Forest Ecology and Management 291 (2013) 357–366

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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 c

a 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

⇑ Corresponding author. Tel.: +1 250 721 7117; faxE-mail address: bhawkins@uvic.ca (B.J. Hawkins).

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.

� 2012 Elsevier B.V. All rights reserved.

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; O’Neill 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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: +1 250 721 6611.

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) 357–366

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 tree’s roots.

Given red alder’s 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 (49�290 N, 124�400 W,50 m asl) and the other on B.C.’s north coast, near Terrace

(54�270 N, 128�80 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 20–22, 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 1–4 (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) to�8, �12, or �16 �C in September and October, �12, �16 or�20 �C in December, �16, �20 or �24 �C in January, and �12 or�20 �C in March. Samples were cooled at 5 �C h�1 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 ¼ 100ðRt � R0Þ=ð1� R0Þ;Rt ¼ Lt=Lk;R0 ¼ Lt=Ld; and

ð1Þ

100 km

Haida Gwaii (QCI)Northern MainlandCentral CoastNorthern Vancouver Is.Western Vancouver Is.Georgia Depression

TR

BW

62

686361

5958 57

53 56

5455

52

48

37 3532

30

2114

415

23

68

13

4331

11

44 45

5051

71•6465

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) 357–366 359

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 withlower rates or no N fixation in the same environment.

Bud samples for N concentration (%NTR, %NBW), 15N, and 13Canalysis were collected from the mid to upper canopy on the southside of each of two trees per family per block for two blocks atBowser on September 21–22, 2010 and two blocks at Terrace onOctober 7–8, 2010. Samples were oven dried at 50 �C to constantweight, homogenized using a ball mill, and 4.0 mg subsampleswere packaged in tin capsules and analyzed for o13C and o15N usingan elemental analyzer interfaced to a continuous flow isotope ratiomass spectrometer at the University of California, Davis Stable Iso-tope Facility. The isotopic composition of the sample was calcu-lated as:

@xð‰Þ ¼ ðRsample � Rstandard=RstandardÞ � 1000;

where Rsample and Rstandard are the ratios of heavy:light isotope inthe sample and a standard, respectively. Soil texture and slope were

relatively uniform within each site, therefore o13C or o15N valueswere compared by site.

2.2. Climate data

Climate data for the period 1961–1990 for each family’s loca-tion of origin were obtained from ClimateWNA (Wang et al.,2012b). ClimateWNA extracts and downscales PRISM (Daly et al.,2002) monthly data and calculates seasonal and annual climatevariables based on the latitude, longitude and elevation of familyorigin (ClimateWNA, 2012). Directly calculated climate variablesused in analyses were: mean annual temperature (MAT), meancoldest month temperature (MCMT), mean warmest month tem-perature (MWMT), continentality (TD = MWMT–MCMT), mean an-nual precipitation (MAP) and mean May-to-Septemberprecipitation (MSP). Derived climate variables used included: de-gree-days above 5 �C (DD5), number of frost-free days (NFFD),beginning date of frost free period (bFFP), ending date of frost freeperiod (eFFP), reference atmospheric evaporative demand (Eref)and climatic moisture deficit (CMD) (Wang et al., 2012b).

2.3. Regions

To explore regional trends in the data, families were assigned tosix regions based on geographic provenance (Table 1). The regionswere: Haida Gwaii, all families from these islands; Northern Main-land, mainland families from north of 52� N and west of 131� W;Central Coast, mainland families from 51�300 N–52�300 N and eastof 127� W; Northern Vancouver Island, families from VancouverIsland north of 50�300 N; Western Vancouver Island, families fromthe windward side of the Vancouver Island Ranges; and Georgia

Table 1Provenance and family identifiers and name, location of origin, regiona and the 10-year difference in height ranking between sites (Bowser–Terrace) of 59 red alder familiesplanted at two field sites. Family number is the combination of provenance and family identifiers. Families starred with an asterisk were not included in all assessments or RDAanalysis.

Prov. Fam. Provenance name Latitude (�N) Longitude (�W) Elev. (m) Region Diff. in ht. rank

4 4 Port Renfrew 48�360 124�140 20 WVI 134 5 Port Renfrew 48�360 124�140 20 WVI 116 1⁄ Klanawa #2 48 46 124 58 40 WVI 538 3 Nitinat Flats 48�500 124�400 30 WVI �48 4 Nitinat Flats 48�500 124�400 30 WVI 81

