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Ecology of Mountain Pine Beetle (Coleoptera: Scolytidae) Cold Hardening in the Intermountain West

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Ecology of Mountain Pine Beetle (Coleoptera: Scolytidae) Cold Hardening in the Intermountain West PHYSIOLOGICAL AND CHEMICAL ECOLOGY Ecology of Mountain Pine Beetle (Coleoptera: Scolytidae) Cold Hardening in the Intermountain West 1 2 B. J. BENTZ AND D. E. MULLINS Environ. Entomol. 28(4): 577Ð587 (1999) ABSTRACT The mountain pine beetle, Dendroctonus ponderosae Hopkins, spends the majority of its life cycle within the phloem of pine trees, experiencing exposure to temperatures below Ϫ30ЊC in many parts of their expansive range. To better understand cold tolerance capabilities of this insect, seasonal patterns of cold-hardiness, as measured by supercooling points in the laboratory, were compared with seasonal patterns of host tree phloem temperatures at several geographic sites for 2 beetle generations. Larvae were found to be intolerant of tissue freezing, and supercooling points measured appear to be a reasonable estimate of the lower limit for survival. Of the compounds analyzed, glycerol was found to be the major cryoprotectant. No differences in supercooling points were found among instars or between larvae collected from the north and south aspect of tree boles. Both phloem temperatures and supercooling points of larvae collected from within the phloem were found to be different among the geographic sites sampled. Mountain pine beetle larvae appear to respond to seasonal and yearly ßuctuations in microhabitat temperatures by adjusting levels of cold hardening. KEY WORDS Dendroctonus ponderosae, bark beetle, supercooling point, freeze intolerant THE MOUNTAIN PINE beetle, Dendroctonus ponderosae tectants such as polyhydric alcohols (polyols) and Hopkins, which overwinters under the bark of pine sugars (Hamilton et al. 1985, Lee and Denlinger 1991). trees in a nonmobile stage, is unable to escape low Polyol synthesis is known to be triggered by low- temperature exposure. When escape from low tem- temperature exposure, with increasing rates at lower peratures is unavoidable, many insect species respond temperatures (Baust 1982, Storey and Storey 1983). by adjusting physiological and biochemical processes Most likely, thermoperiodic cues, represented by that enhance their tolerance to freezing temperatures. some threshold length of time at or below a particular Freeze tolerant species are able to withstand the for- temperature, promote accumulation of an adequate mation of ice in the extracellular body ßuid, whereas concentration of cryoprotectants before the time they freeze intolerant species must avoid freezing of body are needed (Storey and Storey 1991). To more fully tissues (Salt 1961). Freeze avoidance is accomplished understand the role of cold-hardening in mountain through cold-hardening. The supercooling point re- pine beetle population dynamics, therefore, it is nec- fers to the temperature at which spontaneous nucle- essary to relate supercooling capacities as determined ation of body water occurs and ice crystals begin to in the laboratory to the thermal history of the micro- form in the insect tissue (Lee 1989). For those species habitat where larvae reside (Bale 1991). that cannot survive tissue freezing, the supercooling The microhabitat of the mountain pine beetle is the point represents a lethal temperature threshold, al- phloem of living pines, wherein the majority of the life though death may also result as a consequence of cycle is spent typically overwintering as larvae. In the exposure to temperatures above the supercooling northernmost part of their range, winter temperatures point (Lee 1991). The cold-hardening capacity of an below Ϫ30ЊC are not uncommon. Mountain pine bee- insect may vary with the developmental stage, nutri- tle eggs and pupae are considered the least cold tol- tional status, and duration of exposure to speciÞc low erant life-stages (Reid 1963, Reid and Gates 1970, temperatures. Amman 1973), whereas the large larvae are thought to Many physiological mechanisms involved in the be the most cold tolerant (Yuill 1941, Wygant 1942, cold-hardening process have been identiÞed includ- Somme 1964). Given that effects of temperature on ing ice-nucleating proteins, lipoproteins and anti- developmental rate are stage-speciÞc (Bentz et al. freeze proteins, evacuation of the gut to remove po- 1991), cold-hardening capabilities may also depend on tential ice nucleating agents, ice nucleating bacteria, life-stage, with one stage more adapted for overwin- and accumulation of low molecular weight cryopro- tering than another. Although temperature has pre- viously been assigned as the most important mortality factor of the mountain pine beetle (Safranyik 1978, 1 USDA Forest Service, Rocky Mountain Research Station, Logan, UT 84321. Cole 1981), little is understood