Cross-scale interaction of host tree size and climatic water deficit governs bark beetle-induced tree mortality.

The recent Californian hot drought (2012-2016) precipitated unprecedented ponderosa pine (Pinus ponderosa) mortality, largely attributable to the western pine beetle (Dendroctonus brevicomis; WPB). Broad-scale climate conditions can directly shape tree mortality patterns, but mortality rates respond non-linearly to climate when local-scale forest characteristics influence the behavior of tree-killing bark beetles (e.g., WPB). To test for these cross-scale interactions, we conduct aerial drone surveys at 32 sites along a gradient of climatic water deficit (CWD) spanning 350 km of latitude and 1000 m of elevation in WPB-impacted Sierra Nevada forests. We map, measure, and classify over 450,000 trees within 9 km2, validating measurements with coincident field plots. We find greater size, proportion, and density of ponderosa pine (the WPB host) increase host mortality rates, as does greater CWD. Critically, we find a CWD/host size interaction such that larger trees amplify host mortality rates in hot/dry sites. Management strategies for climate change adaptation should consider how bark beetle disturbances can depend on cross-scale interactions, which challenge our ability to predict and understand patterns of tree mortality.

Evidence for Semiochemical Divergence Between Sibling Bark Beetle Species: Dendroctonus brevicomis and Dendroctonus barberi.

We investigated geographic variation in the semiochemistry of major disturbance agents of western North American pine forests, Dendroctonus brevicomis Le Conte and Dendroctonus barberi Hopkins (Coleoptera: Curculionidae: Scolytinae), species separated by the Great Basin in the USA that until recently were synonymous. At 15 sites in the western USA and northern Mexico, beetle populations were examined to determine (1) pheromone production by solitary, mining females, (2) male electroantennogram amplitudes in response to known semiochemicals for the genus, or (3) relative attractiveness of two female-produced pheromone components (endo- and exo-brevicomin) and two host odors (alpha-pinene and myrcene) to beetles in the field. Compared to female beetles collected east of the Great Basin (D. barberi), western females (D. brevicomis) produced a consistently higher proportion of, and male antenna were correspondingly more sensitive to, the exo- than the endo-isomer of brevicomin. With the exception of one sampling location (where no preference was observed), beetles west of the Great Basin were more attracted to exo- than endo- brevicomin trap lures, whereas eastern beetles displayed the reverse preference. In contrast, there was not a consistent difference between these populations regarding relative attraction or olfactory response to myrcene or alpha-pinene, although some geographic variability was evident. These data show that the semiochemical systems of D. brevicomis and D. barberi have diverged and corroborate genetic and morphological evidence that they are distinct, allopatric species.

Ponderosa pine resin defenses and growth: metrics matter.

Bark beetles (Coleoptera: Curculionidae, Scolytinae) cause widespread tree mortality in coniferous forests worldwide. Constitutive and induced host defenses are important factors in an individual tree's ability to survive an attack and in bottom-up regulation of bark beetle population dynamics, yet quantifying defense levels is often difficult. For example, in Pinus spp., resin flow is important for resistance to bark beetles but is extremely variable among individuals and within a season. While resin is produced and stored in resin ducts, the specific resin duct metrics that best correlate with resin flow remain unclear. The ability and timing of some pine species to produce induced resin is also not well understood. We investigated (i) the relationships between ponderosa pine (Pinus ponderosa Lawson & C. Lawson) resin flow and axial resin duct characteristics, tree growth and physiological variables, and (ii) if mechanical wounding induces ponderosa pine resin flow and resin ducts in the absence of bark beetles. Resin flow increased later in the growing season under moderate water stress and was highest in faster growing trees. The best predictors of resin flow were nonstandardized measures of resin ducts, resin duct size and total resin duct area, both of which increased with tree growth. However, while faster growing trees tended to produce more resin, models of resin flow using only tree growth were not statistically significant. Further, the standardized measures of resin ducts, density and duct area relative to xylem area, decreased with tree growth rate, indicating that slower growing trees invested more in resin duct defenses per unit area of radial growth, despite a tendency to produce less resin overall. We also found that mechanical wounding induced ponderosa pine defenses, but this response was slow. Resin flow increased after 28 days, and resin duct production did not increase until the following year. These slow induced responses may allow unsuccessfully attacked or wounded trees to resist future bark beetle attacks. Forest management that encourages healthy, vigorously growing trees will also favor larger resin ducts, thereby conferring increased constitutive resistance to bark beetle attacks.