11 3 Sarita Lake 48�550 124�520 40 WVI �511 4 Sarita Lake 48�550 124�520 40 WVI �5813 3 Betw. the Lakes 48�580 124�430 200 WVI �7413 5 Betw. the Lakes 48�580 124�430 200 WVI �814 2 Ucluelet 49�000 125�340 40 WVI 5915 2 Cassidy 49�030 123�560 107 GD 6415 8 Cassidy 49�030 123�560 107 GD 1821 5 Britannia Creek 49�070 123�070 660 GD 1423 5⁄ China Creek #2 49 10 124 41 400 GD 830 1⁄ Indian River 49�340 122�560 190 GD 5430 3⁄ Indian River 49�340 122�560 190 GD 430 4 Indian River 49�340 122�560 190 GD 030 5 Indian River 49�340 122�560 190 GD 3231 2 Pender Harbor 49�390 124�020 150 GD 331 3 Pender Harbor 49�390 124�020 150 GD �4432 1⁄ Mamquam River 49�430 123�070 100 GD 7632 2 Mamquam River 49�430 123�070 100 GD 9335 1 Culliton Creek 49�530 123�110 250 GD 8235 2⁄ Culliton Creek 49�530 123�110 250 GD 6537 1 Woss #2 49�580 126�150 1000 WVI �5037 5 Woss #2 49�580 126�150 1000 WVI �5443 5 Roberts Lake 50�130 125�330 700 GD �6044 1 Bigtree #1 50�140 125�430 250 GD �745 2 Bigtree #2 50�140 125�430 300 GD �845 3 Bigtree #2 50�140 125�430 300 GD 448 2 Ronning Main 50�360 128�150 30 NVI 648 4 Ronning Main 50�360 128�150 30 NVI 350 1 San Josef Main 50�400 128�040 20 NVI �1350 4 San Josef Main 50�400 128�040 20 NVI 2051 2 NE 62 50�430 127�590 170 NVI �1051 3 NE 62 50�430 127�590 170 NVI 1652 1 Kingcome Inlet 51�300 126�080 30 CC �5353 2 Poole Inlet 52�210 131�210 1 HG �6653 3 Poole Inlet 52�210 131�210 1 HG 1154 4 Hagensborg 52�220 126�350 40 CC �5354 5 Hagensborg 52�220 126�350 40 CC �655 3 Bachelor Bay 52�220 126�550 30 CC 1456 1 Salloomt River 52�260 126�330 150 CC �9656 2 Salloomt River 52�260 126�330 150 CC �9956 4 Salloomt River 52�260 126�330 150 CC �10057 3 Copper Bay 53�070 131�400 10 HG �758 5⁄ Channel 53�080 132�150 20 HG �1359 2⁄ Rennell Sound 53�220 132�270 100 HG 6459 3 Rennell Sound 53�220 132�270 100 HG 7961 3 Masset 54�030 132�000 10 HG �2861 5⁄ Masset 54�030 132�000 10 HG �1162 5 Kitimat 54�150 128�300 60 NM �4963 2 Snow Creek 54�150 129�330 10 NM �5863 4 Snow Creek 54�150 129�330 10 NM �6764 1⁄ Rainbow Summit 54�150 130�020 160 NM 2165 4⁄ Prince Rupert 54�160 130�160 46 NM �2268 2 Shames River 54�260 128�550 100 NM �1171 3 Oliver Lake 54�170 130�160 50 NM �8071 4 Oliver Lake 54�170 130�160 50 NM �53

a Region abbreviations: GD = Georgia Depression, WVI = Western Vancouver Island, NVI = Northern Vancouver Island, CC = Central Coast, NM = Northern Mainland,HG = Haida Gwaii.

360 R.B. Porter et al. / Forest Ecology and Management 291 (2013) 357–366

Depression, families from the southern mainland and eastern Van-couver Island. These regions are similar to those defined byHamann et al. (2011) based on multivariate regression tree analy-sis of height, survival, bud burst, leaf drop, wilting and allozymefrequencies at the Bowser test site; however, we defined NorthernVancouver Island as a separate region based on its unique climate,and grouped southeastern Vancouver Island and south mainlandfamilies into one region, the Georgia Depression, based on biogeo-climatic similarity and the results of Hamann et al. (2000).

2.4. Statistical analysis

Redundancy analysis (RDA) was used to relate trends in 10growth and physiological traits of 48 families (Table 1, Supplemen-tary Data Table 1), planted at both Terrace and Bowser, to their cli-mate of origin (Supplementary Data Table 2), i.e., to determine thenature and degree of variation in traits and performance that canbe explained by differences in the climate of seed source locations.The axes of the RDA represent gradients in family traits, con-

R.B. Porter et al. / Forest Ecology and Management 291 (2013) 357–366 361

strained by the climate of origin data. RDA was appropriate for di-rect gradient analysis because gradient lengths determined bydetrended correspondence analysis (DCA) were less than 0.5 SDunits (ter Braak, 1995). RDA was conducted after normalizationto unit variance, which was done to stabilize the variance and toaccount for differences in measurement units and scales. The sta-tistical significance of the association between the growth andphysiological traits and the climate of origin data was tested with9999 Monte Carlo permutations at P < 0.05. DCA and RDA wereconducted using CANOCO 4.5 (ter Braak and Smilauer, 2002).

