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Root-inhabiting bark beetles (Coleoptera: Curculionidae) and their fungal associates breeding in dying loblolly pine in Alabama.

Root feeding bark beetles in the genus Hylastes (Coleoptera: Curculionidae: Scolytinae) commonly carry ophiostomatoid fungi (Ophistomatales: Ophistomataceae)and collectively contribute to root disorders of Pinus species around the world (Jacobs & Wingfield 2001). One of the most damaging root disorders is black-stain root disease of conifers in the Western United States, caused by the fungal species Leptographium wageneri Kendrick and its primary beetle vector H. nigrinus (Mannerheim) (Witcosky et al. 1986). Recently, Hylastes salebrosus Eichhoff and H. tenuis Eichhoff have been associated with loblolly pine (Pinus taeda L.) decline (Eckhardt et al. 2007), which is considered an emerging forest health issue in the southeastern United States (Eckhardt et al. 2010).

Loblolly pine decline (LPD) is a tree disease complex that is characterized by symptoms that include thinning tree crowns, growth reductions (Eckhardt et al. 2007) and premature mortality in localized areas (Brown and McDowell 1968). Evidence suggests the complex is the result of interacting abiotic (Eckhardt & Menard 2008) and biotic (Eckhardt et al. 2007) stress factors. Hylastes species vector a variety of root-infecting ophiostomatoid fungi (Klebzig et al. 1991, 1995; Eckhardt et al. 2007; Zanzot et al. 2010) which are pathogenic to loblolly pine (Matusick & Eckhardt 2010; Matusick et al. 2011). Hylastes beetles and their associated fungi are thought to collectively contribute to LPD by causing root damage through fungal infection and insect feeding (Eckhardt et al. 2007). Root and lower stem feeding beetle species (Coleoptera: Curculionidae) including H. salebrosus and H. tenuis are found in increased numbers within LPD-affected stands, compared to healthy stands (Eckhardt et al. 2007, Menard 2007). A recent study has found Hylastes to be the most common bark beetle genus observed in loblolly pine stands in central Alabama (Thompson 2011), illustrating their dominance in this ecosystem. Despite their dominance and potential for damage in loblolly pine, the breeding behavior of Hylastes species in the southeastern United States is not well understood. In the current study, observational methods were used to investigate the potential for Hylastes breeding in loblolly pine across 3 crown condition classes (healthy, dying, dead). Additionally, the relationship between ophiostomatoid species, their Hylastes species vectors, and tree condition were investigated.

Loblolly pine stands across central Alabama have experienced high mortality rates, characterized by scattered stand mortality with a distinct lack of above-ground pests (Brown & McDowell 1968). During an investigation of one stand in May 2008 in central Alabama, dying trees were found to be infested with root-inhabiting beetles and their associated ophiostomatoid fungi. Six trees were selected based on crown condition, including 2 with green, healthy crowns (healthy), 2 with severely chlorotic and thinning crowns (dying), and 2 with red crowns (dead). Two primary lateral roots were randomly selected and excavated to approximately 3 meters from the root collar. Roots were removed from trees and carefully dissected. All insects, including immature stages, were collected from roots and adult beetles were identified to species. Root tissue was obtained from each brood gallery for the isolation of ophiostomatoid fungal species using methods described in Eckhardt et al. (2007). Following surface sterilization, tissue was placed on CSMA (malt extract agar containing 800 mg/L of cycloheximide and 200 mg/l of streptomycin sulfate) selective nutrient agar (Jacobs & Wingfield 2001). Each adult insect was also rolled on CSMA to recover ophiostomatoid fungi from insect bodies (Zanzot et al. 2010). Isolated ophiostomatoid fungal species were identified using morphological characters and established keys. Unknown isolates were sequenced and confirmed as new species by M. Wingfield (Forestry and Agricultural Biotechnology Institute, Pretoria, South Africa).

A total of 157 adult beetles (Coleoptera: Curculionidae) were collected from roots, most from dying trees (Table 1). A majority of the beetles collected were Hylastes species, including a total of 113 H. salebrosus (all from dying trees) and 34 H. tenuis (31 from dying and 3 from dead trees). In addition, H. salebrosus larvae and pupae were collected from dying trees. Other adult insect species collected include the black turpentine beetle (Dendroctonus terebrans (Olivier) (1-dying and 3-dead), and Xyleborus pubescens Zimmerman (6-dying trees). This examination is the first to observe and provide evidence for Hylastes species breeding in loblolly pine roots and supports previous reports of Hylastes species breeding behavior in other, similar ecosystems (Blackman 1941; Stoakley 1968; Witcosky & Hansen 1985).

