Forest Ecology and Management 291 (2013) 357366
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Forest Ecology and Management
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Adaptive variation in growth, phenology, cold tolerance and nitrogen fixation ofred alder (Alnus rubra Bong.)
R.B. Porter a, T. Lacourse b, B.J. Hawkins a,, A. Yanchuk ca Centre for Forest Biology, University of Victoria, PO Box 3020, STN CSC, Victoria, BC, Canada V8W 3N5b Department of Biology, University of Victoria, PO Box 3020, STN CSC, Victoria, BC, Canada V8W 3N5c Tree Improvement Branch, BC Ministry of Forests, Lands and Natural Resource Operations, PO Box 9518, STN PROV GOVT, Victoria, BC, Canada V8W 9C2
a r t i c l e i n f o
Article history:Received 27 August 2012Received in revised form 14 November 2012Accepted 16 November 2012Available online 7 January 2013
Keywords:Adaptive variationPhenotypic plasticityGenotype environmentTree improvementBritish Columbia
0378-1127/$ - see front matter 2012 Elsevier B.V. Ahttp://dx.doi.org/10.1016/j.foreco.2012.11.017
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a b s t r a c t
Red alder (Alnus rubra Bong.) is the most abundant deciduous tree on the Pacific coast of North Americaand its use as a timber species is increasing. To explore adaptive variation and genotype environmentinteractions in this species, we examine the pattern and degree of variation in physiological and growthtraits among 59 families of red alder, and relate this variation to the climates of family origin. Red alderfamilies from coastal British Columbia were grown in common garden experiments at two contrastingtest sites. We determined the degree of local adaptation among red alder families and the major climaticvariables driving adaptive variation in this species. Significant genetic variation among regions wasdetected in height, diameter, canopy cover, cold hardiness and nitrogen concentration of red alder fam-ilies. Differences in continentality and available moisture of the climate of origin explained most of theamong-family variation in autumn canopy cover, bud burst, and cold hardiness, whereas temperatureand length of the growing season of origin was associated with among-family differences in cold hardi-ness and growth. Families from northern, moist, coastal regions had earlier bud burst at the southern testsite, and less autumn canopy cover, lower nitrogen concentrations but higher nitrogen fixation, on aver-age, at both test sites. A trade-off between growth and cold hardiness of red alder families was clearlyevident, and family height at the southern test site was negatively correlated with cold hardiness,whereas there was a positive correlation at the northern test site. Red alder families vary in the degreeof phenotypic plasticity; however, our results show that most red alder families tested are relativelytightly adapted to their climate of origin and may perform sub-optimally if planted in a contrasting cli-mate. Phenology, cold hardiness, survival and height of tightly adapted families will be most affected byassisted migration or long-term climate change, but some families do not show strong adaptation to theirclimate of origin and will be more able to acclimate to deviations in climate.
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1. Introduction role and physiological attributes may result in differences in the
Many tree species are subject to great environmental variationin time and in space and consequently exhibit high levels of pheno-typic plasticity and genetic variation (Hamrick et al., 1992). Severaltree species native to the west coast of North America have a widedistribution over more than 25 of latitude, or 3000 km, and stud-ies of some of these species, in particular Douglas-fir (Pseudotsugamenziesii Mirb. Franco), have shown significant clinal variation ingrowth, phenology and physiological traits (Li and Adams, 1993;Aitken and Adams, 1995; ONeill et al., 2001; St Clair et al.,2005). Red alder (Alnus rubra Bong.) has a similarly widedistribution, but less attention has been given to variation in thehardwoods of western North America, which, typically, are compo-nents of early seral forest stages, have shorter lifespans thanassociated conifers and are deciduous. These contrasts in ecological
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plasticity of the hardwood species compared to conifers. Hamricket al. (1992) concluded that genetic diversity is greater in speciesfrom late successional stages, whereas Wehenkel et al. (2011)found the opposite. Our objective was to quantify adaptive varia-tion in key physiological attributes of red alder, the most abundanthardwood on the Pacific coast of North America (Burns andHonkala, 1990) and a valuable timber species.
