416 R ichard K. Be11jami11 ct al. most autho ritative source, and few species have been lul ar ycastlike fo rms (Fig. 18.10 [ ')'n-tbiotaphrina and described since that work was completed. Couch undescribed taxa]) tl1 at inhabit speciali zed host ceU recorded the largest number of species (36) fr·o m the and coelo mic cavities, and the basidiomycetes and United tares, altho ug h these fungi probably arc pre­ ascomycetes associated with siricid wood wasps, ants do minantly tropical. Coll ectors in tropical regio ns likely and termite (Table 18.3). wi ll discover a large number of new taxa, a point Couch (1938:50) recogni zed when he stated that " no discus­ sion of geographic distribution will be of much va lu e." BARK BEETLES AND FUNGI Otl1er useful reference to Septobasidialcs arc those of Couch (1935) and Azema (1975 ). Fungi arc often associated with beetles that inhabit bark and wood of li ving or recently dead trees. Tho e TECHNIQUES FOR SAMPLING FUNGI fun gi fa ll into two categories. One category encompasse INVOLVED IN GARDENING SYMBIOSES TABLE 18.3 Fungi Involved in Gardening Symbioses with Artlu-opods Mutualistic associations between insects and the fu ngi on whj ch tl1 ey feed o r fro m which they acquire enzymes for Ascomycota digesti o n often are referred to as gardening symbio es accharomycctcs (M. M . Martin 1987). Not all of the fungi in these asso­ Saccharomvcctalcs (Ascoidcn, Dipodnscus, Picbin, Cn11dida ) Pyrcno mycctcs ciations arc o bligate members of such symbioses; ratl1er Hypocrcalcs (undescribed ycastlikc forms associated with there is a continuum of associatio ns ranging fr·om those planthoppcrs) in which tl1e fung us is o nl y dispersed by the insect to Xvlarialcs those tl1at are true gardening associatio ns. Some of the X yla ri accac ( Xylnrin) Microascalcs associations are of intcrc t because they may provide Ccratocystiaccac ( Ccmtocystis; Chnlnrn; Ambrosiclln, in parr) systems for evolutio nary studies of a spectrum of inter­ Ophiostomatalcs actions. In o tl1cr cases tl1c interactions are of econo mic Ophiosromataccac ( Ophiostomn; Lcptogrnpbium; Ambrosiel/n, importance because they involve dispersa l of se ri o us in part; SporotbrL\~ Rnffnclcn) fungal patl1ogens o r sapstain fungi tl1at damage trees, Loculoascomycctcs- Di scom~ ' Cctcs Unknown afli nitcs-Symbiotnpbrinn crop plants, and forest products. Some of the fungi rely 13asid iomycota o n the insect fo r surviva l because they arc poor com­ 1-1y mcno mycctcs petitors with apro bcs in tl1cir habitats. The fungi that Aphyllophoralcs fo rm associati o ns include ascomycetes (yeasts, Ophios­ Corticiaccac ( E11tomocorticium and others) toma [Figs. 18.8 and 18.9], eratocystis and related Agaricalcs conidial forms, and aphyll o pho ralean basidio mycetes) Lcpiotaccac ( Cblorophyllmu, Lcucongm·icus, Tcnuitomyccs, and undescri bed forms) that are symbio nts of va ri o us g ro ups of beetl es, in trace!- FIGURE 18.8 Ascosporcs oozing from the necr of an Ophiostomn species pcrithccium. (Ph oto by Kicr Klcpzig, DA Forest Service) - ..... r ..... ·----·- /meet- n11d Otbcr Artbropod-Associntcd Fuugi 41 7 FIGURE 18.9 Resinous lesions on the bark of a pine tree caused by mass inoculation with OpiJiostOIIUI­ miuus, a fungal associate of the southern pine beetle. (Photo by Erich Vallery, USDA Forest Service) species that commonly occur with phloem-feeding methods we descri be are applicable ro colonizers of hard­ beetles, usuall y in li ving trees (gro uped here as bark woods as well. N umerous fungi occupy almost all parts beetles). The other category incl udes species associated of the body surface and gut of a beetle, as well as tl1e with beetles tl1 at require fungi as a primary nutri ent tree tissue the beetle infests. Among the fungi found on reso urce in all life hi srory stages (ambrosia beetles). T he the beetl e surface and within the di gestive tract arc yeasts distinction is artificial, and the fungi often arc cl osely (Call aham and Shi fri nc 1960; Bridges et al. 1984; re lated. H owever, because techniq ues used to study the Leufvc n and Nehls 1986), various saprobcs (Bridges et phloem-feeding and ambrosial associatio ns diffe r some­ al. 1984), and ophiostomaroid fungi (sec "Identifica­ what, we discuss them separately (see "Am brosia Beetles tion," later in this chapter), especially in Ophiosto matales and Fungi" later in this chapter). We in cl ude o ur dis­ (Upadhyay 1993). Species of Ophiostoma and related cussion of phloem-feeding weevil s (Curculi o ni dae) with coni dial fungi associated with beetles include many of the bark beetles. the stain fungi known to disco lor wood (Fig. 18.11 ) Bark beetles colo ni ze both