Low-severity fire increases tree defense against bark beetle attacks.

Induced defense is a common plant strategy in response to herbivory. Although abiotic damage, such as physical wounding, pruning, and heating, can induce plant defense, the effect of such damage by large-scale abiotic disturbances on induced defenses has not been explored and could have important consequences for plant survival facing future biotic disturbances. Historically, low-severity wildfire was a widespread, frequent abiotic disturbance in many temperate coniferous forests. Native Dendroctonus and Ips bark beetles are also a common biotic disturbance agent in these forest types and can influence tree mortality patterns after wildfire. Therefore, species living in these disturbance-prone environments with strategies to survive both frequent fire and bark beetle attack should be favored. One such example is Pinus ponderosa forests of western North America. These forests are susceptible to bark beetle attack and frequent, low-severity fire was common prior to European settlement. However, since the late 1800s, frequent, low-severity fires have greatly decreased in these forests. We hypothesized that non-lethal, low-severity, wildfire induces resin duct defense in P. ponderosa and that lack of low-severity fire relaxes resin duct defense in forests dependent on frequent, low-severity fire. We first compared axial resin duct traits between trees that either survived or died from bark beetle attacks. Next, we studied axial ducts using tree cores with crossdated chronologies in several natural P. ponderosa stands before and after an individual wildfire and, also, before and after an abrupt change in fire frequency in the 20th century. We show that trees killed by bark beetles invested less in resin ducts relative to trees that survived attack, suggesting that resin duct-related traits provide resistance against bark beetles. We then show low-severity fire induces resin duct production, and finally, that resin duct production declines when fire ceases. Our results demonstrate that low-severity fire can trigger a long-lasting induced defense that may increase tree survival from subsequent herbivory.

Limited response of ponderosa pine bole defenses to wounding and fungi.

Tree defense against bark beetles (Curculionidae: Scolytinae) and their associated fungi generally comprises some combination of constitutive (primary) and induced (secondary) defenses. In pines, the primary constitutive defense against bark beetles consists of preformed resin stored in resin ducts. Induced defenses at the wound site (point of beetle entry) in pines may consist of an increase in resin flow and necrotic lesion formation. The quantity and quality of both induced and constitutive defenses can vary by species and season. The inducible defense response in ponderosa pine is not well understood. Our study examined the inducible defense response in ponderosa pine using traumatic mechanical wounding, and wounding with and without fungal inoculations with two different bark beetle-associated fungi (Ophiostoma minus and Grosmannia clavigera). Resin flow did not significantly increase in response to any treatment. In addition, necrotic lesion formation on the bole after fungal inoculation was minimal. Stand thinning, which has been shown to increase water availability, had no, or inconsistent, effects on inducible tree defense. Our results suggest that ponderosa pine bole defense against bark beetles and their associated fungi is primarily constitutive and not induced.

Seeing the forest through the trees: differential dispersal of Hylobius warreni within modified forest habitats.

Hylobius warreni Wood, also known as the Warren root collar weevil, is a flightless insect that feeds on conifers throughout the boreal forests of Canada. Mature trees typically can withstand feeding, but larval feeding around the root collar may cause mortality to young trees. Recently, a large outbreak of mountain pine beetle (Dendroctonus ponderosae Hopkins) has killed a high proportion of mature lodgepole pine (Pinus contorta Douglas variety latifolia) across British Columbia, Canada. This raises concerns that adult weevils may migrate from mature forests with reduced host pools into adjacent young forests that had been salvaged and replanted. To study movement of these walking weevils in different habitat types, we constructed three research plots consisting of various combinations of live-, dead-, and mixed (i.e., live and dead)-tree habitats. We observed dispersal patterns of individually labeled insects using a novel insect trap attached to the base of trees. Approximately 35% of insects were recaptured over 1 mo. Weevils were least likely to be recaptured proximate to the release location when released in a habitat with dead trees. Movement rates therein were almost double the rates of insects moving through live- or mixed-tree habitats. Our findings support the hypothesis that H. warreni may disperse out of habitats with dead trees into areas with higher proportions of green trees. Our findings are discussed in the context of habitat discrimination and potential increases in herbivory by H. warreni in western Canada given salvage harvesting activities after outbreaks of mountain pine beetle.

