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Changes in Transpiration and Foliage Growth in Lodgepole Pine Trees Following Mountain Pine Beetle Attack and Mechanical Girdling ⇑ Robert M

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Changes in Transpiration and Foliage Growth in Lodgepole Pine Trees Following Mountain Pine Beetle Attack and Mechanical Girdling ⇑ Robert M Forest Ecology and Management 289 (2013) 312–317 Contents lists available at SciVerse ScienceDirect Forest Ecology and Management journal homepage: www.elsevier.com/locate/foreco Changes in transpiration and foliage growth in lodgepole pine trees following mountain pine beetle attack and mechanical girdling ⇑ Robert M. Hubbard , Charles C. Rhoades, Kelly Elder, Jose Negron USDA Forest Service, Rocky Mountain Research Station, 240 West Prospect Road, Fort Collins, CO 80526, United States article info abstract Article history: The recent mountain pine beetle outbreak in North American lodgepole pine forests demonstrates the Received 13 June 2012 importance of insect related disturbances in changing forest structure and ecosystem processes. Phloem Received in revised form 18 September 2012 feeding by beetles disrupts transport of photosynthate from tree canopies and fungi introduced to the Accepted 21 September 2012 tree’s vascular system by the bark beetles inhibit water transport from roots to canopy; the implications Available online 28 November 2012 of these processes for tree mortality are poorly understood. We hypothesized that the fungus must quickly disrupt tree water relations because phloem girdling, reported in other studies, requires much Keywords: longer than a year to cause mortality. We tested the hypothesis in lodgepole pine (Pinus contorta) by com- Blue stain fungi paring tree water use, foliar expansion and seasonal variation in predawn water potential on 8 mechan- Phloem Sap flow ically girdled trees, 10 control trees and 17 trees attacked by mountain pine beetle (Dendroctonous Pinus contorta ponderosae). Transpiration began to decline within ten days of beetle infestation; two months later, Dendroctonus ponderosae pre-dawn water potential had also dropped significantly as water transport to the canopy declined by 60% relative to healthy trees. There was no water transport or foliar expansion by beetle-infested trees the following year. Experimentally girdled trees continued to transpire, maintain leaf water potential and grow new foliage similar to healthy trees. Our data suggest that fungi introduced by bark beetles in this study are the primary cause of tree mortality following mountain pine beetle attack and signifi- cantly reduce transpiration soon after beetle infestation. Rapid decline and the eventual cessation of water uptake by infected trees have important implications for water and nutrient cycling in beetle impacted forests. Published by Elsevier B.V. 1. Introduction more temperate forests (Safranyik et al., 2010; Rice et al., 2007; Cullingham et al., 2011). Mountain pine beetle (Dendroctonus ponderosae Hopkins) coe- Bark beetles disrupt two basic life-sustaining transport pro- volved with conifer species and has been an important disturbance cesses trees they infest. Adult beetles consume phloem tissue in agent in North American pine forests for thousands of years. A to build egg galleries and developing larvae consume phloem for number of abiotic and biotic factors typically maintain populations food until maturity. Together, phloem feeding by adult and larval at endemic thresholds (Raffa et al., 2008). At low population levels, beetles contribute to some amount of phloem girdling, disrupting bark beetles usually attack stressed trees creating openings in for- the transport of photosynthate from the canopy to other tissues est stands that allow tree regeneration and dead trees to serve as within the tree. Bark beetles also carry a diversity of spores from habitat for wildlife. However, during the past decade and a half, four main genera of fungi, Ophiostoma, Ceratocystiopsis, Grosmannia mountain pine beetles are causing significant mortality in millions and Ceratocystis (Six and Wingfield, 2011) and a number of species of hectares of lodgepole pine forests that extend from western Can- in these groups have been shown to be phytopathogenic ada to the southern Rockies. The abundance of over mature stands, (Christiansen and Solheim, 1990; Yamaoka et al., 1995; Kim recent drought and warming winter temperatures has created con- et al., 2008). Once inside the tree, fungal spores introduced by bark ditions that support the current outbreak (Raffa et al., 2008). The beetles germinate and the spreading fungal hyphae penetrate possibility of further infestations are likely as beetles move into water conducting xylem tissue in the sapwood and block water alternate hosts such as jack pine (Pinus banksiana) in the boreal for- transport from the soil to the canopy (e.g. Ballard et al., 1984; ests of North America, and ponderosa pine (Pinus ponderosae)in Langstrom et al., 1993; Wullschleger et al., 2004). Both fungal infection of xylem tissue and phloem feeding by bark beetles have the potential to cause tree mortality. The link be- ⇑ Corresponding author. Tel.: +1 970 498 1260. tween phloem consumption by bark beetles and tree mortality has E-mail address: [email protected] (R.M. Hubbard). not been established, but mechanical girdling has been used to 0378-1127/$ - see front matter Published by Elsevier B.V. http://dx.doi.org/10.1016/j.foreco.2012.09.028 R.M. Hubbard et al. / Forest Ecology and Management 289 (2013) 312–317 313 examine tree and ecosystem carbon dynamics. In these studies, July 2006, we identified 36 lodgepole pine trees within a 30 m ra- girdled trees typically live for at least a growing season and often dius that showed no evidence of beetle activity and began monitor- longer before succumbing to the girdle treatment (Scott-Denton ing sap flux density on each tree using Granier style sap flow et al., 2006; Weintraub et al., 2007; Domec and Pruyn, 2008; Chen probes (see details below). Treatment trees had an average diame- et al., 2010). In contrast, experiments that inoculate trees with ter of 24.0 cm (±0.54 se) averaged 15.5 m (±0.3 se) in height and blue-stain fungi or that measured a transpiration response follow- had similar sapwood to leaf area ratios (0.080 cm2 mÀ2 ± 0.001 se). ing beetle infestation suggest that the fungal infection kills trees We randomly selected 24 of the 36 trees for the control and girdled relatively quickly (Yamaoka et al., 1995; Wullschleger et al., treatments and sprayed the stems of these trees with a wide spec- 2004). Although bark beetle fungal associates may not necessarily trum carbamate insecticide (SEVIN, Garden Tech Inc.) to protect support bark beetles in overwhelming tree defenses (Six and them against beetle attack. The insecticide was applied according Wingfield, 2011) the above studies suggest that disruption of pho- to the manufacture’s recommendation and care was taken not to tosynthate transport from the canopy and fungal infection of xy- excessively spray foliage. lem tissue may not be equal players in the eventual mortality of Bark beetle emergence began on July 17, 2006 within our study trees following mountain pine beetle infestation. area and by July 19 bark beetles had attacked eighteen of the treat- In spite of the importance of mountain pine beetle to the ecol- ment trees (including seven sprayed trees), as indicated by the ogy of North American pine forests, there has never been a study presence of abundant pitch tubes and boring dust on the ground, that attempted to simultaneously quantify changes in tree physiol- which are indicative of successful infestation. Consequently, we ogy induced by phloem feeding and fungal infection. Several stud- adjusted our sample size for each treatment by randomly selecting ies have examined changes in transpiration rates following pine non-attacked trees for the control (n = 10) and girdle (n = 8) treat- beetle infestations or inoculations with blue-stain fungi (e.g. ments and assigned the attacked trees to the beetle treatment Yamaoka et al., 1990; Wullschleger et al., 2004) while others have (n = 17). The girdled treatment was implemented late in the after- examined competitive interactions of different beetle species on noon on July 19 by carefully removing a 50 cm wide ring of bark phloem consumption, or attack densities of beetles relative to approximately 2 m above the ground (approximately 0.6 m above phloem carbohydrate concentrations (e.g. Miller and Berryman, the sap flow probes) using a sharp knife and draw blade. The bark 1986). Understanding the mechanisms behind tree mortality fol- peeled easily at the cambium allowing us to avoid injury to the xy- lowing beetle attack is important for development of control strat- lem. At the end of the study, we verified the presence (beetle in- egies as well as how the timing of mortality in trees and stands fested trees) or absence (control and girdled trees) of blue stain affects other ecosystem processes. Our goal in this study was to fungi in sapwood tissue of each treatment by extracting an incre- compare changes in water status and foliar growth of healthy trees, ment core from each tree and by visually examining the xylem tis- trees girdled to disrupt phloem transport, and trees attacked by sue below a 2 cm square section of bark. Blue stain fungal bark beetles and blue stain fungi. To accomplish this, we mechan- mycelium was present in the sapwood of all beetle infested trees ically removed phloem from the entire circumference of healthy and was absent in cores from the girdled and control trees. trees to simulate severe phloem feeding by bark beetles and com- pared transpiration, pre-dawn leaf water potential, leaf expansion 2.3. Environmental data and foliar nitrogen concentrations with beetle attacked and healthy trees over most of two growing
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