Growth and physiological data were also analyzed as mixed lin-ear models (PROC MIXED, REML estimation method, SAS InstituteInc., Cary, NC) to examine which traits contributing to the variationshown in the RDA analysis differed significantly among regions andfamilies. In the models, region was considered as an independent,fixed effect (n = 6) with family as a random effect (n = 50 or 59)nested within the fixed effect of region. Site (n = 2), block (n = 2)and their associated interactions were specified as random terms.Freezing temperature (n = 2 or 3) was considered a fixed factor inthe analyses of cold hardiness. Survival data was arcsin squareroottransformed prior to analysis. All other data was normally distrib-uted. Regional means were compared using least significant differ-ence tests. Best linear unbiased prediction (BLUP) was used toobtain parameter estimates associated with family. Family meanswithin cold hardiness, bud burst and canopy cover data sets werecorrelated for dates and sites using PROC CORR of SAS.

3. Results

3.1. Redundancy analysis

RDA analysis relating the growth and physiological traits of redalder families to the climate of their origin was statistically signif-icant (9999 Monte Carlo permutations, P = 0.0001). RDA axes 1 and2 account for 21.2% and 11.9% of the total variation, respectively(Fig. 2). Correlation between the families’ traits and their climateof origin are high on both RDA axes 1 (92.8%) and 2 (85.3%).

RDA axis 1 (Fig. 2) is correlated most strongly with continental-ity (TD), evaporative demand (Eref), and moisture deficit (CMD).This axis shows a trade-off between early family bud burst at Bow-ser, which has positive loadings, and more autumn canopy coverand higher family N fixation at both Bowser and Terrace, whichhave negative loadings (Fig. 2A). In general, families are dividedon RDA axis 1 along a longitudinal gradient, separating HaidaGwaii and Northern Vancouver Island families from those in theGeorgia Depression and on the Central Coast, which have positiveand negative loadings, respectively (Fig. 2B).

RDA 2 is correlated most strongly with temperature (MAT,MCMT), growing degree-days above 5 �C (DD5), and length of thegrowing season (NFFD, eFFP, bFFP). This axis separates high familycold hardiness at both test sites, and survival, early bud burst, andgrowth at Terrace from low family cold hardiness at both test sitesand height at Bowser (Fig. 2A). RDA 2 represents a latitudinal gra-dient that divides Northern Mainland, Central Coast and HaidaGwaii families from those from the south, i.e., Western VancouverIsland and Georgia Depression (Fig. 2B).

Canopy cover, bud burst, cold hardiness, growth and Terracesurvival account for most of the variation in the growth and phys-iological data, whereas the number of stems, water use efficiency(o13C), Bowser survival and measures of N account for less of thetotal variation (Fig. 2A). N fixation is generally higher in familiesfrom cool, moist regions. In general, physiological attributes offamilies appear to be closely tied to their climate of origin, butthere are also a few families from the Georgia Depression, WesternVancouver Island, and the Central Coast, with scores near the cen-

ter of the RDA biplot (Fig. 2B), that show less variability in all traitsin relation to their climate of origin. For the most part, familiesfrom the same region occupy similar space in the RDA ordination(Fig. 2B), with some regions such as Haida Gwaii more tightly clus-tered than others, e.g., Georgia Depression. Families from OliverLake (Provenance 71) are more similar in their growth and physi-ological traits to families from Haida Gwaii than to other familiesfrom the Northern Mainland and are associated more strongly withvariation on RDA axis 1 (i.e., continentality and available moisture)than RDA axis 2 (i.e., temperature and growing season length).

3.2. Mixed model analysis

The phenological characters of bud burst and autumn canopycover drive variation on the first axis of the RDA analysis (Fig. 2).While there were no significant regional differences in bud burst,families from the Central Coast and Western Vancouver Islandtended to have the least advanced bud burst, on average, on alldates of assessment (Table 2). Families within regions differed sig-nificantly in bud burst stage in April of both years at Bowser(Table 3). Mean family bud burst values were positively correlatedamong all April assessments (P 6 0.007, r P 0.39), thus familiesthat burst bud early or late, did so on both sites and in both years.Autumn canopy cover differed significantly among regions andamong families within region on all dates of assessment (Table 4).In September at the Bowser site and in October at Terrace, familiesfrom the Central Coast and Georgia Depression had the greatestcanopy cover, thus the latest leaf fall, and families from NorthernVancouver Island and Haida Gwaii had the earliest leaf fall(Table 2). In November at Bowser, families from the GeorgiaDepression and Western Vancouver Island had the latest leaf falland Northern Vancouver Island, the earliest (P 6 0.05) (Table 2).Mean family canopy cover values were positively correlatedamong all assessments (P 6 0.0001, r P 0.57), thus families thathad late or early leaf fall in the autumn did so on both sites.

Cold hardiness contributed to a large degree of variation in thephysiological data, and cold hardiness varied significantly amongregions and among families within regions in almost all analyses(Table 5). In all five cold hardiness assessments, families fromthe Central Coast and Northern Mainland were the most cold hardy(P 6 0.05) (Table 2). Mean family indices of injury were positivelycorrelated among all dates and locations (Table 6), thus the mostand least cold hardy families retained their ranking throughoutthe winter on both sites.