about the timing of low 2 Virginia Polytechnic Institute and State University, Blacksburg, temperatures and their effect on the population dy- VA 20461. namics of this nondiapausing species. SpeciÞc objec- 578 ENVIRONMENTAL ENTOMOLOGY Vol. 28, no. 4 Table 1. Site collection information Site Host Elevation, m Latitude Site aspect Basal area, ft2/acre 1992Ð1993 Logan, UT LPP 2,043 41Њ 56Ј NE 210 Ranch, ID LPP 2,061 44Њ 07Ј SW 140 Moose, WY LPP 2,121 42Њ 45Ј N 100 Galena, ID LPP 2,348 43Њ 54Ј W 170 1994Ð1995 Ranch, ID LPP 2,061 44Њ 07Ј SW 170 Beaver, ID LPP 2,247 43Њ 59Ј W 160 Cedar, UT PP 2,622 37Њ 37Ј E 270 LPP, logdepole pine (Pinus contorta Douglas); PP, ponderosa pine (P. ponderosa Laws). tives of this study were the following: to determine Campbell ScientiÞc, Logan, UT). A sudden tempera- supercooling points of Þeld collected mountain pine ture increase (Ն0.5ЊC), which is associated with for- beetle larvae and associated microhabitat temperature mation of an ice lattice in insect tissue, indicated the regimes, to determine the physiological mechanisms supercooling point of each individual instar. After the that allow cold tolerance in mountain pine beetle supercooling point was determined, each larvae was larval stages, and to characterize the pattern of low placed at room temperature and the head capsule temperature tolerance among geographic regions. width measured to determine instar (Logan et al. 1998). After several hours at room temperature, larvae were gently probed to evoke a response. If larvae are Materials and Methods freeze-tolerant, they can survive the freezing process Supercooling Point Determination. Mountain pine and therefore would respond to probing after warm- beetles of different instars were collected from several ing up. Otherwise, if larvae are dead after the freezing infested trees at 4 sites during the 1992Ð1993 genera- process, we assumed they were freeze-intolerant. tion, and 3 sites during the 1994Ð1995 generation (Ta- To assess if larvae were alive at temperatures above ble 1). Individuals were collected from 1 site, Ranch, the measured supercooling point, 16 larvae were both years. All larvae were collected above the snow cooled (as above) to Ϸ4ЊC above the mean super- line from either the north or south aspect of the bole. cooling point determined for 16 additional larvae Samples were collected 6 times during each genera- taken from the same tree. The larvae were slowly tion from the same trees. On each sample date, larvae returned to room temperature and allowed to sit for were removed live from under the bark, placed in petri 24 h. After this period, larval survival was determined. dishes with moistened Þlter paper, and the dishes Supercooling data were analyzed separately for packed in insulated coolers for transportation to the each generation. Larvae from each site were pooled by laboratory. We also recorded the proportion of larvae month of collection. A three-way analysis of variance that were dead at the time of collection. In 1992Ð1993, (ANOVA) with subsampling, blocked by site, was larvae were shipped via overnite express mail to Vir- performed using month, aspect on the tree, and instar ginia Polytechnic Institute and State University as the factors (SAS, PROC GLM, SAS Institute 1989). (VPI&SU), Blacksburg, VA, for supercooling point Although larvae were collected from 2 to 3 trees at determination. In 1994Ð1995, all supercooling point each site on each sample date, this separation was not analysis was performed at the Forestry Sciences Lab- maintained in the supercooling analysis and a measure oratory in Logan, UT. In 1994Ð1995, a subsample from of tree replication at each site was therefore not avail- 3 sample dates were shipped to VPI&SU for polyol able. An experimental error term was calculated as the analysis. interaction between site and the treatment effects The same technique for determining supercooling (aspect, instar, and month). This experimental error points was used both years. Using forceps, individual term included the error caused by subsampling and larvae were positioned between 2 copper constantan was used in calculating the F statistic. Interaction thermocouples (COC0Ð003, Omega Technologies, terms that included cells with empty data were ex- Stamford, CT) resting on the surface of a cold plate cluded from the analysis. The StudentÐNewmanÐ (Stir-Kool Cold plate [SK-31], Thermoelectrics Un- Keuls method was used to compare treatment means. limited, Wilmington, DE) connected to a Fisher Iso- Temperature Measurements. Beetle ßight, host col- temp Circulator (13-874-72A, Pittsburgh, PA) that had onization, and brood emergence were monitored at been cooled to Ϸ0ЊC. Eight larvae were analyzed at 1 each site. Upon successful host colonization, temper- time. Temperatures among thermocouples were sta- ature probes were placed in the phloem of 4 infested bilized by placing an
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