Red alder is a fast-growing tree that achieves the largest size ofany species of the genus. It ranges from 34 N to 60 N latitude onthe west coast of North America, and is the most economicallyimportant broadleaf tree in the region. Apart from a few inlandpopulations in Washington and Idaho, red alder usually grows nofurther than 200 km from the coast and at elevations below1200 m (Xie et al., 2002). Red alder is shade-intolerant (Niinemetsand Valladares, 2006), colonizes recently disturbed sites andestablishes best on open sites in mineral soil (Harrington, 1996),thus it is part of the early stages of forest succession following
358 R.B. Porter et al. / Forest Ecology and Management 291 (2013) 357366
disturbance (Stettler, 1978). Red alder has many characteristicscommon to pioneer species (Bazzaz, 1979; Brzeziecki and Kienast,1994), including prolific, seed production, light-weight seed, rapidjuvenile growth and a short life span relative to late successionaltrees from the same region (Harrington, 1996). In a comparisonof 806 woody plants from the temperate northern hemisphere,red alder ranked as moderately tolerant of drought and waterlog-ging (Niinemets and Valladares, 2006), and it grows best on wetsites (Hook et al., 1987). Red alder is the only tree species of the Pa-cific west coast with the ability to fix atmospheric nitrogen, whichit does via a symbiotic association with the actinomycete Frankiafound within nodules formed on the trees roots.
Given red alders large range, adaptation to local climates is ex-pected, and geographic variation in phenology, cold hardiness andgrowth has been demonstrated over the latitudinal distribution ofthe species (DeBell and Wilson, 1978; Cannell et al., 1987; Xieet al., 1996). In British Columbia (B.C.), clinal differentiation ofheight reaction norms (Hamann et al., 2000) and ecophysiologicaltraits (Dang et al., 1994; Hamann et al., 2011) has been docu-mented along the B.C. coast. Genetic differentiation in allozymeshas been identified between Vancouver Island and mainland alderpopulations (Hamann et al., 1998, 2011; Xie et al., 2002), and theGeorgia Depression has been identified as an area of higher geneticdifferentiation based on height reaction norms (Hamann et al.,2000). In a common garden trial, clinal variation in phenologyand growth of red alder was found among populations collectedfrom transects along Washington and Oregon river drainages, withgrowth inversely related to elevation (Ager et al., 1993). Othercommon garden studies have shown significant genotype x envi-ronment interactions at both population and family levels (Xieet al., 1996; Hamann et al., 1998, 2000), which indicates that someprovenances and/or genotypes may have limited ability to accli-mate to contrasting environments.
Past studies of adaptive variation in red alder have focusedmainly on spatial trends in phenological and growth traits. Thereare no studies of which we are aware that survey genetic variationin nitrogen fixation in red alder and its relation to the climate offamily origin. In the past, there has been limited capability to relateadaptive variation in physiological traits of red alder to climaticvariables of family origin due to lack of regional climate data. Stud-ies of 3-year-old trees from western Washington and Oregon (Ageret al., 1993) and coastal B.C. (Hamann et al., 2000) related familygrowth, survival or phenology to climatic variables from the closestlong-term weather stations. More recently, (Hamann et al., 2011)used multivariate regression tree analysis to partition variationin growth and phenology of the same alder families we studiedbased on interpolated climate variables adjusted for elevation;however, that study was of 4-year-old trees on one test site. Webuild on the results of Hamann et al. (2011) using the most currenthigh-resolution climate data derived from geospatial interpolationof weather station data (Wang et al., 2012b) and 17-year-old aldertrees representing 59 families in two common garden experiments.Our study aimed to determine which growth, phenological andphysiological attributes exhibit the greatest degree of variationamong families of red alder established on two contrasting testsites, and to relate this variation to the climate of family origin.
2. Materials and methods
2.1. Measurements of growth, phenology and physiology
In the spring of 1994, the B.C. Ministry of Forests establishedtwo, long-term, red alder provenance-progeny test trials, one onsouthern Vancouver Island, near Bowser (49290 N, 124400 W,50 m asl) and the other on B.C.s north coast, near Terrace
(54270 N, 12880 W, 200 m asl) (Fig. 1). The tests were establishedwith one-year-old seedlings planted at 3 m spacing in a split-plotdesign, with 41 provenances common to both sites designated asthe main plots and two to five open-pollinated families within eachprovenance as the subplots (Xie, 2008). Subplots contained fivetrees per family planted in a row, and three blocks of five-treerow subplots were planted at each site, but Block 1 at Bowserwas not included in this study due to flooding.