There were no significant differences in height, diameter or sur-vival among regions or among families within regions when datafrom the two sites were analyzed together, however, significantFamily(Region) � Site interactions existed for height and diameter(Table 7). When analyzed separately by site, region had a signifi-cant effect for height and diameter on both sites, and for survivalat Terrace (Table 8). Families from Haida Gwaii consistently wereshortest and had the smallest diameter on both sites (P 6 0.05)(Table 2). Families from the Georgia Depression and Northern Van-couver Island were tallest at Bowser, and families from the North-ern Mainland and Central Coast were the tallest and had thegreatest diameter and survival at Terrace (P 6 0.05) (Table 2). Thisindicates a trade-off between growth and cold hardiness, which issupported by the RDA (Fig. 2A), and indeed, mean family height atBowser was positively correlated with index of injury (taller fami-lies were least cold hardy, iiBWJan r = 0.47, P = 0.0008), but heightat Terrace was negatively correlated with index of injury (tallerfamilies were most cold hardy, iiTROct r = 0.37 P = 0.009). A plotof the best linear unbiased predictions of family height shows fam-ilies from Mamquam River (321, 322), Bigtree (441) and ShannonRiver (682) had superior height growth on both sites whereas

(A) (B)

Fig. 2. Redundancy analysis (RDA) ordination of (A) growth, phenological and physiological traits and (B) climate of origin variables for 48 red alder families from 30provenances, plotted on the first and second RDA axes, which account for 21.2% and 11.9% of the total variation, respectively. Arrow lengths in (B) indicate the correlationbetween climate of origin variables and ordination axes. See Methods for abbreviations of growth, phenological, and physiological traits in (A) and climatic variables in (B).Provenances are color-coded by region and labeled in (B). For provenances with more than one family, families from the same provenance occupy the same positions in theRDA biplot.

Table 2Regional means (±S.E.) of growth and physiological variables measured at Bowser (BW) and Terrace (TR). Measures include: index of bud burst, canopy cover (%), cold hardiness,height (ht) (m), diameter at 1.3 m (dbh) (cm), number of stems, survival, percent bud nitrogen (%N), 15N stable isotope ratio (o15N) and 13C stable isotope ratio (o13C).

Georgia Depression Western Vancouver Island Northern Vancouver Island Central Coast Northern Mainland Haida Gwaii

Bud burstbbBWMar10 2.67 ± 0.02 2.59 ± 0.03 2.73 ± 0.03 2.58 ± 0.03 2.72 ± 0.03 2.76 ± 0.03bbBWApr10 3.18 ± 0.02 3.10 ± 0.03 3.22 ± 0.03 3.03 ± 0.02 3.28 ± 0.03 3.23 ± 0.03bbTRApr10 3.09 ± 0.02 3.03 ± 0.02 3.03 ± 0.02 3.07 ± 0.02 3.16 ± 0.03 3.09 ± 0.03bbBWApr11 3.07 ± 0.03 2.95 ± 0.02 3.12 ± 0.03 2.95 ± 0.03 3.09 ± 0.03 3.05 ± 0.03

Canopy coverccBWSep 57.7 ± 1.2 56.5 ± 1.3 41.2 ± 1.6 63.7 ± 1.4 51.6 ± 1.9 50.0 ± 2.0ccBWNov 48.1 ± 1.0 38.5 ± 1.5 22.1 ± 1.9 51.3 ± 1.3 39.1 ± 2.0 21.9 ± 1.3ccTROct 36.1 ± 1.2 35.1 ± 1.3 17.2 ± 1.5 26.9 ± 1.7 22.1 ± 1.5 23.7 ± 1.6

Cold hardinessiiBWSep 42.9 ± 1.9 45.2 ± 2.3 36.6 ± 2.7 32.9 ± 2.5 31.2 ± 2.5 39.1 ± 3.1iiTROct 21.6 ± 1.2 23.7 ± 1.2 22.6 ± 1.2 15.0 ± 1.2 14.6 ± 1.2 25.3 ± 1.2iiBWDec 20.2 ± 0.8 19.9 ± 0.8 20.3 ± 1.4 15.9 ± 0.7 16.8 ± 0.7 18.6 ± 1.1iiBWJan 28.2 ± 0.7 26.5 ± 0.8 32.8 ± 2.5 18.1 ± 0.7 21.3 ± 0.7 22.4 ± 1.1iiBWMar 45.5 ± 1.1 42.2 ± 1.4 42.5 ± 1.9 27.9 ± 1.1 35.7 ± 0.9 36.7 ± 2.5

Growth & survivalhtBW 11.8 ± 0.2 11.1 ± 0.2 11.8 ± 0.3 9.9 ± 0.2 10.8 ± 0.2 9.8 ± 0.2htTR 11.2 ± 0.2 10.6 ± 0.1 10.2 ± 0.2 12.2 ± 0.3 12.4 ± 0.2 9.3 ± 0.3dbhBW 13.5 ± 0.2 12.8 ± 0.3 12.9 ± 0.4 12.1 ± 0.2 12.1 ± 0.4 10.7 ± 0.3dbhTR 12.9 ± 0.2 12.8 ± 0.3 12.4 ± 0.3 14.6 ± 0.3 13.8 ± 0.3 11.6 ± 0.4stemsBW 1.1 ± 0 1.0 ± 0.0 1.0 ± 0 1.1 ± 0.01 1.0 ± 0 1.2 ± 0.01stemsTR 2.6 ± 0.01 2.5 ± 0.01 2.0 ± 0.02 2.5 ± 0.02 2.3 ± 0.02 2.2 ± 0.01survBW 74.4 ± 2.9 73.6 ± 4.7 81.7 ± 6.0 67.1 ± 8.6 70.0 ± 6.3 77.5 ± 6.3survTR 57.8 ± 3.9 60.6 ± 5.6 62.2 ± 6.4 80.0 ± 5.2 82.2 ± 7.5 64.1 ± 6.9

