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High Root Concentration and Uneven Ectomycorrhizal Diversity Near Sarcodes Sanguinea ( Ericaceae): a Cheater That Stimulates Its Victims? Author(S): Martin I

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High Root Concentration and Uneven Ectomycorrhizal Diversity Near Sarcodes Sanguinea ( Ericaceae): a Cheater That Stimulates Its Victims? Author(S): Martin I High Root Concentration and Uneven Ectomycorrhizal Diversity Near Sarcodes sanguinea ( Ericaceae): A Cheater That Stimulates Its Victims? Author(s): Martin I. Bidartondo, Annette M. Kretzer, Elizabeth M. Pine and Thomas D. Bruns Source: American Journal of Botany, Vol. 87, No. 12 (Dec., 2000), pp. 1783-1788 Published by: Botanical Society of America, Inc. Stable URL: http://www.jstor.org/stable/2656829 Accessed: 29-02-2016 09:39 UTC Your use of the JSTOR archive indicates your acceptance of the Terms & Conditions of Use, available at http://www.jstor.org/page/ info/about/policies/terms.jsp JSTOR is a not-for-profit service that helps scholars, researchers, and students discover, use, and build upon a wide range of content in a trusted digital archive. We use information technology and tools to increase productivity and facilitate new forms of scholarship. For more information about JSTOR, please contact [email protected]. Botanical Society of America, Inc. is collaborating with JSTOR to digitize, preserve and extend access to American Journal of Botany. http://www.jstor.org This content downloaded from 132.174.255.116 on Mon, 29 Feb 2016 09:39:26 UTC All use subject to JSTOR Terms and Conditions American Journal of Botany 87(12): 1783-1788. 2000. HIGH ROOT CONCENTRATION AND UNEVEN ECTOMYCORRHIZAL DIVERSITY NEAR SARCODES SANGUINEA (ERICACEAE): A CHEATER THAT STIMULATES ITS VICTIMS?1 MARTIN I. BIDARTONDO,2 ANNETTE M. KRETZER,3 ELIZABETH M. PINE, AND THOMAS D. BRUNS 111 Koshland Hall, College of Natural Resources, University of California at Berkeley, Berkeley, California 94720-3102, USA Sarcodes sanguinea is a nonphotosynthetic mycoheterotrophic plant that obtains all of its fixed carbon from neighboring trees through a shared ectomycorrhizal fungus. We studied the spatial structuring of this tripartite symbiosis in a forest where Sarcodes is abundant, and its only fungal and photosynthetic plant associates are Rhizopogon ellenae and Abies magnifica, respectively. We found disproportionately high concentrations of Abies roots adjacent to Sarcodes roots compared to the surrounding soil. Rhizopogon ellenae colonizes the vast majority of those Abies roots (86-98%), and its abundance tends to decrease with increasing distance from Sarcodes plants. At 500 cm from Sarcodes plants we did not detect R. ellenae, and the ectomycorrhizal community instead was dominated by members of the Russulaceae and Thelephoraceae, which are commonly dominant in other California pinaceous forests. The highly clumped distribution of Abies-R. ellenae ectomycorrhizas indicates that Sarcodes plants either establish within pre-existing clumps, or they stimulate clump formation. Several lines of evidence favor the latter interpretation, suggesting an unexpected mutualistic aspect to the symbiosis. However, the mechanism involved remains unknown. Key words: Abies magnifica; community structure; mutualism; mycoheterotrophy; parasitism; Rhizopogon ellenae; tripartite sym- biosis. The snow plant, Sarcodes sanguinea Torrey (Ericaceae), is for overcoming competitive exclusion. It appears that by per- the largest (up to several kilograms fresh mass) member of the manently reversing carbon flow in their favor, nonphotosyn- nonphotosynthetic subfamily Monotropoideae. The genus Sar- thetic epiparasites have evolved to one extreme along a con- codes is monotypic and restricted to the mountains of the Si- tinuum of plant strategies for carbon acquisition. erra San Pedro Mdrtir of Baja California, the southern ranges Extreme host specialization appears to be a general pattern and Sierra Nevada of California, and the southern ranges of among nonphotosynthetic epiparasites; this contrasts with pho- Oregon (Wallace, 1975). Like all other monotropes, the snow tosynthetic plants, which typically form mycorrhizas with phy- plant is a mycoheterotroph: a nonphotosynthetic plant that ob- logenetically diverse fungi. Recent studies have shown that tains its fixed carbon from fungi. This is a successful lifestyle some epiparasitic orchids (Taylor and Bruns, 1997) and mon- as evidenced by over 400 known species in 87 genera, notably otropes (Cullings, Szaro, and Bruns, 1996; C. K. Lefevre, and in the families Ericaceae and Orchidaceae (Leake, 1994). R. Molina, personal communication, Oregon State University) Many mycoheterotrophs examined to date are linked to sur- specialize on highly restricted sets of closely related ECM fun- rounding trees via a shared ectomycorrhizal (ECM) fungus gal hosts. In fact, the only exception to this pattern of spe- (Furman and Trappe, 1971; Vreeland, Kleiner, and