Adult beetles were commonly found transporting ophiostomatoid fungal species, including 47% of all beetle species, 40% of H. salebrosus, and 70% of H. tenuis. Collectively, insects transported a total of 5 ophiostomatoid species. Leptographium terebrantis was most commonly transported (23% of all beetles). Additional species in order of frequency included, Grosmannia huntii (R.C. Rob. Jeffr.) Zipfel, Z. W. de Beer & M. J. Wingfield (L. huntii M. J. Wingfield) (19%), L. procerum (6%), and L. serpens (Goid) M. J. Wingf. (1%).

Seven insects transported more than one fungal species. In a similar loblolly pine stand in central Alabama, a large-scale trapping experiment found that H. salebrosus and H. tenuis transported fungal species at slightly higher rates than those reported here (Eckhardt et al. 2007). With respect to the beetle-fungal association, data from this research supports conclusions made by Zanzot et al. (2010), that ophiostomatoid fungi are likely facultatively associated with Hylastes vectors in the southeastern United States.

Ophiostomatoid fungi were predominately isolated from dying and dead trees (Table 2). Leptographium terebrantis and G. huntii were most frequently isolated including from root tissue and beetles from both dead and dying trees. Leptographium procerum was infrequently isolated from dying trees and was the only fungal species isolated from healthy tree tissue, which supports previous reports (Zanzot 2010). Leptographium serpens, which was infrequently isolated from insects, was not isolated from root tissue. Additionally, one undescribed Ophiostoma species was infrequently isolated from tissue during sampling.

The findings reported here represent the first observations of Hylastes species breeding in roots of loblolly pine. Up until this point, the tissue used for brood development of Hylastes species in the southeastern United States has only been hypothesized. These observations have implications on the LPD cycle by confirming dying trees contribute to increasing Hylastes populations, suggesting a positive feedback cycle with regards to LPD in severely affected stands. These observations, coupled with previous findings from elsewhere (Witcosky & Hansen 1985) also suggest Hylastes species development may be restricted to trees in a dying condition. Additional research is needed to determine the root environmental conditions required for Hylastes species development as well as to determine the potential for Hylastes species to invade and successfully reproduce in healthy trees, particularly where populations are high.

REFERENCES CITED

Blackman, M. W. 1941. Bark beetles of the genus Hylastes Erichson in North America. U.S. Dept. of Agric. Misc. Publ. no. 417.

Brown, H. D., and McDowell, W. E. 1968. Status of loblolly pine die-off on the Oakmulgee District, Talladega National Forest, Alabama-1968. U.S. Dep. Agric. For. Serv. Rept. No. 69-2-28.

Eckhardt, L. G., Goyer, R. A., Klepzig, K. D., and Jones, J. P. 2004. Interactions of Hylastes species (Coleoptera: Scolytidae) with Leptographium species associated with loblolly pine decline. J. Econ. Entomol. 97(2): 468-474.

Eckhardt, L. G., Weber, A. M., Menard, R. D., Jones, J. P., and Hess, N. J. 2007. Insect-fungal complex associated with loblolly pine decline in central Alabama. For. Sci. 53(1): 84-92.

Eckhardt, L. G., and Menard, R. D. 2008. Topographic features associated with loblolly pine decline in central Alabama. For. Ecol. Mgt. 255: 1735-1739.

Eckhardt, L., Sward Sayer, M. A., and Imm, D. 2010. State of pine decline in the southeastern United States. Southern J. Appl. For. 34(3): 138-141.

Jacobs, K., and Wingfield, M. J. [eds.]. 2001. Leptographium species, tree pathogens, insect associates and agents of blue-stain. American Phytopath. Soc. St. Paul, MN.

Klepzig, K. D., Raffa, K. F., and Smalley, E. B. 1991: Association of insect-fungal complex with red pine decline in Wisconsin. For. Sci. 37(4): 1119-1139.

Klepzig, K. D., Smalley, E. B., and Raffa, K. F. 1995. Dendroctonus valens and Hylastes porculus (Coleoptera: Scolytidae): vectors of pathogenic fungi (Ophiostomatales) associated with red pine decline disease. Great Lakes Entomol. 28(1): 81-87.