Nitrogen%NBW 1.82 ± 0.03 1.79 ± 0.02 1.75 ± 0.03 1.84 ± 0.03 1.74 ± 0.03 1.67 ± 0.03%NTR 1.93 ± 0.02 1.85 ± 0.02 1.60 ± 0.04 1.93 ± 0.04 1.86 ± 0.02 1.70 ± 0.04o15NBW �2.74 ± 0.12 �2.42 ± 0.15 �3.02 ± 0.19 �2.68 ± 0.17 �2.85 ± 0.16 �2.90 ± 0.20o15NTR �1.76 ± 0.11 �1.88 ± 0.12 �2.49 ± 0.23 �2.08 ± 0.17 �2.02 ± 0.15 �2.34 ± 0.18

Carbono13CBW �26.17 ± 0.20 �26.11 ± 0.18 �26.48 ± 0.27 �25.78 ± 0.21 �26.13 ± 0.29 �26.81 ± 0.42o13CTR �28.72 ± 0.23 �29.33 ± 0.25 �29.35 ± 0.37 �28.84 ± 0.35 �29.22 ± 0.38 �29.30 ± 0.37

362 R.B. Porter et al. / Forest Ecology and Management 291 (2013) 357–366

Poole Inlet (533) and Copper Bay (573) families had exceptionallypoor height growth (Fig. 3).

Although percent bud N and o15N made a relatively smallcontribution to the overall variation among families (Fig. 2) andusually did not differ significantly among regions or families

(Table 9), region did significantly affect percent bud N on the Ter-race site (Table 9). On both sites, families from the Central Coastand Georgia Depression had the highest N concentrations in budswhile families from Haida Gwaii and Northern Vancouver Islandhad among the lowest bud N concentrations (Table 2). Family

Table 3F value of fixed effects and covariance parameter estimates of random effects (italics),and their respective significance levels from mixed model analyses of bud burst onthe Bowser (BW) or Terrace (TR) sites in March or April or 2010 and 2011.

bbBWMar10 bbBWApr20 bbTRApr10 bbBWApr11

Region(F value) 2.82 2.52 2.30 1.93Family(region) 0.0031 0.0147*** 0.0017 0.009*

Block 0.0002 0.0006 0.0001 0.0001Region � block 0.0004 0 0 0.0008Family(region) � blk 0.0043 0.0026 0.0054* 0.0037Residual 0.0607*** 0.0499*** 0.037*** 0.065***

+ Pr > F or Pr Z 6 0.05.* Pr > F or Pr Z 6 0.01.⁄⁄ Pr > F or Pr Z 6 0.001.*** Pr > F or Pr Z 6 0.0001.

Table 4F value of fixed effects and covariance parameter estimates of random effects (italics),and their respective significance levels for mixed model analyses of canopy cover onthe Bowser (BW) or Terrace (TR) sites in September, October or November, 2010.

ccBWSep ccBWNov ccTROct

Region 6.17+ 9.20* 22.55***

Family(region) 14.33* 37.80** 39.23**

Block 1.57 1.65 0.97Region � block 5.07 0 0.18Family(region) � blk 41.94** 10.03 10.26Residual 131.00*** 130.92*** 171.83***

+ P > F or Pr Z 6 0.05.* P > F or Pr Z 6 0.01.** P > F or Pr Z 6 0.001.*** P > F or Pr Z 6 0.0001.

Table 5F value of fixed effects and covariance parameter estimates of random effects (italics),and their respective significance levels for mixed model analyses of cold hardiness onthe Bowser (BW) or Terrace (TR) sites in September, October or December 2010, orJanuary and March 2011.

iiBWSep iiTROct iiBWDec iiBWJan iiBWMar

Region 5.24+ 2.41* 3.38** 2.67 8.15+

Temperature 1197.97** 74.28* 796.58** 138.88* 700.53+

Region � temp 2.75 2.69 3.90* 0.90+ 5.94**

Family(region) 2.35 11.37+ 4.31 12.54 3.88Family(region) � temp 0 0 0 0 0Block 0.471 1.36 0.46 0.51 3.73Region � block 4.77** 9.77** 0.18 8.27 0Temp � block 0 3.25 0 0 0.51Family(region) � blk 41.88** 22.97** 3.30* 26.94* 35.40**

Residual 95.97*** 70.03*** 19.11*** 93.00*** 82.12***

+ P > F or Pr Z 6 0.05.* P > F or Pr Z 6 0.01.** P > F or Pr Z 6 0.001.*** P > F or Pr Z 6 0.0001.

