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Transport of Fungal Symbionts by Mountain Pine Beetles University of Montana ScholarWorks at University of Montana Ecosystem and Conservation Sciences Faculty Publications Ecosystem and Conservation Sciences 2009 Transport of Fungal Symbionts by Mountain Pine Beetles K. P. Bleiker S. E. Potter C. R. Lauzon Diana Six University of Montana - Missoula, [email protected] Follow this and additional works at: https://scholarworks.umt.edu/decs_pubs Part of the Ecology and Evolutionary Biology Commons Let us know how access to this document benefits ou.y Recommended Citation Bleiker, K. P.; Potter, S. E.; Lauzon, C. R.; and Six, Diana, "Transport of Fungal Symbionts by Mountain Pine Beetles" (2009). Ecosystem and Conservation Sciences Faculty Publications. 32. https://scholarworks.umt.edu/decs_pubs/32 This Article is brought to you for free and open access by the Ecosystem and Conservation Sciences at ScholarWorks at University of Montana. It has been accepted for inclusion in Ecosystem and Conservation Sciences Faculty Publications by an authorized administrator of ScholarWorks at University of Montana. For more information, please contact [email protected]. 503 Transport of fungal symbionts by mountain pine beetles K.P. Bleiker1,2 Department of Ecosystem and Conservation Sciences, University of Montana, Missoula, Montana 59812, United States of America S.E. Potter, C.R. Lauzon Department of Biological Sciences, California State University, Hayward, California 94542, United States of America D.L. Six Department of Ecosystem and Conservation Sciences, University of Montana, Missoula, Montana 59812, United States of America Abstract—The perpetuation of symbiotic associations between bark beetles (Coleoptera: Curculionidae: Scolytinae) and ophiostomatoid fungi requires the consistent transport of fungi by successive beetle generations to new host trees. We used scanning electron microscopy and culture methods to investigate fungal transport by the mountain pine beetle (MPB), Dendroctonus ponderosae Hopkins. MPB transports its two main fungal associates, Grosmannia clavigera (Robinson-Jeffrey and Davidson) Zipfel, de Beer and Wingfield and Ophiostoma montium (Rumbold) von Arx, in sac-like mycangia on the maxillary cardines as well as on the exoskeleton. Although spores of both species of fungi were observed on MPB exoskeletons, often in pits, O. montium spores were generally more abundant than G. clavigera spores. However, a general scarcity of spores of either species on MPB exoskeletons compared with numbers on scolytines that lack sac-like mycangia indicates that fungal transport exteriorly on MPBs is incidental rather than adaptive. Conidia were the dominant spore type transported regardless of location or species; however, our results suggest that once acquired in mycangia, conidia may reproduce in a yeast-like form and even produce hypha-like strands and compact conidiophore-like structures. Fungi that propagate in mycangia may provide beetles with a continual source of inocula during the extended egg-laying period. Re´sume´—La perpe´tuation des associations symbiotiques entre les scolytes (Coleoptera: Curculionidae: Scolytinae) et les champignons ophiostomatoı¨des ne´cessite un transport continu des champignons par les ge´ne´rations successives de cole´opte`res vers de nouveaux arbres hoˆtes. Le microscope e´lectronique a` balayage et des me´thodes de culture nous ont servi a`e´tudier le transport des champignons chez le dendroctone du pin ponderosa (MPB), Dendroctonus ponderosae Hopkins. MPB transporte ses deux champignons associe´s principaux, Grosmannia clavigera (Robinson-Jeffrey et Davidson) Zipfel, de Beer et Wingfield et Ophiostoma montium (Rumbold) von Arx, dans des mycanges en forme de sacs sur les cardos des maxilles et sur l’exosquelette. Bien qu’on observe les spores des deux champignons sur l’exosquelette de MPB, souvent dans des fosses, les spores d’O. montium sont ge´ne´ralement plus abondantes que les spores de G. clavigera. Cependant, la rarete´ge´ne´rale des spores des deux espe`ces sur l’exosquelette de MPB par rapport a` l’exosquelette de scolytine´s qui n’ont pas de mycanges en forme de sacs indique que le transport externe de champignons sur MPB est accidentel plutoˆt qu’adaptatif. Quels que soit le site et l’espe`ce, les conidies sont le type dominant de spores transporte´es; cependant, nos observations indiquent qu’une fois entre´es dans les mycanges, les conidies peuvent se reproduire en une forme de levure et meˆme produire des filaments d’hyphes et des structures compactes semblables a` des conidiophores. Les champignons qui se reproduisent Received 12 March 2009. Accepted 22 June 2009. 1 Corresponding author (e-mail: [email protected]). 2 Present address: Canadian Forest Service, Natural Resources Canada, 506 West Burnside Road, Victoria, British Columbia, Canada V8Z 1M5. doi: 10.4039/n09-034 Can. Entomol. 