Phytopathol. Z. 30: 1 17- 148. rhizae, their ecology and physiology. Edireci by G. C. Marks ~T'RIBLEY,D. P., and D.J. READ.19740. The biology of mycor- and T. Kozlowski. Academic Press, New York, NY. pp. rhiza in the Ericaceae Ill: movement of CIJ from host to 43-78. fungus. New Phytol. 73: 731-741. 1974. Ectendomycol-rhiza of Pacific madrone (Arbrltlrs 19746. The biology o€the mycorrhiza in the Ericaceae r?reriiiesii).Trans. Br. Mycol. Soc. 62: 201-204. IV. The effect of mycorrhizal infection of uptake of I5N from 19760. Pure culture synthesis of bearberry mycorrhizae. labelled soil by Vclccitiilrtn tnclcrocrrtpoti ait. New Phytol. 73: Can. J. Bot. 54: 1297-1305. 1149- 1155. 19766. Pure culture synthesis of Pacific rnadrone ecten- 1975. Some nitritional aspects of the biology of ericace- domycorrhizae. Mycologia, 68: 362-369. For personal use only. Can. J. Bot. Downloaded from www.nrcresearchpress.com by USDANALBF on 07/22/16