hardwood and conifer (HarringtOn 1988 and references tl1erein ). Beetle­ trees, and although we will emphasize those that colo­ associated ophiostomatalean fungi also have been impli­ nize conifers and their fungal associates, many of the cated as conifer pathogens (Harringto n and Cobb 1988; 418 Richm·d K Bc11jami11 et al. FIGURE 18.10 Yeastlike symbiotes gathered at the epitherial plug (the junction of the ova ri ole and pedicel ) of a planrhopper. The symbiotes of pianthoppers are transmi tted to the next generation through the ovary, entering the terminal oocyte in the ovarioles posterio rl y. The symbiotes move fi·om the insect fat body to the epitherial plug when the ovary matures . FIGURE 18.11 ross-section of a red pine infected wi tl1 blue-s tain fungi. (Photo by Kier Klcp zig, USDA Forest Service) Harrington 1993), and certain members of this gro up Certain beetles of tl1e curculio nid subfamilies colyti­ are capable of killing trees (Brasier 1988; Harrington nae and Pl atypodinae have evolved specialized structure 1993; ol heim et al. 1993). More often, however, they kn own as myca ngia, the purpose of which appear to be are a sociated with resi nous lesio ns that may ca use the the storage, culture, and transport of fungi ( mycangia occlusion of sapwood (Harrington 1993). Some of these occur also in ambrosia beetles). The mycangia of a few fu ngi also are antagoni sts of beetles, reducing reproduc­ bark-beetle species are complex and include secretory tive succes and larval development (Barras 1970). cell s (Harrington 1993). More commonly, beetle mycan­ Altl1ough tl1e exact ecological ro les played by the va ri ous gia are less developed , simple pits in tl1 e exo keleton of ophi ostomatoid fungi have ye t to be determined, they the head, pro notum, or elytra . These imple structures are undo ubtedly closely associated witl1 bark beetles and may contain yeasts , ophiostomatalean fungi, and otl1er weevils and their tree hosts. Efforts to examine tl1 e diver- fungi, includin g corticio id basidiomycetes (Harrington ity of beetle-associated microorganisms center aro und 1993; Lewinsohn et al. 1994). M yca ngial fungi are tl1 ese fungi. tho ught to be mutuali sts of tl1 eir beetle hosts, pas ibl y -----'='--=-----· --- - - !IIScct· nud Other Artbropod·Associntcd Fungi 419 by receiving nutrients fro m the host (Bridges 19 83; where it is left fo r sevcr3l days. The host material is Bridges and Perry 1985; Gold hammer ct al. 1990). checked dail y fo r insects moving from the soil onto the Often fungi have a yeastlike morpho logy whil e they are stem-secti on surface . In addition, some root weevils may in a mycangium, rather than the hypha! fo rm o utside the be coll ected fro m the lower stem as they ascend at night mycangium and in the environment of the wood . T he to feed o n br3nches (Kicpzig ct al. 1991). Walking raxonomy and ecology of many of these fungi arc not weevil s are fo rced in to a coll ection jar atop a screen fully known (lvloser ct al. 1995 ). funnel that is wrapped around the main stem. Bark beetles th3t attack the lower stem of trees can be coll ected in va ri o us types of flight tr3ps. A lower-stem Coll ection fli ght trap consistin g of an inverted, plastic jug modified Bark-beetle fungi can be found in or o n insects, other by having a coll ection jar 3ttached can be baited with cl1an tl1e beetles that they colo ni ze. True hosts of these turpentine and ethanol and used to collect turpentine fungi are found in only a few coleopteran fa mi li es, beetl es 3nd some root insects (Klcpzig et al. 1991 ). Tur­ including the Curculionidae, especiall y in the subfamilies pentine beetl es also can be c3pturcd in bounce traps in colytinac and Plarypodinae (Harrington 1988; Mall och whi ch the fl ying beetl e strikes a black pipe b3ited with and Blackwell 19933). Kn owledge of the host insect's ethano l and turpentine, 3nd fa ll s into a water-fi lled pool biology facilitates effective coll ection of specimens for below, fro m whi ch it is collected (Fatzinger 1985; isolation of fungi. These insects colonize tl1e lateral Phillips et al. 1988). Lindgren multiple-funnel traps roots, the root collar, the main stem , the br3nches, (Lindgren 1983) can be hung nc3r the ground for developing shoots, and even fi·uits of 3 va ri ety of trees coll ection of lower flower-stem insects fl ying tow3rd (S. L. \Vood 1982; Drooz 1985 ); tl1e best-studied attract3nts (Phillips et al. 1988). insect-fungal complexes are fou nd in coni fe rs. M3ny Most of tl1 e aggressive, tree-killing bark beetles attack bark beetles and weevils use tree- and insect-produced the central and upper portions of the stem (S.