Evaluation of multiple funnel traps and stand characteristics for estimating western pine beetle-caused tree mortality.

The western pine beetle, Dendroctonus brevicomis LeConte (Coleoptera: Curculionidae: Scolytinae), is a major cause of ponderosa pine, Pinus ponderosa Dougl. ex Laws., mortality in much of western North America. This study was designed to quantify relationships between western pine beetle trap catches [including those of its primary invertebrate predator Temnochila chlorodia (Mannerheim) (Coleoptera: Trogositidae)], and levels of tree mortality attributed to western pine beetle at 44 trapping sites (stands) and within five general locations (forests) in California. Furthermore, we evaluated relationships between forest stand characteristics and levels of western pine beetle-caused tree mortality. Preliminary analyses were conducted by Pearson's correlation coefficient (r) using tree mortality per hectare and percentage of tree mortality and 10 potential predictor variables. All predictor variables that had significant correlations (western pine beetle per day, western pine beetle: T. chlorodia, percentage of western pine beetle [percentage of total trap catch represented by western pine beetle], trees per hectare, basal area of all tree species, basal area of P. ponderosa, mean diameter at breast height [dbh] and stand density index) were considered for linear and multiple linear regression models for predicting levels of western pine beetle-caused tree mortality. Our results suggest monitoring western pine beetle populations through the use of pheromone-baited multiple funnel traps is not an effective means of predicting levels of western pine beetle-caused tree mortality. However, levels of western pine beetle-caused tree mortality can be efficiently predicted (adjusted R2 >0.90) at large spatial scales (forests; approximately 3,000-14,000 ha of contiguous host) by simply measuring stand density, specifically the basal area of all tree species or stand density index. The implications of these results to forest management are discussed.

Evaluation of funnel traps for characterizing the bark beetle (Coleoptera: Scolytidae) communities in ponderosa pine forests of north-central Arizona.

Lindgren funnel traps baited with aggregation pheromones are widely used to monitor and manage populations of economically important bark beetles (Coleoptera: Scolytidae). This study was designed to advance our understanding of how funnel trap catches assess bark beetle communities and relative abundance of individual species. In the second year (2005) of a 3-yr study of the bark beetle community structure in north-central Arizona pine (Pinus spp.) forests, we collected data on stand structure, site conditions, and local bark beetle-induced tree mortality at each trap site. We also collected samples of bark from infested (brood) trees near trap sites to identify and determine the population density of bark beetles that were attacking ponderosa pine, Pinus ponderosa Douglas ex Lawson, in the area surrounding the traps. Multiple regression models indicated that the number of Dendroctonus and Ips beetles captured in 2005 was inversely related to elevation of the trap site, and positively associated with the amount of ponderosa pine in the stand surrounding the site. Traps located closer to brood trees also captured more beetles. The relationship between trap catches and host tree mortality was weak and inconsistent in forest stands surrounding the funnel traps, suggesting that trap catches do not provide a good estimate of local beetle-induced tree mortality. However, pheromone-baited funnel trap data and data from gallery identification in bark samples produced statistically similar relative abundance profiles for the five species of bark beetles that we examined, indicating that funnel trap data provided a good assessment of species presence and relative abundance.

Traps and attractants for wood-boring insects in ponderosa pine stands in the Black Hills, South Dakota.