From the 116 families common to both test sites, 59 familiesrepresenting the geographic range of the species in B.C. were se-lected for further study with the aim to choose families from acrossthe range of height growth on the two sites (assessed by the differ-ence in 10-year height between the two sites) (Table 1, Fig. 1). Treeheight at Terrace (labeled htTR) and Bowser (htBW), diameter at1.3 m (dbhTR, dbhBW) and number of stems > 5 cm diameter at50 cm height (stemsTR, stemsBW) of the trees in each family weremeasured in one block at Terrace on April 2022, 2010 and in twoblocks at Bowser on May 13, 2010. Survival was measured as themean proportion of trees surviving out of the five trees plantedper family per block in blocks 1 and 2 at Bowser (survBW), andall three blocks in Terrace (survTR). Bud burst was assessed foreach tree from the 59 families in two blocks at Bowser on March20, 2010 (bbBWMar10), April 10, 2010 (bbBWApr10) and April11, 2011 (bbBWApr11), and in three blocks at Terrace on April21, 2010 (bbTRApr10). The state of the terminal bud was assessedusing binoculars. Buds were scored on a scale of 14 (modifiedfrom Murray et al., 1989), where: 1 = not swollen, 1.5 = slightlyswollen, 2 = swollen, 2.5 = swollen with distinct asymmetricalbulge, 3 = green foliage showing, 3.5 = emergent foliage, and4 = expanded foliage. As an index of leaf fall at the end of the grow-ing season, canopy cover, defined as the percent of sky occupied byleaves for an individual tree canopy, was visually estimated to thenearest 10% for trees in the 59 families in two blocks on each siteon September 23 (ccBWSep) and November 2, 2010 (ccBWNov) atBowser, and October 9, 2010 at Terrace (ccTROct).
Cold hardiness was assessed by electrolyte leakage after con-trolled freezing for 50 families (Table 1) sampled at Bowser on Sep-tember 28 (iiBWSep), and December 1 (iiBWDec), 2010, andJanuary 29 (iiBWJan), and March 25, 2011 (iiBWMar), and at Ter-race on October 15, 2010 (iiTROct). At each collection, two treesper family were sampled in each of two blocks. Branch ends werecollected from the mid to upper canopy on the south side of eachtree using a 10 m pole pruner, and stored on ice for transport tothe laboratory. Samples were rinsed in distilled water and cut into0.5 cm sections, excluding buds. Six branch sections were added toeach of four scintillation vials with 0.2 mL of distilled water. Thefour replicate vials per tree were allocated to each of three freezingtemperatures and one refrigerated control. Samples were frozen ina programmable freezer (Caltech Scientific Ltd., Richmond, B.C.;Lab Chest Freezer Model 8458, Forma Scientific, Walton, MA) to8, 12, or 16 C in September and October, 12, 16 or20 C in December, 16, 20 or 24 C in January, and 12 or20 C in March. Samples were cooled at 5 C h1 and held at eachtest temperature for 1 h prior to removal to a 4 C refrigerator,where they remained overnight. The following morning, 10 mL ofdistilled water was added to each vial, and vials were shaken atroom temperature for 18 h at 75 rpm. Conductivity of the sampleswas measured (Jenway Ltd. 4020 Conductivity Meter, Stafford-shire, UK), and then samples were heated to 100 C, shaken over-night and conductivity remeasured. Index of injury (ii) wascalculated for each tree at each freezing temperature using the for-mula of Flint et al. (1967), where a high index of injury indicateslow cold tolerance:
ii 100Rt R0=1 R0;Rt Lt=Lk;R0 Lt=Ld; and
Haida Gwaii (QCI)Northern MainlandCentral CoastNorthern Vancouver Is.Western Vancouver Is.Georgia Depression
Fig. 1. Location of red alder provenances (circles) and Terrace (TR) and Bowser (BW) test sites (stars) in British Columbia, Canada. (For interpretation of the references tocolour in this figure legend, the reader is referred to the web version of this article.)
R.B. Porter et al. / Forest Ecology and Management 291 (2013) 357366 359
Lt is the conductance of sample frozen at temperature t, Lk the con-ductance of frozen, heat-killed sample, L0 the conductance of refrig-erated, unfrozen sample, and Ld is the conductance of unfrozen,heat-killed sample
Water use efficiency (WUE) of 50 families (Table 1) was as-sessed by stable carbon isotope analysis (o13CTR, o13CBW), and rel-ative proportion of nitrogen (N) fixed from the atmosphere wasassessed by stable N isotope analysis (o15NTR, o15NBW) on budsamples. o13C is positively correlated with both intrinsic andlong-term WUE in trees (Sun et al., 1996), with a more negativeo13C indicating lower WUE. o15N is negatively correlated with ratesof N fixation (Shearer and Kohl, 1986). Due to 15N enrichment ofsoils by edaphic processes, plants with higher rates of N fixationhave less enrichment and a more negative o15N than plants...