141: 503–514 (2009) E 2009 Entomological Society of Canada 504 Can. Entomol. Vol. 141, 2009 dans les mycanges peuvent fournir aux cole´opte`res une source continue d’inoculum durant la longue pe´riode de ponte des œufs. [Traduit par la Re´daction] Introduction 2007). MPB is an eruptive, tree-killing bark beetle. Its fungal associates may provide it with Ambrosia beetles and bark beetles (Coleop- nutritional benefits and this may have important tera: Curculionidae: Scolytinae) are well implications for its population dynamics (Six known for their mutualistic associations with and Paine 1998; Bleiker and Six 2007). The fungi ophiostomatoid fungi (Ascomycota). Poten- may also play a role in overwhelming tree tial benefits to scolytine beetles of the asso- defenses and modifying the phloem in ways that ciation include nutritional supplementation benefit developing brood, like altering chemical and modification of host-tree tissues by the and moisture conditions (e.g., Reid et al. 1967; fungi, which favour brood development (e.g., Raffa and Berryman 1983; Yamaoka et al. 1995; Whitney 1971; Coppedge et al. 1995; Ayres et Lee et al. 2006; Bleiker and Six 2009). Both al. 2000; Bleiker and Six 2007). Fungi benefit species of fungi are also commonly isolated from by gaining access to new host trees that would the exoskeleton of adult MPBs. Six (2003a) otherwise be inaccessible. These benefits can found that for beetles caught in flight traps, only be reaped if the partners are able to G. clavigera was more often isolated from consistently maintain their association. mycangia than from the exoskeleton, while the Many ambrosia beetles and some bark reverse was true for O. montium. However, no beetles possess mycangia, which are special- differences were found for preflight adults ized integumental structures for transporting removed from under bark. Grosmannia clavigera fungi (Batra 1963). Traditionally the term may be better adapted to dispersal in mycangia mycangia has been reserved for sac- or tube- because MPB has a longer shared evolutionary like invaginations of the integument, which history with this fungus than with O. montium may be lined with glands (Six 2003b). Some (Six and Paine 1999). Ophiostoma montium may bark beetles, e.g., Ips typographus L., I. pini be an opportunistic ‘‘cheater’’ in the system, (Say), I. sexdentatus Boerner, Scolytus ventralis with spores better adapted for transport on the LeConte, and Dendroctonus pseudotsugae Hop- exoskeleton (Six and Paine 1998, 1999). MPB kins, lack sac-like mycangia but still are closely possesses well-defined pits on the elytra; associated with fungi (Livingston and Berryman however, whether or not the pits consistently 1972; Levieux et al. 1989; Furniss et al. 1990, transport fungi, and thus function as secondary 1995; Lewinsohn et al. 1994). These beetles rely mycangia, is not known. on exterior structures on the exoskeleton, such We used scanning electron microscopes as pits, to transport their fungal associates. Six (SEMs) to examine the exterior surface and (2003b) argued that any structures, such as mycangial openings of adult MPBs to deter- exterior pits, that consistently transport fungi mine where G. clavigera and O. montium are essentially function as mycangia. transported on the body and whether or The mountain pine beetle (MPB), Dendroc- not exterior structures (e.g., pits, asperites, or tonus ponderosae Hopkins, has paired sac-like setae) consistently transport fungi. We also mycangia (glandular status unknown) on the investigated the morphology of the fungi maxillary cardines of both sexes (Whitney and during transport and whether the two species Farris 1970). The most common fungi isolated are differentially transported on the body and from the mycangia of MPBs are Grosmannia in the maxillary mycangia. clavigera (Robinson-Jeffrey and Davidson) Zipfel, de Beer and Wingf. (previously Ophio- Materials and methods stoma clavigerum)andOphiostoma montium (Rumbold) von Arx (Whitney and Farris 1970; Adult MPBs used in this study came Six 2003a; Bleiker and Six 2007; Six and Bentz from near Superior and Butte, Montana E 2009 Entomological Society of Canada Bleiker et al. 505 (47.198905˚N, 112.471651˚W, and 45.834137˚N, severed head, and intact thorax and abdomen 112.471651˚W, respectively). At the Superior of each beetle were prepared for examination site, adults were collected from lodgepole pine by SEM as described above. (Pinus contorta Douglas ex Louden, Pinaceae) In 2006, one maxilla and one elytron were trees successfully mass-attacked by MPBs in excised from 51 beetles from the Butte popu- the summer of 2002. Trees were felled in lation and placed on 2% malt extract agar February 2003, cut into short logs (approxi- (MEA) amended with 100 ppm cyclohexamide. mately 60 cm long), and placed in rearing cages Cyclohexamide reduces contamination by inci- with collection cups. Rearing cages were made dental fungi, but the two species of mycangial from 60 L plastic bins or garbage cans. Two fungi associated with the MPB are tolerant of vents, each approximately 20 cm 6 15 cm, this antibiotic. Cultures were stored in the were cut in each cage and covered with fine laboratory (at approximately 22 ˚C) for a wire mesh and dark cotton cloth. A 6 cm minimum of 4 weeks before fungal isolates were diameter hole was cut in the side of each cage identified.
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