Recent large-scale wildfires have increased populations of wood-boring insects in the Black Hills of South Dakota. Because little is known about possible impacts of wood-boring insects in the Black Hills, land managers are interested in developing monitoring techniques such as flight trapping with semiochemical baits. Two trap designs and four semiochemical attractants were tested in a recently burned ponderosa pine, Pinus ponderosa Dougl. ex Laws., forest in the Black Hills. Modified panel and funnel traps were tested in combination with the attractants, which included a woodborer standard (ethanol and alpha-pinene), standard plus 3-carene, standard plus ipsenol, and standard plus ipsdienol. We found that funnel traps were equally efficient or more efficient in capturing wood-boring insects than modified panel traps. Trap catches of cerambycids increased when we added the Ips spp. pheromone components (ipsenol or ipsdienol) or the host monoterpene (3-carene) to the woodborer standard. During the summers of 2003 and 2004, 18 cerambycid, 14 buprestid, and five siricid species were collected. One species of cerambycid, Monochamus clamator (LeConte), composed 49 and 40% of the 2003 and 2004 trap catches, respectively. Two other cerambycids, Acanthocinus obliquus (LeConte) and Acmaeops proteus (Kirby), also were frequently collected. Flight trap data indicated that some species were present throughout the summer, whereas others were caught only at the beginning or end of the summer.

Influence of elevation on bark beetle (Coleoptera: Curculionidae, Scolytinae) community structure and flight periodicity in ponderosa pine forests of Arizona.

We examined abundance and flight periodicity of five Ips and six Dendroctonus species (Coleoptera: Curculionidae, Scolytinae) among three different elevation bands in ponderosa pine (Pinus ponderosa Douglas ex. Lawson) forests of northcentral Arizona. Bark beetle populations were monitored at 10 sites in each of three elevation bands (low: 1,600-1,736 m; middle: 2,058-2,230 m; high: 2,505-2,651 m) for 3 yr (2004-2006) using pheromone-baited Lindgren funnel traps. Trap contents were collected weekly from March to December. We also studied temperature differences among the elevation bands and what role this may play in beetle flight behavior. Bark beetles, regardless of species, showed no consistent elevational trend in abundance among the three bands. The higher abundances of Ips lecontei Swaine, I. calligraphus ponderosae Swaine, Dendroctonus frontalis Zimmerman, and D. brevicomis LeConte at low and middle elevations offset the greater abundance of I. knausi Swaine, D. adjunctus Blandford, D. approximatus Dietz, and D. valens LeConte at high elevations. I. pini (Say) and I. latidens LeConte were found in similar numbers across the three bands. Flight periodicity of several species varied among elevation bands. In general, the flight period shortened as elevation increased; flight initiated later and terminated earlier in the year. The timing, number, and magnitude of peaks in flight activity also varied among the elevation bands. These results suggest that abundance and flight seasonality of several bark beetles are related to elevation and the associated temperature differences. The implications of these results are discussed in relation to bark beetle management and population dynamics.

Effects of associational resistance and host density on woodland insect herbivores.

1. Specialist herbivores often become less abundant per unit of host tissue as host density increases (resource dilution). They usually become less abundant when non-host species are mixed with their host plants (associational resistance). Most studies of these trends have involved herbaceous host plants and have not examined both trends for the same herbivores. 2. Three hypotheses were tested for the response of insect specialists to host plant density: resource concentration, plant apparency and resource dilution. Two hypotheses were tested for the response of herbivores to non-host plants: associational resistance and plant apparency. 3. From 1992 to 2007, I examined the responses of three monophagous insect herbivores to the densities of their host, Pinus edulis, and of two non-hosts, Pinus ponderosa and Juniperus spp. 4. Herbivore loads increased with host density, though the correlations were weak and often variable between generations. These results were consistent with the resource concentration and plant apparency hypotheses, but not with resource dilution. 5. Herbivore loads decreased as non-host density increased, consistent with the associational resistance hypothesis. This and other studies have shown that associational resistance is important in many types of plant communities. 6. The absence of resource dilution on woodland trees contrasted with studies of herbaceous host plants. Further comparisons of woody and herbaceous host plants are needed to elucidate the reasons for this difference.

The disruption of an ant-aphid mutualism increases the effects of birds on pine herbivores.