Vreeland, cialization was the snow plant, which appeared to be a gen- 1981; Cullings, Szaro, and Bruns, 1996; Taylor and Bruns, eralist (Cullings, Szaro, and Bruns, 1996). However, we have 1997). This interaction is called "epiparasitism" because the recently determined that the snow plant is specialized over a mycoheterotroph indirectly parasitizes the trees (Bjorkman, large area of the Sierra Nevada of California on the ECM 1960), thus cheating the ECM mutualism. Furthermore, some fungus Rhizopogon ellenae A. H. Smith (Bidartondo, Kretzer, ECM photosynthetic angiosperms are now known to engage and Bruns, 1998), a member of the suilloid lineage of the in facultative epiparasitism. Simard et al. (1997a, b) demon- Boletales (Bruns et al., 1998). Over its entire range, the snow strated that in nature carbon can be derived from the better plant may actually form a "geographic mosaic of specializa- competitor tree species by a poorer one if both are colonized tion" (Thompson, 1994). by common ECM fungi, thereby providing a novel mechanism Although we follow Bjorkman (1960) in referring to the monotropes as epiparasites, a net cost to either the photosyn- I Manuscript received 15 June 1999; revision accepted 7 September 1999. thetic plant or the fungal associate remains to be shown The authors thank Timothy Szaro for computer and laboratory assistance, (Leake, 1994). Epiparasitism is consistent with (a) the hetero- Remi Cohen and Dirk Redecker for field assistance, and Dan Luoma and trophic habit of the monotropes; (b) the fact that extreme spe- Peter Price for comments on the manuscript. A USDA competitive grant from cialization is a common characteristic of parasitic systems the Forest Biology Program and a cooperative agreement with the Southwest Forest Experiment Station helped support this research, as well as grants from (Price, 1980; Thompson, 1994); and (c) evidence for flow of the East Bay Chapter of the California Native Plant Society, the Berkeley 14C-labeled glucose from trees to Monotropa hypopitys L. (Er- Chapter of the Sigma Xi Society, the Mycological Society of San Francisco, icaceae), a close relative of Sarcodes (Bjorkman, 1960). How- and the Monsen Foundation to M. I. B. ever, Bjorkman also found that the growth of a fungus isolated 2 Author for correspondence (e-mail: [email protected]). from Monotropa mycorrhizas was greatly stimulated by an 3Current address: 2082 Cordley Hall, Department of Botany and Plant Pa- thology, Oregon State University, Corvallis, Oregon 97331-2902 USA. extract of the plant. Miller and Allen (1992) speculate that 1783 This content downloaded from 132.174.255.116 on Mon, 29 Feb 2016 09:39:26 UTC All use subject to JSTOR Terms and Conditions 1784 AMERICAN JOURNAL OF BOTANY [Vol. 87 potential ecophysiological benefits for trees of supplying car- gested and dense mass of brittle, succulent, highly branched monotropoid mycorrhizal roots from which adventitious inflorescence axes emerge (Wal- bon to Monotropa may render the association mutualistic. Re- lace, 1975). In one case, we were unable to find the rootball in the soil after search on monotrope symbioses has focused on the mycohet- the inflorescence axis accidentally broke off. All soil cores and rootballs were erotrophic plant's nutrition (Bj6rkman, 1960), mycorrhizal ul- kept at 4?C and processed within 3 wk of field sampling. trastructure (Duddridge and Read, 1982; Robertson and Rob- We sprayed each soil core vigorously with tap water over 2 mm and 500- ertson, 1982), germination (Francke, 1934; S. McKendrick, p,m mesh stacked sieves to separate coarse and fine soil fractions. The Sar- personal communication, University of Sheffield), flowering codes rootballs were manually broken into small pieces and otherwise treated (D. Luoma, personal communication, Oregon State Universi- in the same manner. All the washed soil and roots collected in both sieves ty), and associated fungi (Cullings, Szaro, and Bruns, 1996). were spread thinly in petri dishes and examined using stereo microscopes. All However, little is known about basic ecological traits of mon- Abies roots were collected from each individual core or rootball and sorted otropes, and this is partly responsible for our difficulties in into morphotypes according to gross mantle characters (color, color changes, understanding the nature of their interactions. branching pattern, presence of rhizomorphs, mantle surface, thickness). We In this study, we investigated the ECM community of a red discarded degraded roots and placed recognizable ECM roots that were par- fir, Abies magnifica Andr. Murray (Pinaceae), forest where the tially degraded and/or not turgid in separate morphotypes. We did not attempt snow plant flowers abundantly, and we asked what part R. to identify identical morphotypes among different cores based on morpholog- ellenae played in this community. Although one might expect ical characters alone, but instead relied
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