Table 6Pearson correlation coefficients (r) and P-values (italics) for mean family index ofinjury measured at Bowser and Terrace over the winter of 2010–2011.

iiTROct iiBWDec iiBWJan iiBWMar

iiBWSep 0.5271 0.5302 0.2933 0.56150.0001 0.0001 0.0430 <0.0001

iiTROct 0.2887 0.5263 0.34920.0466 0.0001 0.0150

iiBWDec 0.3161 0.44730.0286 0.0014

0.47770.0006

Table 7F value of fixed effects and covariance parameter estimates of random effects (italics),and their respective significance levels for mixed model analyses of height, diameterat 1.3 m, number of stems and survival.

Height Diameter Stems Survival

Region 0.98 1.61 0.99 0.22Family(region) 0.04 0.38 0.007 0Site 0 0.001 0.79 0Block(site) 0.77 0.21 0.04 0Region � site 0.77 0.51 0 0Region � block (site) 0.03 0 0.06+ 0.03Family(region) � site 0.90** 0.74+ 0.05 0.02Residual 2.41*** 8.01*** 1.32*** 0.09***

+ P > F or Pr Z 6 0.05.⁄ P > F or Pr Z 6 0.01.** P > F or Pr Z 6 0.001.*** P > F or Pr Z 6 0.0001.

Table 8F value of fixed effects and covariance parameter estimates of random effects (italics),and their respective significance levels for mixed model analyses of height (ht),diameter at 1.3 m (dbh) and survival (surv) measured at the Bowser (BW) and Terrace(TR) sites.

htBW htTR dbhBW dbhTR survBW survTR

Region 4.91+ 6.05** 4.88+ 3.79+ 0.19 3.37+

Family(region) 0.29 0.87* 1.01* 0.58 0.01 0Block 1.47 – 0.16 – 0 0Region � block 0 – 0 – 0.02 0Family(region) � blk 1.52*** – 1.80 – 0 0.01Residual 1.74*** 2.05*** 6.14*** 7.97*** 0.07*** 0.09

+ P > F or Pr Z 6 0.05.* P > F or Pr Z 6 0.01.** P > F or Pr Z 6 0.001.*** P > F or Pr Z 6 0.0001.

R.B. Porter et al. / Forest Ecology and Management 291 (2013) 357–366 363

mean o15N was positively correlated with percent bud N on bothsites (BW r = 0.577, P 6 0.0001; TR r = 0.555, P 6 0.0001), thus fam-ilies with more N obtained from N fixation tended to have lower Nconcentrations in buds. In conjunction with high bud N concentra-tion, families from Haida Gwaii and Northern Vancouver Islandalso derived the greatest proportion of N from fixation on bothsites, on average (Table 2). Families did not differ significantly ino13C.

Fig. 3. Best linear unbiased predictions of red alder family height at Bowser andTerrace. Cross-hairs indicate mean height at Bowser (vertical) and Terrace(horizontal). Families are colour-coded by region. Exceptional families are notedby number.

Table 9F values of fixed effects and covariance parameter estimates of random effects(italics), and their respective significance levels for mixed model analyses of percentbud nitrogen (%N) and o15N measured at the Bowser (BW) and Terrace (TR) sites.

%NBW %NTR o15NBW o15NTR

Region 2.25 4.04+ 2.36 1.97Family(region) 3.29 e�7 1.29 e�7 0 0.08Block 0 0 0.59 0Region � block 0 4.32 e�7 0 0.01Family(region) � blk 0 1.12 e�6 0.02 0Residual 3.13 e�6 3.39 e�6 0.47*** 0.68***

⁄ P > F or Pr Z 6 0.01.+ P > F or Pr Z 6 0.05.⁄⁄ P > F or Pr Z 6 0.001.*** P > F or Pr Z 6 0.0001.

364 R.B. Porter et al. / Forest Ecology and Management 291 (2013) 357–366

4. Discussion

Although red alder exhibits less allozymic diversity than mostlong-lived woody species (Xie et al., 2002), quantitative geneticvariation is abundant in the species. Our analysis shows clear evi-dence that red alder families are adapted to the climatic conditionsof seed origin. In general, the RDA ordination separated red alderfamilies from the six regions according to contrasting responsesin growth and physiology between the two test sites that wereassociated with climate of family origin. Of the climatic variablesincluded in the redundancy analysis, differences in continentalityand available moisture explained the most variation in physiolog-ical traits between families grown at the two test sites. Significantdifferences existed among families from the six regions in manyphysiological and growth traits which contrasts with patterns ofallozymic variation, where a separation of mainland and islandregions explains a large majority of the variation (Xie et al.,2002; Hamann et al., 1998).