Predators affect herbivores directly and indirectly, by consumptive and nonconsumptive effects, and the combined influence of multiple predators is shaped by interactions among predators. I documented the individual and combined effects of birds (chickadees, nuthatches, warblers) and ants (Formica podzolica) on arthropods residing in pine (Pinus ponderosa) canopies in a factorial field experiment. Birds and ants removed herbivores but simultaneously benefited them by removing predatory arthropods. Birds and ants had net negative and positive effects, respectively, on the abundance of herbivore prey, supporting the notion that vertebrate predators have stronger negative effects on herbivores than do arthropod predators. Aphids (ant-tended and untended species) constituted three-quarters of herbivore biomass. The effect of birds on ant-tended aphids was twice that on untended aphid species or tended aphid species without ants. This was not due to there being more ant-tended aphids for birds to prey on; tended and untended aphid species were in similar abundances in the absence of birds. Instead, the effects of birds were strengthened by attributes of the mutualism that rendered tended aphids susceptible to predation. These dynamics led to nonadditive effects of birds and ants: birds only reduced tended aphid species and total herbivore abundances on trees with ants, while ants only increased tended aphid species and total herbivore abundances in the absence of birds. Consequently, top predators in this system only influenced total herbivore abundance when they disrupted an ant-aphid mutualism.

Evaluation of insecticides for protecting Southwestern ponderosa pines from attack by engraver beetles (Coleoptera: Curculionidae: Scolytinae).

Insecticides that might protect pine trees from attack by engraver beetles (Ips spp.) have not been rigorously tested in the southwestern United States. We conducted two field experiments to evaluate the efficacy of several currently and potentially labeled preventative insecticides for protecting high-value ponderosa pine, Pinus ponderosa Dougl ex. Laws., from attack by engraver beetles. Preventative sprays (0.19% permethrin [Permethrin Plus C]; 0.03, 0.06, and 0.12% bifenthrin [Onyx]; and 1.0 and 2.0% carbaryl [Sevin SL] formulations) and systemic implants (0.875 g per capsule acephate [Acecap] and 0.650 g per capsule dinotefuran) were assessed on bolts (sections of logs) as a surrogate for live trees for a period of 13 mo posttreatment. The pine engraver, Ips pini (Say), was the most common bark beetle found attacking control and treated bolts, but sixspined ips, Ips calligraphus (Germar), and Ips lecontei Swain also were present. After approximately 13 mo posttreatment in one experiment, the spray treatments with 2.0% carbaryl, 0.19% permethrin, and 0.06 or 0.12% bifenthrin prevented Ips attack on the bolts at a protection level of > or = 70%. The acephate and dinotefuran systemic insecticides, and the 0.03% bifenthrin spray, provided inadequate (< or = 36%) protection in this experiment. For the other experiment, sprayed applications of 1.0% carbaryl, 0.19% permethrin, and 0.06% bifenthrin prevented beetle attack at protection levels of > or = 90, > or = 80, and > or = 70%, respectively, when bolts were exposed to Ips beetle attack for approximately 9-15 wk posttreatment. The sprays with 0.19% permethrin and 0.06% bifenthrin also provided > or = 90% protection when bolts were exposed for approximately 15-54 wk posttreatment. We concluded that under the conditions tested, 1.0 and 2.0% carbaryl, 0.19% permethrin, and 0.06 and 0.12% binfenthrin were acceptable preventative treatments for protecting ponderosa pine from successful engraver beetle attack for one entire flight season in the U.S. Southwest.

Host physiological condition regulates parasitic plant performance: Arceuthobium vaginatum subsp. cryptopodum on Pinus ponderosa.

Much research has focused on effects of plant parasites on host-plant physiology and growth, but little is known about effects of host physiological condition on parasite growth. Using the parasitic dwarf mistletoe Arceuthobium vaginatum subsp. cryptopodum (Viscaceae) and its host Pinus ponderosa, we investigated whether changes in host physiological condition influenced mistletoe shoot development in northern Arizona forests. We conducted two studies in two consecutive years and used forest thinning (i.e., competitive release) to manipulate host physiological condition. We removed dwarf mistletoe shoots in April, before the onset of the growing season, and measured the amount of regrowth in the first season after forest thinning (Study I: n=38 trees; Study II: n=35 trees). Thinning increased tree uptake of water and carbon in both studies, but had no effect on leaf N concentration or delta13C. Mistletoe shoot growth was greater on trees with high uptake of water and carbon in thinned stands than trees with low uptake in unthinned stands. These findings show that increased resource uptake by host trees increases resources to these heterotrophic dwarf mistletoes, and links mistletoe performance to changes in host physiological condition.