Matusick, G., and Eckhardt, L. G. 2010. Variation in virulence among four-root-inhabiting ophiostomatoid fungi on Pinus taeda L., P. palustris Mill., and P. elliottii Engelm. seedlings. Canadian J. Plant Path. 32(3): 361-367.

Matusick, G., Somers, G. L., and Eckhardt, L. G. 2011. Root lesions in large loblolly pine (Pinus taeda L.) following inoculation with root-inhabiting ophiostomatoid fungi. For. Path. 42: 37-43.

Menard, R. D. 2007. An assessment of the risk mapping system for the use of managing loblolly pine decline sites within red-cockaded woodpecker habitat. M.S. Thesis Louisiana State University. Baton Rouge, LA.

Stoakley, J. T. 1968. Control of the pine weevil, Hylobius abietis L., and of Hylastes species. Forestry 41(2): 182-188.

Thompson, J. A. 2011. Two-year bark and ambrosia beetle diversity study at the Talladega National Forest in the Southeastern United States. M.S. Thesis, Auburn University, Auburn, AL.

Witcosky, J. J., and Hansen, E. M. 1985. Root-colonizing insects recovered from Douglas-fir in various stages of decline due to black-stain root disease. Phytopathology 75: 399-402.

Witcosky, J. J., Schowalter, T. D., and Hansen, E. M. 1986. Hylastes nigrinus (Coleoptera: Scolytidae), Pissodes fasciatus, and Steremnius carinatus (Coleoptera: Curculionidae) as vectors of black-stain root disease of Douglas-fir. Environ. Entomol. 15: 1090-1095.

Zanzot, J. W., Matusick, G., and Eckhardt, L. G. 2010: Ecology of root-feeding beetles and their associated fungi on longleaf pine in Georgia. Eviron. Entomol. 39(2): 415-423.

GEORGE MATUSICK (1), (3), ROGER D. MENARD (2), YUAN ZENG (3) AND LORI G. ECKHARDT (3)

(1) The Nature Conservancy, Chattahoochie Fall Line Project, Fort Benning, GA, USA

(2) U.S. Department of Agriculture, Forest Service, Forest Health Protection. Pineville, LA, USA

(3) School of Forestry and Wildlife Sciences, Auburn University. Auburn, AL

* Corresponding author; E-mail: gmatusick@tnc.org
TABLE 1. THE TOTAL NUMBER OF BEETLES COLLECTED AND
BEETLES COLLECTED FOUND TRANSPORTING OPHIOSTOMATOID
FUNGI IN 6 LOBLOLLY PINE TREES REPRESENTING
3 HEALTH CONDITIONS.

 Beetles
 Tree Adult vectoring
Tree Health Class # beetles (#) fungi (#)

Healthy (1) 1 0 0
 2 0 0
Dying (2) 3 26 19
 4 125 50
Dead (3) 5 3 3
 6 3 2
Total 157 74

(1) Sample trees with predominantly (>90%) healthy foliage
(dark green).

(2) Sample trees with predominantly (>70%) dying foliage (pale
green and yellow).

(3) Sample trees lacking most (>90%) foliage, with the remaining
being dead (red).

TABLE 2. NUMBER OF INDEPENDENT ISOLATES OF EACH OF
4 OPHIOSTOMATOID FUNGI ISOLATED FROM ROOT TISSUE
(BEETLE GALLERIES) AND ADULT BEETLE BODIES,
COLLECTED FROM LOBLOLLY PINE TREES WITHIN 3 HEALTH
CONDITIONS.

 (1) Dead Trees (2) Dying Trees

Fungal Species Tissue Beetles Tissue Beetles

L. terebrantis 18 3 45 62
G. huntii 3 2 13 43
L. procerum 1 0 10 12
L. serpens 0 0 0 2

 (3) Healthy Trees

Fungal Species Tissue Beetles

L. terebrantis 0 0
G. huntii 0 0
L. procerum 9 0
L. serpens 0 0

(1) Sample trees lacking most (>90%) foliage, with the
remaining being dead (red).
(2) Sample trees with predominantly (>70%) dying foliage
(pale green and yellow).
(3) Sample trees with predominantly (>90%) healthy
foliage (dark green).
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Title Annotation:Scientific Notes
Author:Matusick, George; Menard, Roger D.; Zeng, Yuan; Eckhardt, Lori G.
Publication:Florida Entomologist
Article Type:Report
Geographic Code:1U6AL
Date:Mar 1, 2013
Words:1843
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