Along RDA axis 1, families from less continental and moister re-gions (e.g., Haida Gwaii and Northern Vancouver Island) had earlierbud burst on the southern test site, but earlier leaf drop, lower Nconcentrations and higher rates of N fixation on both sites(Fig. 2A). Allozyme analysis has also shown that families from Hai-da Gwaii and Northern and Western Vancouver Island cluster to-gether (Hamann et al., 1998). The phenological patterns weobserved, where northern families had earlier bud burst and leafdrop than southern families when planted at the same site, aresimilar to those shown in red alder by Hamann et al. (2011) andfor bud burst of northern deciduous trees in general (Li et al.,2003; Jensen and Hansen, 2008). Ager et al. (1993) found leafabscission in red alder from Washington and Oregon was stronglyrelated to the date of first fall frost at the seed source, and high ele-vation and more continental sources abscised leaves two weeksearlier than low elevation, coastal sources.

Differences in temperature and growing season length of thefamily locations of origin were important in driving trade-offs incold hardiness and growth between the two test sites (Fig. 2). Fam-ilies from northern regions were characterized by higher cold har-diness and growth at the northern test site, whereas families fromsouthern regions had lower cold hardiness, and poorer survival andgrowth at the northern site. Cannell et al. (1987) also found thatred alder’s autumn hardiness increases with the latitude of seedorigin. Thus, at both three (Hamann et al., 2000) and 17 years,red alder families from northern regions have greater height andsurvival at Terrace compared to southern test sites, and familiesfrom southern regions perform best at southern test sites, in asso-ciation with longer, warmer summers.

We did not detect family differences in long-term water useefficiency, as measured by the stable C isotope ratio of buds. Thisagrees with Dang et al. (1994), who found no significant difference

among red alder provenances in instantaneous water use effi-ciency. Measures of water use efficiency are influenced by both Cuptake and water loss, however, and investigation of stomatal con-trol in red alder showed northwestern B.C. provenances had lessstomatal sensitivity to water vapor pressure deficit than southeast-ern provenances (Dang et al., 1994). Earlier wilting has also beenobserved in northern provenances under drought conditions, com-pared to provenances from Vancouver Island (Hamann et al.,2011). Indices of available moisture (CMD and Eref) of the climateof family origin explained a large degree of variation in the physi-ological traits of families in our redundancy analysis (Fig. 2B). Thiscombined evidence of family differences in stomatal control andadaptation to water availability suggests that families from moist,humid sites with little moisture deficit would perform sub-opti-mally on dry sites.

In Douglas-fir, a conifer that commonly grows in associationwith red alder, adaptation is largely a consequence of a trade-offbetween selection for winter cold hardiness and high growth ratesin mild environments (Li and Adams, 1993; St Clair et al., 2005;Darychuk et al., 2012). Douglas-fir has strong genetic variation ingrowth associated with elevation, latitude, longitude and distanceto the ocean (St Clair et al., 2005). Although red alder has less var-iation in growth among provenances (Xie, 2008; Hamann et al.,2011), we observed a clear trade-off between growth and cold har-diness. Taller families on the milder Bowser site had lower coldhardiness. Both species appear to be under strong selection for coldhardiness and phenology. Interestingly, in Douglas-fir, genetic cor-relations between spring and fall cold injury are negative (Aitkenand Adams, 1995; O’Neill et al., 2001) and it has been recom-mended that spring and fall cold hardiness should be treated asseparate traits in that species (O’Neill et al., 2001). This contrastswith our results for red alder where family cold hardiness was sig-nificantly and positively correlated on all dates of assessment, indi-cating that the fundamental structure of genes controlling coldhardiness in the two species may differ. Unlike red alder, geneticvariation in water use efficiency exists in Douglas-fir (Zhanget al., 1993), but there is little evidence for a growth–drought har-diness trade-off in either species (St Clair et al., 2005; Darychuket al., 2012).

Family variation in N nutrition was significant, particularly onthe colder, wetter Terrace site. While genetic variation in parame-ters associated with N fixation has been demonstrated in crop spe-cies (Graham et al., 2004; Abi-Ghanem et al., 2011), work withalders is limited, and often focuses on variation among Frankiastrains rather than alder genotypes (Carpenter and Robertson,1984; Hooker and Wheeler, 1987; Markham, 2008). Cultivar differ-ences in nodule number and mass, speed of nodulation, acetylenereduction activity, and nodule enzyme production and functionhave been documented in clover, soybean, common bean, alfalfa,pea and lentil (Graham et al., 2004; Abi-Ghanem et al., 2011),and this same variation might be expected in red alder. Indicationsare that red alder naturally associates with a limited number ofFrankia genotypes, and forest age and management regime appearto be more significant in determining the Frankia genotype thangeographic location (Kennedy et al., 2010), thus variation in N fix-ation may be more affected by genetic variation in alder than inFrankia. However, Markham and Chanway (1999) found that ge-netic variation in both the alder and the Frankia strains affectedplant growth and N fixation. In our study, northern families fromenvironments with moist, cool summers had more bud N derivedfrom fixation and lower bud N concentrations, suggesting that pop-ulations from regions with wet, cool soils that limit N mineraliza-tion and uptake may have greater selection pressure for N fixationthan N uptake. Markham and Chanway (1999) also found that al-der seedlings from N-poor, high elevation sites had a greater pro-portion of N derived from fixation than did seedlings from N-rich

R.B. Porter et al. / Forest Ecology and Management 291 (2013) 357–366 365

sites when inoculated with an unfamiliar Frankia strain. These re-sults suggest that in favorable environments there may be selec-tion for a less effective symbiosis, thus potential exists for asynergistic matching of fast-growing alder families with high N-fixing Frankia strains.

4.1. Management implications

The physiological traits of red alder most tightly tied to the cli-mate of origin are autumn leaf drop, bud burst and cold hardiness.These traits, and to a lesser extent N fixation, are sensitive tochanges in continentality and moisture regime. For example, ifNorthern Vancouver Island families are grown on Northern Main-land sites with more extreme differences between summer andwinter and lower available moisture, our data suggest these fami-lies will be poorly adapted. Survival, growth and cold hardinesswere sensitive to changes in temperature regime and growing sea-son length. Ager et al. (1993) found temperature amplitude, a sim-ilar index to continentality, was highly correlated with the growthpotential of red alder from four river drainages in Washington andOregon, but in that study, phenology was most closely related tospring thermal sums and fall frost dates. In our study, some fami-lies, such as those from Haida Gwaii, show strong adaptation to rel-atively uniform annual temperatures and abundant availablemoisture. Haidai Gwaii families are slow-growing, but have highrates of N fixation, on average. Most families from the NorthernMainland are adapted to cooler temperatures and shorter growingseasons and have relatively high cold tolerance. Families fromsouthern regions are associated with warmer temperatures andlonger growing seasons and retain leaves later in the autumn.However, there are also a few families from the Georgia Depres-sion, Central Coast and Western Vancouver Island that load nearthe center of the RDA biplot (Fig. 2B) and therefore do not showstrong adaptation to the climatic conditions of seed origin. Whilemore test sites across red alder’s range and more families withinregions are needed to capture the full range of variation and confi-dently delineate seed zones for red alder, our results support thoseof Hamann et al. (2011) and indicate that four to six seed zones areappropriate for red alder within British Columbia, rather than thetwo seed zones (Xie, 2008) currently used for seed productionand deployment. With greater sample sizes and spatial coverage,multivariate functions of key climatic variables identified by theRDA could be used to define seed zones.

These results are relevant in the context of selection of familiesfor breeding programs and seed deployment strategies in the faceof climatic change. At present, red alder grows mainly at low ele-vations throughout the Coastal Western Hemlock biogeoclimaticzone of British Columbia. With warming climates, this zone is pre-dicted to shift upwards in elevation by over 300 m, but northwardsby only 69 km by the 2080s (Wang et al., 2012a). In contrast, bio-climate envelope models of population habitat for tree speciesfrom the Coastal Western Hemlock zone indicate much greaternorthwards shifts of optimal climate niches in the same period(Gray and Hamann, 2012). Most red alder families tested aretightly adapted to their climate of origin and are expected to per-form sub-optimally if planted in a contrasting climate or if local cli-mates change significantly, with traits such as phenology, coldhardiness, and height most likely to be affected. Our results suggestthat assisted migration of alder families in reforestation should berestricted to shifts in elevation rather than latitude, at least untilbioclimate envelope models for red alder can provide more infor-mation. Some red alder families appear to show high phenotypicplasticity, which should confer enhanced ability to acclimate to cli-matic differences. A few families are consistent, high performers incontrasting environments. These high-performing families are in-cluded in the base populations for the red alder breeding program

in British Columbia, and could be considered for planting over agreater range of elevation.

More generally, our results highlight the risk of assuming thatspecies with low overall genetic diversity have little regional adap-tation and that seed can be transferred across considerable dis-tances with limited concern. We demonstrate that importantdifferences in a variety of traits that confer critical adaptations tolocal climatic conditions are present in a species in which theymight not have been expected, given indices of genetic variation.Knowledge of adaptive genetic variation is critical to tree breedingprograms, and, given ongoing and projected future climate change,to any consideration of assisted migration. A solid understandingof current adaptive patterns is essential for designing managementstrategies for the future.

Acknowledgements

Funding for this work was provided by the Future Forest Eco-system Scientific Council, as part of the interdisciplinary projecttitled ‘‘Using red alder as an adaptation strategy to reduce environ-mental, social and economic risks of climate change in coastalB.C.’’. We thank Louise de Montigny of the B.C. Ministry of Forests,Range and Natural Resource Operations for spearheading this pro-ject and Craig Farnden for his administrative guidance. The invalu-able assistance of Chang-Yi Xie, Keith Bird, Lisa Hayton, and PeterOtt of the Tree Improvement Branch, and Dan Belisle of the KalumDistrict Office of the B.C. Ministry of Forests and Natural ResourceOperations is gratefully acknowledged. We thank Laura Gray forhelp with Fig. 1 and Joe Antos for constructive comments on themanuscript. T. Lacourse is supported by research grants fromNSERC and the Canadian Foundation for Innovation.

Appendix A. Supplementary material

Supplementary data associated with this article can be found,in the online version, at http://dx.doi.org/10.1016/j.foreco.2012.11.017.

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